The Impact of Dietary Transition Metals on Host-Bacterial Interactions
Open accessAbstract
Transition metals are required cofactors for many proteins that are critical for life, and their concentration within cells is carefully maintained to avoid both deficiency and toxicity. To defend against bacterial pathogens, vertebrate immune proteins sequester metals, in particular zinc, iron, and manganese, as a strategy to limit bacterial acquisition of these necessary nutrients in a process termed “nutritional immunity.” In response, bacteria have evolved elegant strategies to access metals and counteract this host defense. In mammals, metal abundance can drastically shift due to changes in dietary intake or absorption from the intestinal tract, disrupting the balance between host and pathogen in the fight for metals and altering susceptibility to disease. This review describes the current understanding of how dietary metals modulate host-microbe interactions and the subsequent impact on the outcome of disease.
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- Premisenone given
Hosts have evolved metal-sequestering mechanisms collectively called nutritional immunity to limit bacterial growth.
“To limit bacterial growth, hosts have evolved mechanisms to sequester metals in a process termed “nutritional immunity” (Figure 2).”
Quote in the paperSubstantial claim- Rests on an assumption: Bacteria require nutrient metals for essential biological processes.
- Rests on an assumption: Dietary metals are rapidly complexed to host-derived molecules, so bacteria must compete with hosts to obtain the metals they need to survive.
- Interpretationreasoning
Dietary metals can shift the distribution and function of the intestinal microbiota.
“Dietary metals, as a critical nutrient, also have the potential to shift the distribution and function of the microbiota.”
Quote in the paperSubstantial claim - Premisecitation
Neutrophils limit nutrient metal availability by releasing lactoferrin to sequester iron.
“Neutrophils further limit nutrient metal availability by releasing lactoferrin to sequester iron (Legrand et al., 2004)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Legrand et al., 2004 source
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- Interpretationreasoning
Redistribution of metals away from bacteria is a key contributor to host-pathogen interactions.
“Host control of metal availability underscores how the redistribution of metals away from bacteria represents a key contributor to host-pathogen interactions.”
Quote in the paperSubstantial claim - Premisecitation
Lipocalin-2 sequesters high-affinity metal-binding siderophores released by pathogenic bacteria, preventing their uptake.
“Lipocalin-2 sequesters the high affinity metal binding siderophore molecules released by pathogenic bacteria to prevent uptake (Xiao et al., 2017).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Xiao et al., 2017 source
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- Premisecitation
Calprotectin also binds ferrous iron, nickel, and copper in vitro.
“though recent reports revealed that calprotectin also binds ferrous iron, nickel, and copper in vitro (Besold et al., 2017; Nakashige et al., 2015; Nakashige et al., 2017).”
Quote in the paperNot a substantial claim0 of 3 sources checked - Premisecitation
Oxygen availability during inflammation drives dysbiosis by favoring Enterobacteriaceae expansion through respiration.
“For example, the availability of oxygen during inflammation drives a disruption, or dysbiosis, of the microbiota by favoring Enterobacteriaceae expansion through respiration (Byndloss et al., 2018).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Byndloss et al., 2018 source
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- Premisecitation
Neutrophils release calprotectin as granule components or as part of neutrophil extracellular traps.
“by releasing the antimicrobial protein calprotectin either as part of granules or as a component of neutrophil extracellular traps (Zackular et al., 2015).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Zackular et al., 2015 source
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- Premisecitation
During inflammation, IL-6 signals the liver to release hepcidin, which promotes iron accumulation in phagocytic cells by inducing degradation of the iron exporter ferroportin.
“during an inflammatory episode interleukin-6 (IL-6) signals to the liver to release the hormone hepcidin, which promotes iron accumulation in phagocytic cells by inducing degradation of the iron exporter ferroportin (Fpn1) (Nemeth et al., 2004).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Nemeth et al., 2004 source
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- Premisecitation
Infiltrating neutrophils and macrophages block bacterial iron acquisition in part by releasing lipocalin-2.
“Infiltrating neutrophils and macrophages block bacterial iron acquisition in part by releasing the protein lipocalin-2 (Xiao et al., 2017).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Xiao et al., 2017 source
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- Premisecitation
Patients receiving zinc supplementation to treat diarrhea have lessened diarrheal morbidity.
“In practice, patients receiving zinc supplementation to treat diarrhea have lessened diarrheal morbidity (Bhandari et al., 2002)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Bhandari et al., 2002 source
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- Premisecitation
Calprotectin primarily binds zinc and manganese during infection.
“Calprotectin primarily binds zinc and manganese during infection”
Quote in the paperNot a substantial claim0 of 3 sources checked - Interpretationreasoning
Low intestinal zinc may shift microbiota homeostasis away from beneficial bacteria such as A. muciniphila and a low-inflammatory environment toward expansion of pathogenic bacteria.
“Thus, low intestinal zinc may push microbiota homeostasis away from beneficial bacteria such as A. muciniphila and a low inflammatory environment to favor the expansion of pathogenic bacteria.”
Quote in the paperSubstantial claim - Premisecitation
Zinc deficiency is a risk factor for childhood diarrhea.
“For instance, zinc deficiency is a risk factor for childhood diarrhea (Walker et al., 2013)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Walker et al., 2013 source
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- Premisecitation
Even without other microbes, C. jejuni can steal iron directly from host lactoferrin and transferrin, a process called iron piracy.
“Even in the absence of other microbes, C. jejuni can steal iron directly from host lactoferrin and transferrin in a process termed iron piracy (Miller et al., 2008).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Miller et al., 2008 source
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- Premisecitation
Salmonella Typhimurium initially colonizes the intestines before invading through Peyer's patches to reach deeper tissues.
“The non-typhoidal Salmonella (NTS) serovar Salmonella Typhimurium initially colonizes the intestines before invading through Peyer’s patches to reach deeper tissues (Santos et al., 2009).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Santos et al., 2009 source
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- Premisecitation
Clostridium difficile typically does not cause disease in otherwise healthy individuals because the microbiota block colonization.
“The spore-forming Gram-positive bacterium Clostridium difficile typically does not cause disease in otherwise healthy individuals, as the microbiota effectively block C. difficile colonization (Theriot and Young, 2015)(Figure 3).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Theriot and Young, 2015
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- Premisecitation
S. Typhimurium bypasses calprotectin-dependent manganese sequestration using the cation transporters MntH, SitABCD, and ZupT.
“S. Typhimurium bypasses calprotectin-dependent manganese sequestration by the action of the cation transporters MntH, SitABCD, and ZupT (Diaz-Ochoa et al., 2016).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Diaz-Ochoa et al., 2016 source
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- Premisecitation
Campylobacter jejuni encodes genes for heme and iron uptake that are transcribed under iron-limited stress.
“Campylobacter jejuni encodes genes necessary for the uptake of heme and iron that are transcribed under iron-limited stress (Crofts et al., 2018).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Crofts et al., 2018 source
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- Premisecitation
Heme supplementation reduces the relative abundance of Firmicutes, which include beneficial butyrate-producing Clostridia.
“For instance, heme (an iron-containing porphyrin molecule) supplementation reduces the relative abundance of Firmicutes (Constante et al., 2017), which contain members from the beneficial butyrate-producing class Clostridia.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Constante et al., 2017 source
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- Premisecitation
Patients receiving zinc supplementation have a reduced risk of prolonged diarrheal episodes.
“and a reduced risk of prolonged diarrheal episodes (Sazawal et al., 1995).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Sazawal et al., 1995 source
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- Interpretationreasoning
Iron or heme supplementation increases susceptibility to Enterobacteriaceae and other enteric pathogens.
“It is then not surprising that iron or heme supplementation increases susceptibility to Enterobacteriaceae and other enteric pathogens.”
Quote in the paperSubstantial claim - Premisecitation
S. Typhimurium's ability to avoid lipocalin-2-mediated defenses provides a selective advantage during inflammation.
“The ability of S. Typhimurium to avoid lipocalin-2 mediated defenses provides a selective advantage during inflammation (Raffatellu et al., 2009).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Raffatellu et al., 2009 source
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- Interpretationnone given
Changes in metal absorption and transport can significantly affect disease beyond the intestines by altering immune cell physiology, metal localization, and bacterial access to metals.
“Yet, changes to metal absorption and transport can have a significant impact on disease beyond the intestines through alterations in immune cell physiology, metal localization, and bacterial access to metals.”
Quote in the paperNot a substantial claim - Premisecitation
In some studies, zinc deficiency in elderly individuals is associated with increased risk of pneumonia caused by Staphylococcus aureus, Streptococcus pneumoniae, Klebsiella pneumoniae, Legionella pneumophila, and Haemophilus influenzae.
“In some studies, zinc deficiency in elderly individuals is associated with an increased risk of pneumonia caused by Staphylococcus aureus, Streptococcus pneumoniae, Klebsiella pneumoniae, Legionella pneumophila, and Haemophilus influenzae (Barnett et al., 2010).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Barnett et al., 2010 source
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- Premisecitation
Antibiotics and chemotherapeutic agents disrupt microbiota-mediated colonization resistance and allow C. difficile to establish in the intestines.
“However, a variety of risk factors including exposure to antibiotics and chemotherapeutic agents disrupt microbiota-mediated colonization resistance and allow C. difficile to take hold in the intestines (Abou Chakra et al., 2014).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Abou Chakra et al., 2014 source
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- Interpretationreasoning
The timing of zinc supplementation is important: basal zinc deficiencies must be restored before, rather than during, infection to improve disease outcome.
“These data suggest that the timing of zinc supplementation is important, where basal zinc deficiencies must be restored prior to, rather than during, infection to improve disease outcome.”
Quote in the paperSubstantial claim - Premisecitation
Yersinia enterocolitica and Y. pseudotuberculosis encode uptake receptors for yersiniabactin and other siderophores to support their iron needs.
“Yersinia enterocolitica and Y. pseudotuberculosis encode uptake receptors for yersiniabactin and other siderophores to support their iron needs (Rakin et al., 2012).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Rakin et al., 2012 source
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- Premisecitation
Members of Enterobacteriaceae are more abundant after dietary heme treatment.
“Furthermore, members of the Enterobacteriaceae are found in greater abundance following dietary heme treatment (Constante et al., 2017).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Constante et al., 2017 source
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- Interpretationcitation
Dietary iron drives changes to the microbiota that may increase susceptibility to infection.
“Yet, studies examining the effects of dietary iron suggest iron drives changes to the microbiota that may result in increased susceptibility to infection ((Constante et al., 2017; Jaeggi et al., 2015); Figure 3).”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
In an OVA-induced allergic airway inflammation model, rats on low zinc diets have higher eosinophil, neutrophil, and monocyte migration to the lungs after an inflammatory insult.
“In an OVA-induced allergic airway inflammation model, rats on low zinc diets experience higher eosinophil, neutrophil, and monocyte migration to the lungs following an inflammatory insult (Lu et al., 2012).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Lu et al., 2012
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- Interpretationreasoning
Iron is a precious resource in the gut for both the microbiota and pathogenic bacteria.
“Overall, iron represents a precious resource in the gut for both the microbiota and pathogenic bacteria.”
Quote in the paperSubstantial claim - Premisereasoning
Manganese acquisition allows manganese-dependent superoxide dismutase and catalase to detoxify superoxide to water.
“Acquisition of manganese then allows catalysis by manganese-dependent superoxide dismutase and catalase to collectively detoxify superoxide to water.”
Quote in the paperSubstantial claim - Interpretationreasoning
A significant part of the host immune response relies on iron sequestration to slow pathogen growth and enable other immune branches to capture and kill invading microbes.
“A significant part of the host immune response relies on the sequestration of iron to slow pathogen growth enabling other branches of the immune system to capture and kill invading microbes.”
Quote in the paperSubstantial claim - Premisecitation
Without further insult, the high-zinc dysbiotic community retains colonization resistance against C. difficile.
“Without further insult, this dysbiotic community retains colonization resistance against C. difficile.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Zackular et al., 2016 source
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- Premisecitation
The increased immune cell migration in low-zinc rats is reversed by zinc supplementation.
“These effects are reversed upon zinc supplementation”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Liu et al., 2013 source
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- Premisecitation
NRAMP1 in the Salmonella-containing vacuole pumps nutrient metals, including manganese, out of the vacuole to starve S. Typhimurium and limit its growth.
“The cation transporter NRAMP1 localized within the SCV is responsible for pumping nutrient metals, including manganese, out of the SCV to starve S. Typhimurium and limit growth (Loomis et al., 2014).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Loomis et al., 2014 source
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- Interpretationcitation
Manganese transport and its roles in colonization and virulence in other enteric pathogens are less well known but probably play similar critical roles as in S. Typhimurium.
“Manganese transport and its roles in colonization and virulence in other enteric pathogens are less well known but presumably play similar critical roles as seen in S. Typhimurium (Juttukonda and Skaar, 2015).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Juttukonda and Skaar, 2015
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- Premisecitation
In mice, high dietary zinc generates dysbiosis favoring expansion of Enterococcus, Porphorymonadaceae, Lachnospiraceae, and Clostridia XI while limiting Turicibacter.
“In mice, high dietary zinc generates a dysbiosis that favors expansion of Enterococcus, Porphorymonadaceae, Lachnospiraceae, and Clostridia XI while limiting the population of Turicibacter (Zackular et al., 2016).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Zackular et al., 2016 source
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- Interpretationreasoning
Iron supplementation to treat Plasmodium-induced anemia may subvert the host response by giving NTS access to higher intracellular iron, allowing the bacteria to reduce iron-acquisition energy expenditure and devote resources to replication.
“Iron supplementation to treat Plasmodium-induced anemia may subvert the host response by providing NTS access to higher intracellular iron, allowing the bacteria to decrease energy expenditure on iron acquisition and devote resources to replication.”
Quote in the paperSubstantial claim - Premisecitation
Five months of dietary iron supplementation restored hemoglobin levels of iron-deficient Kenyan girls to levels similar to iron-replete girls.
“A study in Kenyan girls found that 5 months of dietary iron supplementation could restore hemoglobin levels of iron-deficient girls to levels similar to iron-replete girls.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Leenstra et al., 2009 source
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- Premisecitation
Iron-replete girls were at increased risk of infection with the malarial parasite Plasmodium.
“However, iron-replete girls were at an increased risk of infection with the malarial parasite Plasmodium (Leenstra et al., 2009)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Leenstra et al., 2009 source
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- Premisecitation
Even with M. tuberculosis iron-acquisition factors, macrophage iron withholding effectively limits bacterial growth.
“Even with the expression of M. tuberculosis iron-acquisition factors, macrophage iron withholding effectively aids in limiting bacterial growth (Schaible et al., 2002).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Schaible et al., 2002 source
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- Premisecitation
Infected macrophages respond by increasing Fpn1 and lipocalin 2 expression, which limits NTS replication.
“To counteract the iron scavenging of the pathogen, infected macrophages respond by increasing Fpn1 and lipocalin 2 expression, which effectively limits NTS replication (Nairz et al., 2007).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Nairz et al., 2007 source
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- Premisecitation
African iron loading is positively correlated with increased risk of death from Mycobacterium tuberculosis.
“This iron loading is positively correlated with an increased risk of death from the causative agent of tuberculosis, Mycobacterium tuberculosis (Cronje and Bornman, 2005).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Cronje and Bornman, 2005
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- Premisecitation
Staphylococcus aureus acquires iron through toxin-dependent lysis of red blood cells followed by heme uptake through the iron-regulated surface determinant system.
“S. aureus is well equipped to acquire iron through the toxin-dependent lysis of red blood cells followed by the uptake of heme through the iron-regulated surface determinant (Isd) system (Grigg et al., 2010).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Grigg et al., 2010 source
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- Interpretationreasoning
Iron loading bypasses metal restriction by providing M. tuberculosis an iron-replete intracellular environment.
“However, iron-loading bypasses metal restriction by providing M. tuberculosis an iron-replete intracellular environment.”
Quote in the paperSubstantial claim - Interpretationreasoning
An inadequate supply of zinc available to invading pathogens should negatively influence bacterial survival.
“However, an inadequate supply of zinc available to invading pathogens should also negatively influence bacterial survival.”
Quote in the paperSubstantial claim - Premisecitation
NTS within phagocytic cells acquires ferrous and ferric iron by upregulating FeoB or FepB and the siderophores enterochelin and salmochelin.
“Once infected, NTS within phagocytic cells acquires ferrous and ferric iron by upregulating expression of the iron importers FeoB or FepB, respectively, (Nagy et al., 2014) and the siderophores enterochelin and salmochelin (Nagy et al., 2013).”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
Hypercalprotectinaemia is associated with increased incidence of recurrent infections.
“however hypercalprotectinaemia, in which patients have excessive serum calprotectin, is associated with increased incidence of recurrent infections (Sampson et al., 2002).”
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- Premisecitation
Acinetobacter baumannii encodes several mechanisms to ensure zinc bioavailability.
“For instance, the nosocomial Gram-negative bacterium Acinetobacter baumannii encodes several mechanisms to ensure zinc bioavailability (Mortensen and Skaar, 2013).”
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- Premisecitation
The ability to overcome host-mediated zinc sequestration is a shared feature of respiratory pathogens including A. baumannii, P. aeruginosa, K. pneumoniae, and S. pneumoniae.
“The ability to overcome host-mediated zinc sequestration is a shared feature of respiratory pathogens including A. baumannii, P. aeruginosa, K. pneumoniae, and S. pneumoniae (Achouiti et al., 2012; Dintilhac et al., 1997; Nairn et al., 2016; Pederick et al., 2015)”
Quote in the paperNot a substantial claim0 of 3 sources checked - Premisecitation
Pseudomonas aeruginosa expresses a ZnuABC zinc transporter under zinc-deplete conditions.
“Pseudomonas aeruginosa, a soil bacterium that commonly colonizes the respiratory tract of cystic fibrosis patients, also expresses a ZnuABC zinc transporter under zinc-deplete conditions (Pederick et al., 2015).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Pederick et al., 2015 source
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- Interpretationreasoning
Excess iron supplementation could undermine efforts to correct malaria-induced anemia by increasing the risk of NTS bacteremia.
“Together, these studies suggest excess iron supplementation could upset efforts to correct malaria-induced anemia by increasing risks for NTS bacteremia, as others have suggested (van Santen et al., 2013), but more work is needed to clarify these relationships.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites van Santen et al., 2013 source
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- Interpretationnone given
Adequate zinc intake and absorption are important for proper immune cell function, including metal sequestration to limit bacterial access.
“Adequate zinc intake and absorption is important to maintain proper immune cell function, which includes sequestering the metal to limit bacterial access.”
Quote in the paperSubstantial claim - Interpretationreasoning
Zinc deficiency may increase susceptibility to infection through immune dysregulation.
“As a result, zinc deficiency may drive increased susceptibility to infection because of immune dysregulation.”
Quote in the paperNot a substantial claim - Interpretationreasoning
Bacterial virulence factors that compete with the host for zinc contribute significantly to pathogenesis.
“This suggests that bacterial virulence factors that compete with the host for zinc contributes significantly to pathogenesis.”
Quote in the paperNot a substantial claim - Premisecitation
Plasmodium acquires iron from heme largely through lysis of red blood cells.
“which acquires iron from heme largely through lysis of red blood cells (Akinosoglou et al., 2012).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Akinosoglou et al., 2012 source
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- Premisecitation
The A. baumannii Zur regulon includes HutH, which liberates zinc from histidine and forms a labile zinc pool under zinc-deplete conditions.
“Also included in the A. baumannii Zur regulon is a histidine ammonia lysase HutH that liberates zinc from histidine and forms a labile zinc pool under zinc-deplete conditions (Nairn et al., 2016).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Nairn et al., 2016 source
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- Interpretationreasoning
Increasing iron availability in the form of hemoglobin may promote bacterial overgrowth at systemic sites.
“However, increasing iron availability in the form of hemoglobin may also promote bacteria overgrowth at systemic sites.”
Quote in the paperSubstantial claim - Interpretationreasoning
The redundant zinc acquisition mechanisms of P. aeruginosa show that zinc is critical for pathogen survival in the host environment.
“The redundant mechanisms used by P. aeruginosa to acquire zinc illustrates how critical the metal is to survival of the pathogen within a host environment.”
Quote in the paperSubstantial claim - Interpretationnone given
Systemic zinc status affects multiple aspects of immunity.
“Systemic zinc status affects multiple aspects of immunity.”
Quote in the paperSubstantial claim - Interpretationreasoning
The clinical association between high dietary iron and increased M. tuberculosis death risk suggests that increased T-cell recruitment alone is not sufficient to overcome iron-mediated disruption of other immune responses.
“Yet, the clinical associations between high dietary iron and the risk of death from M. tuberculosis suggests an increase in T-cell recruitment alone is not sufficient to overcome iron-mediated disruption to other aspects of the immune response.”
Quote in the paperSubstantial claim - Premisecitation
Not all studies find significant associations between iron supplementation and increased malaria risk.
“While not all studies find significant associations between iron supplementation and increased malaria risk (Spottiswoode et al., 2014)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Spottiswoode et al., 2014 source
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- Premisecitation
Iron deficiency is associated with increased risk of gastric cancer.
“Iron deficiency is associated with an increased risk of gastric cancer (Cover and Peek, 2013).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Cover and Peek, 2013
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- Premisecitation
Excess manganese raises pro-inflammatory cytokine expression in macrophages.
“manganese excess increases expression of pro-inflammatory cytokines from neuron-associated glial cells (Dodd and Filipov, 2011) and macrophages (Mokgobu et al., 2015)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Mokgobu et al., 2015 source
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- Premisecitation
In a mouse model of systemic S. aureus infection, a high-manganese diet increases bacterial burdens in the heart.
“In a mouse model of systemic S. aureus infection, high dietary manganese leads to increased bacterial burdens in the heart and enhanced bacterial virulence (Juttukonda et al., 2017).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Juttukonda et al., 2017 source
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- Premisecitation
Excess manganese boosts macrophage activity.
“as well as enhances natural killer cell (Rogers et al., 1983) and macrophage activity (Smialowicz et al., 1985)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Smialowicz et al., 1985 source
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- Premisecitation
In animal models, copper deficiency reduces macrophage-mediated killing of S. pneumoniae, M. tuberculosis, P. haemolytica, and S. Typhimurium.
“In animal models copper deficiency limits macrophage-mediated bactericidal killing against S. pneumoniae, M. tuberculosis, P. haemolytica, and S. Typhimurium (Johnson et al., 2015; Jones and Suttle, 1983; Newberne et al., 1968; Wolschendorf et al., 2011).”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationreasoning
S. aureus's ability to use heme as an iron source is delicately balanced against heme's potential toxicity.
“The ability of S. aureus to use heme as an iron source is then delicately balanced against its potential toxicity.”
Quote in the paperNot a substantial claim - Interpretationreasoning
Optimal immune function requires metal levels to be balanced.
“exemplifying how balancing metal levels is necessary for optimum immune function”
Quote in the paperSubstantial claim - Premisecitation
Bacteria have developed ways to counter host copper stress, including copper exporters.
“In response, bacteria have evolved mechanisms to relieve host-mediated copper stress including copper exporters (Johnson et al., 2015).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Johnson et al., 2015 source
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- Premisecitation
Iron deficiency increases H. pylori expression of the Cag pathogenicity island, which encodes a type 4 secretion system used to deliver CagA into host cells.
“In either case, iron deficiency increases H. pylori expression of the Cag pathogenicity island that encodes for a type 4 secretion system used to deliver CagA into host cells (Merrell et al., 2003).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Merrell et al., 2003 source
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- Premisecitation
Excess manganese boosts natural killer cell activity.
“as well as enhances natural killer cell (Rogers et al., 1983) and macrophage activity (Smialowicz et al., 1985)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Rogers et al., 1983 source
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- Premisecitation
Helicobacter pylori infection exacerbates carcinogenesis by increasing pathogen virulence.
“While there are likely multiple mechanisms linking iron deficiency to cancer development, infection with the Gram-negative bacterium Helicobacter pylori exacerbates carcinogenesis by increasing pathogen virulence (Noto et al., 2013).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Noto et al., 2013 source
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- Interpretationnone given
Iron deficiency suppresses multiple arms of the immune response.
“As mentioned previously, iron deficiency suppresses multiple arms of the immune response.”
Quote in the paperSubstantial claim - Interpretationreasoning
S. aureus heme utilization and detoxification mechanisms illustrate why dietary interventions to restore hemoglobin in iron deficiency anemia should be approached cautiously to avoid promoting bacterial growth.
“S. aureus heme utilization and detoxification mechanisms provide an example of why dietary interventions to restore hemoglobin levels in iron deficiency anemia should be cautiously approached to avoid promoting bacterial growth.”
Quote in the paperSubstantial claim - Interpretationcitation
Copper deficiency is likely to influence host-pathogen interactions.
“Copper deficiencies are most likely to affect host-pathogen interactions”
Quote in the paperSubstantial claim- Rests on an assumption: Copper, nickel, cobalt, and molybdenum come from the diet and are needed for several cellular processes.
- Premisecitation
CagA drives the relocation of transferrin receptors to the apical surface, where H. pylori resides, from their normal basolateral position.
“CagA causes the mislocalization of transferrin receptors from the basolateral membrane to the apical surface where the pathogen is located (Tan et al., 2011).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Tan et al., 2011 source
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- Premisecitation
In S. aureus infection, neutrophils are critical innate defenders that exhibit impaired killing under iron limitation.
“As an example, in S. aureus infection neutrophils are critical innate defenders that exhibit impaired killing capacities under iron limitation (Moore and Humbert, 1984).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Moore and Humbert, 1984
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- Interpretationreasoning
Evidence suggests a connection between dietary manganese and nutritional immunity.
“but evidence points to a link between dietary manganese and nutritional immunity”
Quote in the paperSubstantial claim - Premisecitation
High manganese suppresses lymphocyte proliferation.
“However, high manganese also inhibits lymphocyte proliferation (Hart, 1978)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Hart, 1978 source
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- Premisecitation
An iron-limited diet in hereditary hemochromatosis patients reduces overall V. vulnificus bacterial burden.
“In accordance with increased iron availability in the blood improving bacterial survival, an iron-limited diet in hereditary hemochromatosis patients reduces the overall V. vulnificus bacterial burden (Arezes et al., 2015).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Arezes et al., 2015 source
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- Premisecitation
In E. coli, part of this copper toxicity comes from copper binding to the FeS cluster assembly protein IscA and blocking FeS assembly.
“that in E. coli is mediated in part through binding to FeS cluster assembly protein IscA and inhibiting FeS assembly (Tan et al., 2014)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Tan et al., 2014 source
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- Interpretationnone given
Hereditary hemochromatosis may benefit the host response to intracellular bacteria by limiting intracellular iron availability.
“However, hereditary hemochromatosis may benefit the host response to intracellular bacteria by limiting intracellular iron availability.”
Quote in the paperNot a substantial claim - Premisecitation
Bacterial nitric oxide synthase protects S. aureus from heme-induced oxidative stress.
“In addition, bacterial nitric oxide synthase (bNOS) protects S. aureus from heme-induced oxidative stress (Surdel et al., 2016).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Surdel et al., 2016 source
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- Interpretationreasoning
Iron supplementation to improve neutrophil bactericidal activity may balance the potential for enhanced S. aureus growth.
“Therefore, iron supplementation to improve neutrophil bactericidal activities may balance the potential for enhanced S. aureus growth.”
Quote in the paperSubstantial claim - Premisecitation
Copper is part of ferroxidases such as ceruloplasm and hephaestin, which convert iron(II) to iron(III).
“Additionally, copper is a component of ferroxidases, such as ceruloplasm and hephaestin, that oxidize iron(II) to iron(III) (Vashchenko and MacGillivray, 2013).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Vashchenko and MacGillivray, 2013
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- Premisecitation
In that mouse model, a high-manganese diet increases bacterial virulence.
“In a mouse model of systemic S. aureus infection, high dietary manganese leads to increased bacterial burdens in the heart and enhanced bacterial virulence (Juttukonda et al., 2017).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Juttukonda et al., 2017 source
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- Interpretationreasoning
Treatment options targeting iron homeostasis depend heavily on host genetic factors and the pathogenic lifestyle of the bacteria.
“Treatment options targeting iron homeostasis are thus highly dependent on host genetic factors and the pathogenic lifestyle of the bacteria.”
Quote in the paperSubstantial claim - Premisecitation
Excess manganese raises pro-inflammatory cytokine expression in glial cells associated with neurons.
“manganese excess increases expression of pro-inflammatory cytokines from neuron-associated glial cells (Dodd and Filipov, 2011)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Dodd and Filipov, 2011
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- Premisecitation
Heme challenges S. aureus because electron shuttling through heme and quinone molecules in the bacterial cell membrane generates damaging superoxide.
“However heme presents its own challenge for S. aureus as electron shuttling through heme and quinone molecules in the bacterial cell membrane result in the generation of damaging superoxide molecules (Wakeman et al., 2012).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Wakeman et al., 2012 source
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- Premisecitation
Zinc, iron, and manganese are the transition metals most commonly used as critical cofactors or structural components in mammalian and bacterial proteins.
“Zinc, iron, and manganese are the most common transition metals serving critical cofactor or structural roles in mammalian and bacterial proteins (Andreini et al., 2008).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Andreini et al., 2008 source
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- Premisecitation
H. pylori alters host iron metabolism when iron is scarce, aiding its survival in the stomach.
“H. pylori subsequently acquires iron from transferrin and reveals how H. pylori manipulates host iron metabolism under iron-deplete conditions to promote survival in the stomach.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Tan et al., 2011 source
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- Premisecitation
H. pylori obtains iron from transferrin.
“H. pylori subsequently acquires iron from transferrin”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Tan et al., 2011 source
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- Interpretationreasoning
Many studies have shown associations between metal deficiency or overload and susceptibility to bacterial infection.
“While several studies have elucidated associations between metal deficiencies or overloads with susceptibility to bacterial infection”
Quote in the paperSubstantial claim- Rests on an assumption: Associations between H. pylori, gastric cancer, and iron deficiency are well established.
- Interpretationnone given
During infection, multiple metal pools fluctuate.
“Furthermore, during infection multiple metal pools are in a state of flux”
Quote in the paperSubstantial claim - Premisecitation
Molybdenum, as part of the molybdenum cofactor with pterin, is required for reductases and dehydrogenases in bacterial respiration that are important during Enterobacteriaceae infection.
“Molybdenum, when complexed with a pterin molecule to form a molybdenum cofactor, is necessary for the catalytic activity of reductases and dehydrogenases in bacterial respiration that are critical during infection by the Enterobacteriaceae (Lopez et al., 2016).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Lopez et al., 2016 source
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- Interpretationnone given
These adverse effects depend on immune status and genetic factors.
“and are dependent on immune status and genetic factors”
Quote in the paperNot a substantial claim - Interpretationreasoning
Disrupting this balance harms the survival of both hosts and microbes.
“with disturbance of this balance causing repercussions for the survival of both parties”
Quote in the paperSubstantial claim - Interpretationreasoning
Attempts to correct developmental or neurological problems from metal imbalances by changing diet often cause harm by undermining nutritional immunity.
“Complicating matters, efforts to correct the developmental or neurological abnormalities of metal imbalances through changing dietary intake quite often have adverse effects by subverting nutritional immunity”
Quote in the paperSubstantial claim- Rests on an assumption: The link between dietary manganese and susceptibility to infectious disease is poorly understood.
- Rests on an assumption: Copper, nickel, cobalt, and molybdenum come from the diet and are needed for several cellular processes.
- Interpretationnone given
Mammalian nutrition is strongly linked to susceptibility to infectious disease.
“There is undoubtedly a strong connection between mammalian nutrition and susceptibility to infectious disease.”
Quote in the paperNot a substantial claim- Rests on an assumption: The link between dietary manganese and susceptibility to infectious disease is poorly understood.
- Rests on an assumption: Other metals, despite being less abundant, are essential for life.
- Rests on an assumption: Copper, nickel, cobalt, and molybdenum come from the diet and are needed for several cellular processes.
- Rests on an assumption: Nickel, cobalt, and molybdenum are important in many bacterial enzymes.
- Rests on an assumption: Associations between H. pylori, gastric cancer, and iron deficiency are well established.
- Rests on an assumption: It is unclear how the inflammatory environment caused by high dietary manganese affects susceptibility to bacterial colonization.
- Interpretationreasoning
Maintaining a balance between metal deficiency and toxicity requires coordinated action by both mammals and microbes.
“Striking a balance between metal deficiency and toxicity requires coordinated efforts for both mammals and microbes”
Quote in the paperSubstantial claim - Interpretationnone given
The mechanisms behind increased susceptibility are often unclear.
“often the mechanisms leading to increased susceptibility are not as clear”
Quote in the paperSubstantial claim
- Classified as probably not a substantial claim. 9
- May combine two claims. 67
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PremisereasoningCellular transition metal levels must be tightly regulated because these metals are toxic at high concentrations.
“Despite their importance to numerous cellular processes, transition metals are toxic at high concentrations. Thus, transition metal levels inside the cell must be tightly controlled to maintain homeostasis.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationEnteroaggregative E. coli is the main causative agent of traveler's diarrhea and encodes virulence factors that allow attachment to and aggregation on the intestinal epithelium.
“Enteroaggregative E. coli (EAEC), the main causative agent of traveler’s diarrhea, encodes virulence factors that allow the pathogen to attach to and aggregate on the intestinal epithelium (Okhuysen and Dupont, 2010).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Okhuysen and Dupont, 2010
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PremisecitationResource availability strongly shapes population structure, and limiting resources drive competition between species and individuals.
“As with any ecosystem, resource availability is a strong force dictating population structure, with limiting resources driving competition between species and even individuals (Hornung et al., 2018).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Hornung et al., 2018
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PremisecitationMost known enzymes use at least one metal cofactor, and zinc is the most frequent enzyme-associated transition metal, followed by iron and manganese.
“Nearly 60% of known enzymes contain at least one metal cofactor, with zinc being the most common enzyme-associated transition metal ion followed by iron and manganese (Andreini et al., 2008).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Andreini et al., 2008
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PremisecitationDietary zinc supplementation reverses EAEC disease progression, inhibits EAEC adherence and biofilm formation, and reduces epithelial pro-inflammatory cytokine production.
“Consistently, dietary zinc supplementation reverses disease progression, inhibits EAEC adherence and biofilm formation, and reduces epithelial production of pro-inflammatory cytokines (Medeiros et al., 2013).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Medeiros et al., 2013
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PremisecitationZinc deficiency stresses EAEC and increases expression of virulence factors, including toxins that worsen diarrheal episodes and weight loss.
“Zinc deficiency serves as a stressor for EAEC and leads to increased expression of virulence factors, including toxins that worsen diarrheal episodes and exaggerate weight loss (Bolick et al., 2014).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Bolick et al., 2014
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PremisecitationZinc deficiency is correlated with lower relative abundances of Clostridiales and Verrucomicrobia and higher abundances of Enterobacteriaceae and Enterococcus.
“Specifically, zinc deficiency is correlated with low relative abundances of Clostridiales and Verrucomicrobia populations and concomitant increases in Enterobacteriaceae and Enterococcus (Reed et al., 2015; Starke et al., 2014).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Reed et al., 2015
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- cites Starke et al., 2014
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PremisecitationHigh levels of Akkermansia muciniphila are associated with low inflammation and normal lipid and carbohydrate metabolism.
“High levels of Akkermansia muciniphila, a member of the Verrucomicrobia, is associated with low inflammation and normal lipid and carbohydrate metabolism (Dao et al., 2016; Schneeberger et al., 2015)”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Dao et al., 2016 source
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- cites Schneeberger et al., 2015
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PremisecitationEnteropathogenic E. coli exposed to high dietary zinc experiences cell envelope stress and reduced expression of the LEE pathogenicity island.
“Another virulent E. coli, enteropathogenic E. coli (EPEC), experiences cell envelope stress and reduced expression of the main virulence factor, the locus of enterocyte effacement (LEE) pathogenicity island, upon exposure to high dietary zinc (Xue et al., 2015).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Xue et al., 2015
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InterpretationreasoningExcess zinc intake could disrupt gut microbial populations and predispose individuals to infection.
“While zinc supplementation is essential for zinc-deficient individuals, excess zinc intake could disrupt the balance of gut microbial populations and predispose individuals to infection.”
Quote in the paperSubstantial claimMay combine two claims.
PremisereasoningIn the intestinal lumen, calprotectin competes with pathogens for manganese and represses the bacterial response to superoxide radicals.
“In the intestinal lumen, calprotectin competes with pathogens for manganese and represses the bacterial response to superoxide radicals.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationZinc supplementation can improve host resistance to infection, but in some cases it fails to correct impairments in the immune response.
“While zinc supplementation can improve host resistance to infection, in some cases it fails to correct impairments in the immune response (Yuan et al., 2016).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Yuan et al., 2016
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PremisecitationS. Typhimurium increases expression of the manganese and iron transporter SitABCD, which is required for full virulence.
“In response, S. Typhimurium increases expression of the manganese and iron transporter SitABCD, which is required for full virulence (Boyer et al., 2002; Janakiraman and Slauch, 2000).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Boyer et al., 2002 source
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- cites Janakiraman and Slauch, 2000
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PremisecitationS. Typhimurium increases expression of iron transport systems required for full virulence, in part by supplying iron to FeS clusters needed for respiration.
“S. Typhimurium also increases expression of iron transport systems required for full virulence (Boyer et al., 2002; Janakiraman and Slauch, 2000) in part by providing iron to iron-sulfur (FeS) clusters necessary for respiration (Byndloss et al., 2018).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Boyer et al., 2002 source
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- cites Janakiraman and Slauch, 2000
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- cites Byndloss et al., 2018
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InterpretationcitationZinc may have anti-inflammatory properties and limit collateral damage during inflammation.
“and suggest that zinc may have anti-inflammatory properties and limit collateral damage during inflammation (Liu et al., 2013).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Liu et al., 2013
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PremisecitationDuring Salmonella-induced inflammation, the host releases lactoferrin to sequester iron and lipocalin-2 to bind bacterial siderophores and undermine bacterial iron acquisition.
“During Salmonella-induced inflammation, the host releases lactoferrin to sequester iron and lipocalin-2 to bind bacterial siderophores and undermine bacterial iron acquisition (Raffatellu et al., 2009).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Raffatellu et al., 2009 source
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InterpretationreasoningC. jejuni may benefit from siderophores produced by other bacteria, suggesting a form of bacterial commensalism.
“This suggests a type of bacterial commensalism where C. jejuni benefits from the energy expended by other bacteria to produce siderophores.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationDietary iron has less than 20% absorption efficiency, leaving most ingested iron in the intestinal lumen for the microbiota.
“Dietary iron has less than 20% absorption efficiency leaving the bulk of iron intake within the intestinal lumen to the microbiota (Jaeggi et al., 2015).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Jaeggi et al., 2015 source
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PremisecitationManganese is a required coenzyme for some superoxide dismutases that detoxify bactericidal superoxide radicals generated during inflammation, making it important for pathogens after immune stimulation.
“Manganese is a required coenzyme for some superoxide dismutases in the detoxification of bactericidal superoxide radicals (Damo et al., 2012) generated during inflammation and as such is important for pathogens after stimulating an immune response.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Damo et al., 2012
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PremisecitationThe high-zinc dysbiotic community becomes more susceptible to antibiotics, so lower doses are needed to overcome colonization resistance and allow C. difficile colonization.
“Yet, the new community structure becomes more susceptible to antibiotics, thus lower doses are needed to overcome colonization resistance and allow C. difficile to colonize (Zackular et al., 2016).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Zackular et al., 2016
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PremisecitationIn rats, oral iron administration increases Ruminococcaceae, Defluvitalaceae, and Coprococcus and decreases Lachnospiraceae.
“In rats, oral iron administration leads to increased representation of Ruminococcaceae, Defluvitalaceae, and Coprococcus, as well as decreased representation of Lachnospiraceae (Fang et al., 2018).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Fang et al., 2018
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PremisecitationIn patients with low enteric pathogen burdens, iron supplementation effects on the gut range from marginally impactful to beneficial through increased fecal short-chain fatty acids and lowered inflammation.
“In cases where patients naturally have low enteric pathogen burdens, the effects of iron supplementation on the gut ranges from marginally impactful (Dostal et al., 2014a) to beneficial through increasing fecal concentrations of anti-inflammatory short chain fatty acids (Dostal et al., 2014b) and lowering inflammation (Kortman et al., 2015).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Dostal et al., 2014a
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- cites Dostal et al., 2014b
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- cites Kortman et al., 2015
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PremisecitationC. jejuni can bind and take up enterobactin but does not encode the machinery to produce siderophores.
“C. jejuni can also bind and uptake enterobactin; however, it does not encode the machinery to produce siderophores (Xu et al., 2010).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Xu et al., 2010
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PremisecitationEcN outcompetes and suppresses S. Typhimurium colonization in an iron-dependent manner and only when lipocalin-2 is present.
“EcN is able to outcompete and suppress S. Typhimurium colonization in an iron-dependent manner and only in the presence of lipocalin-2 (Deriu et al., 2013)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Deriu et al., 2013 source
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PremisecitationLow dietary zinc is associated with lowered antibody titers, reduced lymphocyte proliferation, and reduced circulating T lymphocytes, CD4+ memory T cells, and naïve T cells.
“where low zinc is associated with lowered antibody titers (Girodon et al., 1999), reduced lymphocyte proliferation, and reduced levels of circulating T lymphocytes, CD4+ memory T cells, and naïve T cells (Barnett et al., 2010; Fraker and King, 2004).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Girodon et al., 1999
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- cites Barnett et al., 2010
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- cites Fraker and King, 2004
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PremisecitationButyrate production is associated with increased regulatory T-cell differentiation and lowered inflammation.
“Butyrate production is associated with increased differentiation of regulatory T-cells and lowered inflammation (Sun et al., 2017).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Sun et al., 2017
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InterpretationreasoningAltering manganese availability in the intestines likely drives bacterial population shifts that may compromise microbiota function and host health.
“It is unknown how dietary manganese deficiency or excess in humans affects the gut population but as with other necessary nutrients it is likely that altering manganese availability within the intestines drives bacterial population shifts that may compromise microbiota function and host health.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationIn children, zinc supplementation to correct zinc deficiency is reported to lower median time to recovery from severe pneumonia, though some studies found no benefit.
“In children, zinc supplementation to correct zinc deficiency is reported to lower the median time to recovery from severe pneumonia, though it is important to note that some studies found no benefit to zinc supplementation (Basnet et al., 2015).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Basnet et al., 2015
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PremisecitationS. Typhimurium produces the stealth siderophore salmochelin, whose additional glycosylation moiety prevents lipocalin-2 binding.
“To subvert host nutritional immunity, S. Typhimurium produces the stealth siderophore salmochelin that includes an additional glycosylation moiety (Fischbach et al., 2006) that prevents lipocalin-2 binding.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Fischbach et al., 2006
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PremisecitationZinc deficiency is correlated with increased risk of lung infection and arises from low zinc intake and consumption of foods high in zinc-sequestering phytates and fiber, affecting nearly a third of the world's population.
“Zinc deficiency is correlated with an increased risk of lung infection and arises from both low zinc intake and consumption of foods high in zinc-sequestering phytates and fiber to affect nearly a third of the world’s population (Wessells and Brown, 2012).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Wessells and Brown, 2012
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PremisecitationE. coli Nissle 1917 encodes mechanisms to take up exogenous iron and heme and to use the siderophores yersiniabactin, aerobactin, and salmochelin.
“The probiotic bacterium E. coli Nissle 1917 (EcN) encodes mechanisms to uptake exogenous iron and heme as well as the siderophores yersiniabactin, aerobactin, and salmochelin (Deriu et al., 2013).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Deriu et al., 2013 source
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PremisecitationHemoglobin holds a significant portion of the body's iron, and restoring hemoglobin via dietary or parenteral nutrition in iron-deficiency anemia patients is common.
“Hemoglobin holds a significant portion of the body’s iron and restoring hemoglobin levels via dietary or parenteral nutrition in iron-deficiency anemia patients is a common practice (Camaschella, 2015).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Camaschella, 2015
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PremisecitationDietary African iron loading is characterized by high intracellular macrophage iron due to leaching from drinking containers and is enhanced in individuals with an Fpn1 mutation.
“Dietary African iron loading is a condition characterized by high concentrations of intracellular macrophage iron due to leaching from drinking containers that is enhanced in individuals with a genetic predisposition based on a Fpn1 mutation (Gordeuk et al., 2003).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Gordeuk et al., 2003
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PremisecitationWithin alveolar macrophages, M. tuberculosis experiences iron starvation and upregulates metal import genes and releases the siderophore mycobactin.
“Within alveolar macrophages, M. tuberculosis experiences iron starvation and, in response, upregulates genes involved in metal import (Dubnau et al., 2005) and releases the siderophore mycobactin (De Voss et al., 2000).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Dubnau et al., 2005
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- cites De Voss et al., 2000 source
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PremisecitationPseudomonas biofilms are negatively charged due to extracellular DNA and chelate positively charged divalent metal ions, including zinc, to promote bacterial virulence and survival.
“Pseudomonas biofilms are negatively charged owing to extracellular DNA and chelate positively charged divalent metal ions, including zinc, to promote bacterial virulence and survival (Mulcahy et al., 2008).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Mulcahy et al., 2008
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PremisecitationEthanol-induced zinc deficiency in macrophages leads to impaired phagocytosis, suggesting zinc deficiency may prevent adequate pathogen clearance.
“However, zinc deficiency may prevent adequate pathogen clearance, as ethanol-induced zinc-deficiency in macrophages leads to impaired phagocytosis (Konomi et al., 2015).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Konomi et al., 2015
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PremisecitationIron deficiency has complex effects on macrophage function and bactericidal radical formation: low iron reduces Fenton-mediated hydroxyl formation but also increases radical generation through respiratory chain defects and reduced oxidative stress handling.
“The effects of iron deficiency on macrophage function and bactericidal radical formation is complex, as low iron reduces Fenton-mediated hydroxyl formation but also increases radical generation through defects in the respiratory chain and a reduced capacity to handle oxidative stress (Koskenkorva-Frank et al., 2013).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Koskenkorva-Frank et al., 2013
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PremisecitationPlasmodium infection induces anemia and increased IL-10 expression, which synergize to suppress phagocytic cell control of NTS and contribute to co-infection.
“Plasmodium infection induces anemia and increased expression of the anti-inflammatory cytokine IL-10, which synergize to suppress phagocytic cell control of NTS and contributes to co-infection (Lokken et al., 2014).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Lokken et al., 2014
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PremisecitationNTS enhances iron availability by triggering ERRγ expression, leading to increased hepcidin expression and iron store accumulation within macrophages.
“NTS also enhances iron availability through triggering expression of estrogen-related receptor gamma (ERRγ), which leads to increased hepcidin expression and accumulation of iron stores within macrophages (Kim et al., 2014).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Kim et al., 2014 source
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PremisecitationExcess iron interferes with nitric oxide production, which feeds back to limit Fpn1 expression and increases intracellular iron stores.
“To compound the effect, excess iron interferes with nitric oxide production, which feeds back to limit Fpn1 expression and increases intracellular iron stores (Nairz et al., 2013; Nairz et al., 2007)(Figure 2).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Nairz et al., 2013 source
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- cites Nairz et al., 2007
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InterpretationreasoningZinc deficiency may enhance innate immune cell recruitment, but cell dysfunction could inhibit effective bacterial killing.
“While zinc deficiency may enhance innate immune cell recruitment to combat pathogen invasion, cell dysfunction could inhibit effective bacterial killing.”
Quote in the paperSubstantial claimMay combine two claims.
InterpretationreasoningP. aeruginosa zinc acquisition affects both bacterial replication and virulence factor expression.
“P. aeruginosa zinc acquisition has consequences not only for bacterial replication, but also in the expression of virulence factors.”
Quote in the paperSubstantial claimMay combine two claims.
InterpretationreasoningHost calprotectin release and metal transporter activity collectively slow intracellular bacterial replication.
“These responses collectively slow intracellular bacterial replication.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationA. baumannii infection triggers neutrophil calprotectin release to limit metal availability to extracellular bacteria, while host metal transporters including NRAMP1 export divalent metals from bacteria-containing endosomes.
“A. baumannii infection triggers the release of calprotectin from infiltrating neutrophils to limit metal availability to extracellular bacteria while host metal transporters including NRAMP1 (Nevo and Nelson, 2006) export multiple divalent metals out of bacteria-containing endosomes.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Nevo and Nelson, 2006
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PremisecitationB lymphocytes show reduced proliferation in iron deficiency, and long-term iron deficiency reduces IgG and IgM antibody production.
“B lymphocytes also show reduced proliferation (Kuvibidila et al., 1983) and long-term iron deficiency reduces production of IgG and IgM antibodies (Kochanowski and Sherman, 1985).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Kuvibidila et al., 1983
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- cites Kochanowski and Sherman, 1985
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PremisecitationIron deficiency in animal models inhibits T cell proliferation in the liver, spleen, and thymus and reduces activation of T cells and natural killer T cells.
“Immunologically, iron deficiency in animal models inhibits T cell proliferation in the liver (Bonaccorsi-Riani et al., 2015), spleen (Kuvibidila et al., 1983), and thymus (Brekelmans et al., 1994) and reduces activation of T cells and natural killer T cells (Bonaccorsi-Riani et al., 2015).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Bonaccorsi-Riani et al., 2015
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- cites Kuvibidila et al., 1983
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- cites Brekelmans et al., 1994
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PremisecitationOne study found that children given iron supplements had increased risk of death compared with controls, prompting early termination of the study.
“As an example, one study found that children provided iron supplements were at an increased risk of death compared to controls, prompting early termination of the study (Sazawal et al., 2006).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Sazawal et al., 2006 source
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PremisecitationUnder zinc limitation, A. baumannii Zur de-represses the energy-dependent zinc transporter ZnuABC, which is necessary for survival in murine pneumonia, partly by supporting anti-oxidative stress defenses via a zinc-copper superoxide dismutase.
“In response to zinc limitation, the A. baumannii transcriptional zinc uptake regulator (Zur) de-represses the energy-dependent zinc transporter ZnuABC that is necessary for survival in murine models of pneumonia (Mortensen et al., 2014), in part by contributing to anti-oxidative stress defenses via a zinc-copper superoxide dismutase (Hassan et al., 2017).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Mortensen et al., 2014
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- cites Hassan et al., 2017
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PremisecitationZinc acquisition by P. aeruginosa transporters is complemented by release of the siderophore pyochelin, which can bind multiple divalent cations.
“Zinc acquisition by P. aeruginosa transporters is complemented by the release of the siderophore pyochelin, which can bind multiple divalent cations (Brandel et al., 2012).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Brandel et al., 2012
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PremisecitationHigh dietary iron weakens host defense by inhibiting macrophage interferon-γ signaling, decreasing neutrophil recruitment, and reducing pro-inflammatory cytokine expression.
“Additionally, high dietary iron weakens other arms of the host defense. Iron inhibits macrophage interferon-γ signaling, a pro-inflammatory cytokine important for producing bactericidal nitric oxide gas (Weiss et al., 1992), decreases the recruitment of neutrophils (a primary innate defense against M. tuberculosis infection), and reduces pro-inflammatory cytokine expression (Agoro et al., 2017).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Weiss et al., 1992
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- cites Agoro et al., 2017 source
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PremisecitationModerate iron supplementation increases T-cell recruitment to granulomas and enhances reactive oxygen species production that limits M. tuberculosis replication.
“It should be noted that moderate iron supplementation also results in increased T-cell recruitment to granulomas and enhanced reactive oxygen species production that limits M. tuberculosis replication (Agoro et al., 2017).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Agoro et al., 2017 source
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PremisecitationZinc triggers increased antibiotic resistance and promotes biofilm formation within cystic fibrosis sputum.
“Zinc triggers increased resistance to antibiotics and promotes biofilm formation within cystic fibrosis sputum (Marguerettaz et al., 2014).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Marguerettaz et al., 2014
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PremisecitationH. pylori infection is associated with iron deficiency, possibly by reducing gastric acid production and iron absorption or by inducing blood loss through gastric ulcers.
“H. pylori infection itself is associated with iron deficiency, possibly through reducing gastric acid production and iron absorption (Dale et al., 1998) or by inducing blood loss through gastric ulcers (Beckett et al., 2016).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Dale et al., 1998
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- cites Beckett et al., 2016
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThere is controversy over whether H. pylori is the driver in causing iron deficiency.
“However, there is controversy over whether H. pylori is the driver in causing iron deficiency (Banerjee and Bishop, 2005).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Banerjee and Bishop, 2005
Not checked in the free run.
May combine two claims.
InterpretationcitationHigh dietary manganese undermines nutritional immunity and increases pathogen virulence.
“In this manner, high dietary manganese subverts nutritional immunity and potentiates pathogen virulence.”
Quote in the paperSubstantial claim- Rests on an assumption: S. aureus invasion of organ tissue usually causes neutrophils to migrate to bacterial abscesses and release calprotectin, which binds manganese.
May combine two claims.
PremisecitationHereditary hemochromatosis is caused by an HFE mutation that leads to excess iron absorption through disrupted hepcidin and Fpn1 interactions and increases susceptibility to multiple bacterial pathogens including V. vulnificus, Y. pseudotuberculosis, Y. enterocolitica, and L. monocytogenes.
“Hereditary hemochromatosis is caused by a mutation in the HFE gene (chromosome 6p21.3) that leads to the excess absorption of iron through disruption of hepcidin and Fpn1 interactions (Adams and Barton, 2007) and increases susceptibility to multiple bacterial pathogens (Khan et al., 2007), including V. vulnificus, Y. pseudotuberculosis, Y. enterocolitica, and L. monocytogenes.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Adams and Barton, 2007
Not checked in the free run.
- cites Khan et al., 2007 source
Not checked in the free run.
May combine two claims.
PremisecitationLocal copper levels rise at sites of bacterial invasion and cause bactericidal toxicity.
“it is widely accepted that localized copper abundance increases at sites of bacterial invasion to cause bactericidal toxicity (Besold et al., 2016)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Besold et al., 2016 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationOthers discovered a positive link between H. pylori and reduced iron absorption.
“others discovered a positive link between H. pylori and reduced iron absorption(Beckett et al., 2016).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Beckett et al., 2016
Not checked in the free run.
May combine two claims.
PremisecitationThe Isd system contains high-affinity receptors that remove heme from hemoglobin for transport across the cell wall, and cytosolic heme oxygenases degrade heme to release iron.
“The Isd system contains high affinity receptors to remove heme from hemoglobin for transport across the cell wall (Grigg et al., 2010) and once internalized, cytosolic heme oxygenases degrade heme to release iron (Wilks and Heinzl, 2014).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Grigg et al., 2010
Not checked in the free run.
- cites Wilks and Heinzl, 2014
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationSome researchers found that Helicobacter infection does not influence absorption from iron supplementation.
“Whereas some researchers found that Helicobacter infection does not influence absorption from iron supplementation (Herter-Aeberli et al., 2017)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Herter-Aeberli et al., 2017
Not checked in the free run.
May combine two claims.
PremisecitationNickel serves as a cofactor in bacterial urease and NiFe hydrogenases, which aid pathogen virulence.
“Nickel is a cofactor in bacterial urease and NiFe hydrogenases that contribute to pathogen virulence (de Reuse et al., 2013; Remy et al., 2013).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites de Reuse et al., 2013
Not checked in the free run.
- cites Remy et al., 2013
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationIn humans, recognized causes of copper deficiency include gastric surgery, too much zinc intake, and malabsorption.
“In humans, the causes of copper deficiency, if known, include prior gastric surgery, excessive zinc consumption, and malabsorption (Kumar, 2006).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Kumar, 2006
Not checked in the free run.
May combine two claims.
PremisecitationOther Gram-positive and Gram-negative pathogens have evolved diverse mechanisms to use heme as an iron source and could complicate efforts to correct iron deficiency by hemoglobin restoration.
“However, other Gram-positive as well as Gram-negative pathogens have evolved diverse mechanisms to use heme as an iron source (Anzaldi and Skaar, 2010) and could also complicate efforts to correct iron deficiency by hemoglobin restoration.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Anzaldi and Skaar, 2010 source
Not checked in the free run.
May combine two claims.
InterpretationreasoningCopper availability affects host-pathogen interactions directly and also influences iron homeostasis.
“Thus, copper availability both directly affects host-pathogen interactions as well as impacts iron homeostasis.”
Quote in the paperSubstantial claim- Rests on an assumption: Copper, nickel, cobalt, and molybdenum come from the diet and are needed for several cellular processes.
May combine two claims.
PremisecitationIn mice given a high-manganese diet, calprotectin does not restrict manganese availability even though S. aureus triggers calprotectin release around heart abscesses.
“While S. aureus induces the release of calprotectin around the heart abscess, calprotectin fails to limit manganese availability when mice are provided a high manganese diet (Juttukonda et al., 2017).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Juttukonda et al., 2017
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationH. pylori infects nearly one-half of the world's population and is one of the greatest risk factors for distal gastric carcinomas.
“H. pylori infects nearly one-half of the world’s population and is one of the greatest risk factors for the development of distal gastric carcinomas (Cover and Peek, 2013).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Cover and Peek, 2013
Not checked in the free run.
May combine two claims.
PremisecitationVibrio vulnificus is highly virulent and contributes to upwards of 50% of mortality from bloodstream infections in hereditary hemochromatosis patients.
“The Gram-negative bacterium Vibrio vulnificus is highly virulent and contributes to upwards of 50% of the mortality of blood stream infections in patients suffering from hereditary hemochromatosis (Horseman and Surani, 2011).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Horseman and Surani, 2011 source
Not checked in the free run.
May combine two claims.
PremisecitationS. aureus senses heme through the HssRS two-component system, which under high heme activates the HrtAB efflux pump and limits intracellular heme availability.
“To protect against heme toxicity, S. aureus senses heme through the two-component regulatory system HssRS, which under high heme conditions activates expression of the efflux pump HrtAB and limits intracellular heme availability (Stauff and Skaar, 2009).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Stauff and Skaar, 2009
Not checked in the free run.
May combine two claims.
PremisecitationIncreased iron in the blood of hereditary hemochromatosis patients may serve as an iron pool for pathogens such as V. vulnificus, which increase high-affinity iron transporters or siderophores during iron starvation.
“Increased iron in the blood of hereditary hemochromatosis patients (Adams and Barton, 2007) may then serve as a pool of iron available for pathogens such as V. vulnificus, which increase expression of high affinity iron transporters or iron-binding siderophore molecules during iron starvation (Pajuelo et al., 2016).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Adams and Barton, 2007
Not checked in the free run.
- cites Pajuelo et al., 2016
Not checked in the free run.
May combine two claims.
PremisecitationCobalt is part of coenzyme B12 and is needed for several processes, including ethanolamine use that supports S. Typhimurium growth in the gut.
“Cobalt is incorporated into coenzyme B12 and is necessary for multiple physiological processes including ethanolamine utilization that contributes to S. Typhimurium growth in the intestines (Thiennimitr et al., 2011).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Thiennimitr et al., 2011
Not checked in the free run.
Probably not a substantial claim: may not pass S4 (based).
InterpretationreasoningThe availability of one metal often changes the distribution of other metal cations.
“with the availability of one metal often influencing the distribution of other metal cations”
Quote in the paperNot a substantial claim
The paper relies on this without support.
Bacteria require nutrient metals for essential biological processes.
“Bacteria, like their mammalian hosts, require nutrient metals for essential biological processes.”
The paper relies on this without support.
Dietary metals are rapidly complexed to host-derived molecules, so bacteria must compete with hosts to obtain the metals they need to survive.
“Given that dietary metals are rapidly complexed to host-derived molecules (Figure 1), bacteria must compete with their hosts to obtain the metals required to survive.”
The paper relies on this without support.
The link between dietary manganese and susceptibility to infectious disease is poorly understood.
“The role of dietary manganese and susceptibility to infectious disease is not well described”
The paper relies on this without support.
S. aureus invasion of organ tissue usually causes neutrophils to migrate to bacterial abscesses and release calprotectin, which binds manganese.
“S. aureus invasion into organ tissue typically results in neutrophil migration to the bacterial abscesses where they release calprotectin to bind manganese.”
The paper relies on this without support.
Other metals, despite being less abundant, are essential for life.
“However, other metals, though not as abundant, are also critical for life.”
The paper relies on this without support.
Copper, nickel, cobalt, and molybdenum come from the diet and are needed for several cellular processes.
“Copper, nickel, cobalt, and molybdenum are diet-derived and important for the proper functioning of several cellular processes.”
The paper relies on this without support.
Nickel, cobalt, and molybdenum are important in many bacterial enzymes.
“Nickel, cobalt, and molybdenum are important in many bacterial enzymes.”
The paper relies on this without support.
Associations between H. pylori, gastric cancer, and iron deficiency are well established.
“Though there are well-established associations between H. pylori, gastric cancer, and iron deficiency”
The paper relies on this without support.
It is unclear how the inflammatory environment caused by high dietary manganese affects susceptibility to bacterial colonization.
“It remains unclear how the altered inflammatory environment mediated by elevated manganese from the diet affects susceptibility to bacterial colonization”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Tissue metal levels in vertebrate hosts are mainly controlled by absorption from dietary sources in the intestinal tract, whereas bacterial pathogens acquire metal from the extracellular and intracellular environments of host tissues during infection.
“Tissue metal levels in vertebrate hosts are mainly controlled by absorption from dietary sources in the intestinal tract, whereas bacterial pathogens acquire metal from the extracellular and intracellular environments of host tissues during infection 5 .”
From Nutritional immunity: the battle for nutrient metals at the host–pathogen interface (2022) · cites this paper as [5]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
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InfluentialGlobal burden of childhood pneumonia and diarrhoea
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Iron Deficiency Anemia: A Common and Curable DiseasePreprint
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BackgroundJohnson, N. B., Hayes, L., Brown, K., Hoo, E., & Ethier, K. A. (2014) · PubMed · Cited by 578 · see citing works
Probiotic Bacteria Reduce Salmonella Typhimurium Intestinal Colonization by Competing for Iron
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BackgroundThe NRAMP family of metal-ion transporters
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“A. baumannii infection triggers the release of calprotectin from infiltrating neutrophils to limit metal availability to extracellular bacteria while host metal transporters, including NRAMP1 (Nevo and Nelson, 2006), export multiple divalent metals out of bacteria-containing endosomes.”
Reprogramming of the immune system during zinc deficiency
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BackgroundLipocalin 2: an emerging player in iron homeostasis and inflammation
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BackgroundZIP8 Regulates Host Defense through Zinc-Mediated Inhibition of NF-κB
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BackgroundSelf-citationHuman calprotectin is an iron-sequestering host-defense protein
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Dietary zinc alters the microbiota and decreases resistance to Clostridium difficile infection
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“Typhimurium increases expression of the manganese and iron transporter SitABCD, which is required for full virulence (Boyer et al., 2002; Janakiraman and Slauch, 2000).”
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“High levels of Akkermansia muciniphila, a member of the Verrucomicrobia, are associated with low inflammation and normal lipid and carbohydrate metabolism (Dao et al., 2016; Schneeberger et al., 2015), while high abundance of the Enterobacteriaceae is associated with intestinal dysbiosis.”
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“The Isd system contains high-affinity receptors to remove heme from hemoglobin for transport across the cell wall (Grigg et al., 2010) and once internalized, cytosolic heme oxygenases degrade heme to release iron (Wilks and Heinzl, 2014).”
InfluentialLife in the inflamed intestine, Salmonella style
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“For instance, heme (an iron-containing porphyrinmolecule) supplementation reduces the relative abundance of Firmicutes (Constante et al., 2017), which contain members from the beneficial butyrate-producing class Clostridia.”
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“pneumoniae (Achouiti et al., 2012; Dintilhac et al., 1997; Nairn et al., 2016; Pederick et al., 2015), but there remains much to be discovered about the diverse strategies performed by these bacteria.”
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“Nickel is a co-factor in bacterial urease and NiFe hydrogenases that contribute to pathogen virulence (de Reuse et al., 2013; Remy et al., 2013).”
ZnuA and zinc homeostasis in Pseudomonas aeruginosa
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“While not all studies find significant associations between iron supplementation and increased malaria risk (Spottiswoode et al., 2014), it is clear that caution must be exercised when manipulating the balance of iron to avoid collateral alterations in infection risk.”
BackgroundNickel Sequestration by the Host-Defense Protein Human Calprotectin
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“It is not clear whether shifts in the microbiota from iron supplementation result from direct microbe interactions or indirectly through altered host inflammation, as is seen in patients with irritable bowel syndrome (Bonovas et al., 2016).”
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“main causative agent of traveler’s diarrhea, encodes virulence factors that allow the pathogen to attach to and aggregate on the intestinal epithelium (Okhuysen and Dupont, 2010).”
BackgroundDiet, microbial virulence, and Helicobacter pylori -induced gastric cancer
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Healthy hosts rule within: ecological forces shaping the gut microbiota
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“, 2002; Janakiraman and Slauch, 2000), in part by providing iron to iron-sulfur (FeS) clusters necessary for respiration (Byndloss et al., 2018).”
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Self-citationHeme oxygenation and the widening paradigm of heme degradation
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“baumannii transcriptional zinc uptake regulator (Zur) derepresses the energy-dependent zinc transporter ZnuABC that is necessary for survival in murine models of pneumonia (Mortensen et al., 2014), in part by contributing to anti-oxidative stress defenses via a zinc-copper superoxide dismutase (Hassan et al.”
BackgroundSelf-citationMenaquinone biosynthesis potentiates haem toxicity in <i><scp>S</scp>taphylococcus aureus</i>
Wakeman, C. A., Hammer, N. D., Stauff, D. L., Attia, A. S., Anzaldi, L. L., Dikalov, S. I., Calcutt, M. W., & Skaar, E. P. (2012) · Molecular Microbiology · doi:10.1111/mmi.12063 · Cited by 94 · see citing works
Self-citationMalaria: a haematological disease
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“which acquires iron from heme largely through lysis of red blood cells (Akinosoglou et al., 2012).”
BackgroundHunger for iron: the alternative siderophore iron scavenging systems in highly virulent Yersinia
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“dotuberculosis encode uptake receptors for yersiniabactin and other siderophores to support their iron needs (Rakin et al., 2012).”
BackgroundCampylobacter jejuni transcriptional and genetic adaptation during human infection
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“uptake of heme and iron that are transcribed under iron-limited stress (Crofts et al., 2018).”
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“In response, bacteria have evolved mechanisms to relieve hostmediated copper stress including copper exporters (Johnson et al., 2015).”
BackgroundThe effect of copper deficiency on the resistance of mice to infection with Pasteurella haemolytica
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Responses of Mycobacterium tuberculosis to Growth in the Mouse Lung
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“Typhimurium produces the stealth siderophore salmochelin that includes an additional glycosylation moiety (Fischbach et al., 2006) that prevents lipocalin-2 binding.”
Reuse, H. D., Vinella, D., & Cavazza, C. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00094 · Cited by 80 · cited 1× · see citing works
“Nickel is a co-factor in bacterial urease and NiFe hydrogenases that contribute to pathogen virulence (de Reuse et al., 2013; Remy et al., 2013).”
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“Plasmodium infection induces anemia and increased expression of the anti-inflammatory cytokine IL-10, which synergize to suppress phagocytic cell control of NTS and contributes to co-infection (Lokken et al., 2014).”
The Heme Sensor System of Staphylococcus aureus
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“Within alveolar macrophages, M. tuberculosis experiences iron starvation and, in response, upregulates genes involved in metal import (Dubnau et al., 2005) and releases the siderophore mycobactin (De Voss et al., 2000).”
Nagy, T. A., Moreland, S. M., Andrews-Polymenis, H., & Detweiler, C. S. (2013) · Infection and Immunity · doi:10.1128/iai.00412-13 · Cited by 72 · cited 2× · see citing works
“Once infected, NTS within phagocytic cells acquires ferrous and ferric iron by upregulating expression of the iron importers FeoB or FepB, respectively (Nagy et al., 2014), and the siderophores enterochelin and salmochelin (Nagy et al., 2013).”
Dietary Manganese Promotes Staphylococcal Infection of the Heart
Juttukonda, L. J., Berends, E. T. M., Zackular, J. P., Moore, J. L., Stier, M. T., Zhang, Y., Schmitz, J. E., Beavers, W. N., Wijers, C. D., Gilston, B. A., et al. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.08.009 · Cited by 68 · cited 4× · see citing works
“In a mouse model of systemic S. aureus infection, high dietary manganese leads to increased bacterial burdens in the heart and enhanced bacterial virulence (Juttukonda et al., 2017).”
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“Immunologically, iron deficiency in animal models inhibits T cell proliferation in the liver (Bonaccorsi-Riani et al., 2015), spleen (Kuvibidila et al., 1983), and thymus (Brekelmans et al., 1994), and reduces activation of T cells and natural killer T cells (Bonaccorsi-Riani et al., 2015).”
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Iron deficiency impairs Intra-hepatic lymphocyte mediated immune response
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“Immunologically, iron deficiency in animal models inhibits T cell proliferation in the liver (Bonaccorsi-Riani et al., 2015), spleen (Kuvibidila et al., 1983), and thymus (Brekelmans et al., 1994), and reduces activation of T cells and natural killer T cells (Bonaccorsi-Riani et al., 2015).”
Studying microbial functionality within the gut ecosystem by systems biology
Hornung, B., dos Santos, V. A. P. M., Smidt, H., & Schaap, P. J. (2018) · Genes & Nutrition · doi:10.1186/s12263-018-0594-6 · Cited by 57 · cited 1× · see citing works
“As with any ecosystem, resource availability is a strong force dictating population structure, with limiting resources driving competition between species and even individuals (Hornung et al., 2018).”
Decreased antibody formation in iron-deficient rat pups—effect of iron repletion
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Zinc stress induces copper depletion in Acinetobacter baumannii
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“Consistently, dietary zinc supplementation reverses disease progression, inhibits EAEC adherence and biofilm formation, and reduces epithelial production of pro-inflammatory cytokines (Medeiros et al., 2013).”
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“Plasmodium infection induces anemia and increased expression of the anti-inflammatory cytokine IL-10, which synergize to suppress phagocytic cell control of NTS and contributes to co-infection (Lokken et al., 2014).”
BackgroundInfluentialIron and Fur in the life cycle of the zoonotic pathogen Vibrio vulnificus
Pajuelo, D., Hernández‐Cabanyero, C., Sanjuán, E., Lee, C., Silva-Hernández, F. X., Hor, L., MacKenzie, S. A., & Amaro, C. (2016) · Environmental Microbiology · doi:10.1111/1462-2920.13424 · Cited by 44 · see citing works
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Utilization of Lactoferrin-Bound and Transferrin-Bound Iron by <i>Campylobacter jejuni</i>
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“, 2015) as well as enhancing natural killer cells (Rogers et al., 1983) and macrophage activity (Smialowicz et al.”
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Oral zinc and common childhood infections—An update
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<scp><i>S</i></scp><i>almonella</i>acquires ferrous iron from haemophagocytic macrophages
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The iron link between malaria and invasive non-typhoid Salmonella infections
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Iron overload and tuberculosis: a case for iron chelation therapy.
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“While zinc supplementation can improve host resistance to infection, in some cases it fails to correct impairments in the immune response (Yuan et al., 2016).”
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Evidence that manganese inhibits an early event during stimulation of lymphocytes by mitogens
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“However, high manganese also inhibits lymphocyte proliferation (Hart, 1978), exemplifying how balancing metal levels is necessary for optimum immune function.”
BackgroundInhibition of bacterial superoxide defense
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“aureus from hemeinduced oxidative stress (Surdel et al., 2016).”
Herter‐Aeberli, I., Eliancy, K., Rathon, Y., Loechl, C., Pierre, J. M., & Zimmermann, M. B. (2017) · British Journal Of Nutrition · doi:10.1017/s0007114517002045 · Cited by 17 · cited 1× · see citing works
“cobacter infection does not influence absorption from iron supplementation (Herter-Aeberli et al., 2017), others discovered a positive link between H.”
BackgroundKonomi, J. V., Harris, F. L., Ping, X., et al. (2014) · Alcohol and Alcoholism · doi:10.1093/alcalc/agu073 · Cited by 9 · cited 1× · see citing works
“However, zinc deficiency may prevent adequate pathogen clearance, as ethanol-induced zinc deficiency in macrophages leads to impaired phagocytosis (Konomi et al., 2015).”
Banerjee, S., & Bishop, W. P. (2004) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200501000-00025 · Cited by 4 · cited 1× · see citing works
“pylori is the driver in causing iron deficiency (Banerjee and Bishop, 2005).”
BackgroundBanerjee, S., Bishop, W. P., Braegger, C., et al. (2005) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1002/j.1536-4801.2005.tb00939.x
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The gut microbiota at the intersection of diet and human health
Gentile, C. L., & Weir, T. L. (2018) · Science · doi:10.1126/science.aau5812 · Cited by 1,049 · see citing works
Nutritional immunity: the battle for nutrient metals at the host–pathogen interface
Murdoch, C. C., & Skaar, E. P. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00745-6 · Cited by 701 · see citing works
Self-citationKlein, R., & Hultgren, S. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0324-0 · Cited by 479 · see citing works
Fussell, J. C., Franklin, M., Green, D. C., Gustafsson, M. E. R., Harrison, R. M., Hicks, W., Kelly, F. J., Kishta, F., Miller, M. R., Mudway, I., et al. (2022) · Environmental Science & Technology · doi:10.1021/acs.est.2c01072 · Cited by 477 · see citing works
Mucins and Their Role in Shaping the Functions of Mucus Barriers
Wagner, C. E., Wheeler, K. M., & Ribbeck, K. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100617-062818 · Cited by 308 · see citing works
Bahr, G., González, L. J., & Vila, A. J. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00138 · Cited by 284 · see citing works
Ferreira, R. L. U., Sena‐Evangelista, K. C. M., de Azevedo, E. P., Pinheiro, F. I., Cobucci, R. N., & Pedrosa, L. F. C. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.685317 · Cited by 228 · see citing works
“Manganese, zinc, selenium, and iron act as critical cofactors for bacterial enzymes responsible for DNA replication and transcription, antioxidant action, and cellular respiration (97).”
BackgroundHör, J., Matera, G., Vogel, J., Gottesman, S., & Storz, G. (2020) · EcoSal Plus · doi:10.1128/ecosalplus.esp-0030-2019 · Cited by 188 · see citing works
“Iron is a critical and often limiting nutrient for all organisms, particularly for bacterial pathogens that must acquire the metal ion from their hosts (reviewed in reference 149).”
BackgroundBacterial siderophores: diversity, uptake pathways and applications
Schalk, I. J. (2024) · Nature Reviews Microbiology · doi:10.1038/s41579-024-01090-6 · Cited by 248 · see citing works
A protein-based cGAS-STING nanoagonist enhances T cell-mediated anti-tumor immune responses
Wang, X., Liu, Y., Xue, C., Hu, Y., Zhao, Y., Cai, K., Li, M., & Luo, Z. Y. (2022) · Nature Communications · doi:10.1038/s41467-022-33301-0 · Cited by 224 · see citing works
High fat diet, gut microbiome and gastrointestinal cancer
Tong, Y., Gao, H., Qi, Q., Liu, X., Li, J., Gao, J., Li, P., Wang, Y., Du, L., & Wang, C. (2021) · Theranostics · doi:10.7150/thno.56157 · Cited by 205 · see citing works
“Meanwhile, some micronutrients such as vitamins and zinc can also affect the composition of intestinal microbes [219, 220].”
BackgroundMetals as phagocyte antimicrobial effectors
Sheldon, J. R., & Skaar, E. P. (2019) · Current Opinion in Immunology · doi:10.1016/j.coi.2019.04.002 · Cited by 143 · see citing works
Self-citationRoles of S100A8 , S100A9 and S100A12 in infection, inflammation and immunity
Xia, P., Ji, X., Li, Y., Lian, S., Chen, Z., & Luo, Y. (2023) · Immunology · doi:10.1111/imm.13722 · Cited by 165 · see citing works
“This triggers local inflammatory and immune responses, promotes the oligomerization of S100A8 and S100A9, limits pathogen growth and virulence factor activity and enhances pathogen resistance [23, 24].”
BackgroundImmunometabolic crosstalk during bacterial infection
Rosenberg, G., Riquelme, S. A., Prince, A. S., & Avraham, R. (2022) · Nature Microbiology · doi:10.1038/s41564-022-01080-5 · Cited by 150 · see citing works
The role of iron in host–microbiota crosstalk and its effects on systemic glucose metabolism
Mayneris‐Perxachs, J., Moreno‐Navarrete, J. M., & Fernández‐Real, J. M. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00721-3 · Cited by 158 · see citing works
Dendritic cell–derived hepcidin sequesters iron from the microbiota to promote mucosal healing
Bessman, N. J., Mathieu, J. R. R., Renassia, C., Zhou, L., Fung, T. C., Fernandez, K. C., Austin, C., Moeller, J. B., Zumerle, S., Louis, S., et al. (2020) · Science · doi:10.1126/science.aau6481 · Cited by 145 · see citing works
Iron sequestration by transferrin 1 mediates nutritional immunity in <i>Drosophila melanogaster</i>
Iatsenko, I., Marra, A., Boquete, J.-P., Peña, J., & Lemaitre, B. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1914830117 · Cited by 133 · see citing works
Xenosiderophore Utilization Promotes Bacteroides thetaiotaomicron Resilience during Colitis
Zhu, W., Winter, M. G., Spiga, L., Hughes, E. R., Chanin, R. B., Mulgaonkar, A., Pennington, J., Maas, M., Behrendt, C. L., Kim, J., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.01.010 · Cited by 100 · see citing works
“During colitis, microbial access to metals is limited, presumably by the release of lactoferrin and calprotectin (reviewed in Hood and Skaar, 2012; Lopez and Skaar, 2018; Zhu et al., 2019b).”
BackgroundEmerging Opportunities To Manipulate Metal Trafficking for Therapeutic Benefit
Hunsaker, E. W., & Franz, K. J. (2019) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.9b01029 · Cited by 106 · see citing works
Microbiome Dynamics: A Paradigm Shift in Combatting Infectious Diseases
Kamel, M. S., Aleya, S., Alsubih, M., & Aleya, L. (2024) · Journal of Personalized Medicine · doi:10.3390/jpm14020217 · Cited by 96 · see citing works
“Some commensal bacteria can sequester limiting nutrients like iron, reducing its availability to pathogens and limiting their growth [66–68].”
BackgroundThe roles of metals in insect–microbe interactions and immunity
Hrdina, A., & Iatsenko, I. (2021) · Current Opinion in Insect Science · doi:10.1016/j.cois.2021.12.004 · Cited by 65 · see citing works
Sauer, A. K., & Grabrucker, A. M. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01295 · Cited by 85 · see citing works
“The low relative abundance of Verrucomicrobia populations and a decrease in beneficial bacteria was correlated with zinc deficiency in further studies (Lopez and Skaar, 2018).”
BackgroundMetallobiology of Lactobacillaceae in the gut microbiome
Huynh, U., & Zastrow, M. L. (2022) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2022.112023 · Cited by 80 · see citing works
Multifunctional role of zinc in human health: an update
Kiouri, D. P., Tsoupra, E., Peana, M., Perlepes, S. P., Stefanidou, M. E., & Chasapis, C. T. (2023) · EXCLI journal · doi:10.17179/excli2023-6335 · Cited by 83 · see citing works
“Zinc deficiency has been associated with a decrease in Verrucomicrobia and Proteobacteria and an increase in Firmicutes, Actinobacteria and Bacteroidetes in mice (Lopez and Skaar, 2018; MaynerisPerxachs et al., 2016).”
BackgroundIntestinal mucin is a chaperone of multivalent copper
Reznik, N., Gallo, A. D., Rush, K. W., Javitt, G., Fridmann‐Sirkis, Y., Ilani, T., Nairner, N. A., Fishilevich, S., Gokhman, D., Chacón, K. N., et al. (2022) · Cell · doi:10.1016/j.cell.2022.09.021 · Cited by 69 · see citing works
Shaw, C. A., Hess, M., & Weimer, B. C. (2022) · Virulence · doi:10.1080/21505594.2022.2127196 · Cited by 72 · see citing works
Riedelberger, M., Penninger, P., Tscherner, M., Seifert, M., Jenull, S., Brunnhofer, C., Scheidl, B., Tsymala, I., Bourgeois, C., Petryshyn, A., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.01.023 · Cited by 64 · see citing works
Broom, L. J., Monteiro, A. N. T. R., & Piñon, A. (2021) · Animals · doi:10.3390/ani11051276 · Cited by 67 · see citing works
“In a process referred to as ‘nutritional immunity’, the host’s immune-related proteins sequester metals to deprive bacteria (pathogens) of these essential nutrients [68].”
BackgroundStructural and Proteomic Characterization of the Initiation of Giant Virus Infection
Schrad, J. R., Abrahão, J. S., Cortines, J. R., et al. (2020) · Cell · doi:10.1016/j.cell.2020.04.032 · Cited by 67 · see citing works
“During phagocytosis, amoebal phagosomes drop to ~pH 4 (not low enough to trigger stargate opening in vitro), but they are also inundated with metals (like Cu and Zn) and ROS (German et al., 2013; Lopez and Skaar, 2018).”
BackgroundInfluentialComprehensive Review Regarding Mercury Poisoning and Its Complex Involvement in Alzheimer’s Disease
Paduraru, E., Iacob, D. G., Rarinca, V., Rusu, A., Jijie, R., Ilie, O., Ciobica, A. S., Nicoară, M., & Doroftei, B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23041992 · Cited by 65 · see citing works
“Thus ensuring the control of metal bioavailability and brain-related trophic nutrients that prevent bacterial overgrowth [135].”
BackgroundMacGilvary, N. J., Kevorkian, Y. L., & Tan, S. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007591 · Cited by 51 · see citing works
The impact of iron and heme availability on the healthy human gut microbiome in vivo and in vitro
Celis, A. I., Relman, D., & Huang, K. (2023) · Cell Chemical Biology · doi:10.1016/j.chembiol.2022.12.001 · Cited by 57 · see citing works
The impact of maternal and early life malnutrition on health: a diet-microbe perspective
Forgie, A. J., Drall, K. M., Bourque, S. L., Field, C. J., Kozyrskyj, A. L., & Willing, B. P. (2020) · BMC Medicine · doi:10.1186/s12916-020-01584-z · Cited by 59 · see citing works
“plementation, Proteobacteria may thrive at the expense of other gut bacteria [150, 151].”
BackgroundChen, L., Wang, Z., Wang, P., Yu, X., Ding, H., Wang, Z., & Feng, J. (2021) · Microbiology Spectrum · doi:10.1128/spectrum.00483-21 · Cited by 60 · see citing works
The Role of Microbiota in Drosophila melanogaster Aging
Arias-Rojas, A., & Iatsenko, I. (2022) · Frontiers in Aging · doi:10.3389/fragi.2022.909509 · Cited by 47 · see citing works
Regulation of mitochondrial iron homeostasis by sideroflexin 2
Mon, E. E., Wei, F., Ahmad, R. N. R., Yamamoto, T., Moroishi, T., & Tomizawa, K. (2018) · The Journal of Physiological Sciences · doi:10.1007/s12576-018-0652-2 · Cited by 52 · see citing works
Manganese homeostasis at the host-pathogen interface and in the host immune system
Wu, Q., Mu, Q., Xia, Z., Min, J., & Wang, F. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.12.006 · Cited by 57 · see citing works
Price, S. L., Vadyvaloo, V., DeMarco, J. K., Brady, A., Gray, P. A., Kehl-Fie, T. E., Garneau-Tsodikova, S., Perry, R. D., & Lawrenz, M. B. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2104073118 · Cited by 49 · see citing works
Williams, C. L., Caraballo‐Rodríguez, A. M., Allaband, C., Zarrinpar, A., Knight, R. D., & Gauglitz, J. M. (2018) · Drug Discovery Today Disease Models · doi:10.1016/j.ddmod.2019.08.012 · Cited by 46 · see citing works
“Interactions between gut microbiota and iron have been well documented in the literature [72,73], as well as a role for dietary transition metals to modulate host–microbe interactions [74].”
BackgroundHorký, P., Skalíčková, S., Urbánková, L., et al. (2019) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-019-0319-8 · Cited by 50 · see citing works
“The low Zn doses can be even beneficial for bacterial growth and used as essential trace elements [32, 33].”
BackgroundRajan, M., Anderson, C. P., Rindler, P. M., Romney, S. J., Ferreira, M. C., Gertz, J., & Leibold, E. A. (2019) · eLife · doi:10.7554/elife.44674 · Cited by 42 · see citing works
“Excess iron also predisposes humans to infectious diseases, and limiting iron availability to microbes is a critical host innate immune response (Lopez and Skaar, 2018; Weiss and Carver, 2018).”
BackgroundInfluentialIslam, T., Albracht‐Schulte, K., Ramalingam, L., Schlabritz‐Lutsevich, N., Park, O., Zabet‐Moghaddam, M., Kalupahana, N. S., & Moustaïd‐Moussa, N. (2022) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2022.109242 · Cited by 49 · see citing works
Mechanisms of host adaptation by bacterial pathogens
Barber, M. F., & Fitzgerald, J. R. (2024) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuae019 · Cited by 49 · see citing works
“Among the best studied group of nutrients in this regard ar e tr ansition metals suc h as ir on, zinc, and manganese, which serve as necessary cofactors for many essential bacterial proteins (K elliher 2016 , P almer and Skaar 2016 , Sheldon et al. 2016 , Lopez and Skaar 2018 , Gerner et al. 2020 ).”
BackgroundIron at the host-microbe interface
Gerner, R. R., Nuccio, S.-P., & Raffatellu, M. (2020) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2020.100895 · Cited by 45 · see citing works
Effect of Dietary Magnesium Content on Intestinal Microbiota of Rats
García-Legorreta, A., Soriano-Pérez, L. A., Flores-Buendía, A. M., Medina‐Campos, O. N., Noriega, L. G., Granados‐Portillo, O., Nambo‐Venegas, R., Tovar, A. R., Mendoza-Vargas, A., Barrera‐Oviedo, D., et al. (2020) · Nutrients · doi:10.3390/nu12092889 · Cited by 46 · see citing works
“For instance, zinc deficiency in piglets is associated with a lower abundance of Clostridiales and Verrucomicrobia and a higher abundance of Enterobacteriaceae and Enterococcus [8].”
BackgroundInfluentialMetal-doped carbon dots for biomedical applications: From design to implementation
Qi, J., Zhang, P., Zhang, T., et al. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e32133 · Cited by 45 · see citing works
“Transition metals are cofactors required for many life-critical proteins and are essential for all life forms [31].”
BackgroundMaurakis, S., Keller, K., Maxwell, C. N., Pereira, K., Chazin, W. J., Criss, A. K., & Cornelissen, C. N. (2019) · PLOS Pathogens · doi:10.1371/journal.ppat.1007937 · Cited by 45 · see citing works
Longitudinal Investigation of the Gut Microbiota in Goat Kids from Birth to Postweaning
Zhuang, Y., Chai, J., Cui, K., Bi, Y., Diao, Q., Huang, W., Usdrowski, H. M., & Zhang, N. (2020) · Microorganisms · doi:10.3390/microorganisms8081111 · Cited by 44 · see citing works
“Turicibacter is known to reduce the susceptibility to Salmonella infection [36].”
BackgroundBacillus subtilisTerC Family Proteins Help Prevent Manganese Intoxication
Paruthiyil, S., Pinochet‐Barros, A., Huang, X., & Helmann, J. D. (2019) · Journal of Bacteriology · doi:10.1128/jb.00624-19 · Cited by 40 · see citing works
“Mammalian hosts may limit the bioavailability of Mn(II) for use by pathogens, as part of the innate immune mechanism known as nutritional immunity (12, 13).”
BackgroundThe Immune Protein Calprotectin Impacts Clostridioides difficile Metabolism through Zinc Limitation
Lopez, C. A., Beavers, W. N., Weiss, A., Knippel, R. J., Zackular, J. P., Chazin, W., & Skaar, E. P. (2019) · mBio · doi:10.1128/mbio.02289-19 · Cited by 42 · see citing works
“Disruption of the microbiota through antimicrobial compounds, drastic changes in diet (4), or alterations in the host immune status (5) increases susceptibility to colonization by opportunistic pathogens such as Clostridioides difficile.”
BackgroundSelf-citationIron Reshapes the Gut Microbiome and Host Metabolism
Botta, A. M., Barra, N. G., Lam, N. H., Chow, S., Pantopoulos, K., Schertzer, J. D., & Sweeney, G. (2021) · Journal of Lipid and Atherosclerosis · doi:10.12997/jla.2021.10.2.160 · Cited by 39 · see citing works
Xiong, D., Muema, C., Zhang, X., Pan, X., Xiong, J., Yang, H., Yu, J., & Wei, H. (2021) · Virologica Sinica · doi:10.1007/s12250-021-00391-x · Cited by 39 · see citing works
“Many studies have proven that microbiota is an important component of human body (Kamada et al. 2013; Lopez and Skaar 2018).”
BackgroundRegulation of Bacterial Manganese Homeostasis and Usage During Stress Responses and Pathogenesis
Martin, J. E., & Waters, L. S. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.945724 · Cited by 35 · see citing works
“At the organismal level, host-mediated metal changes may manifest differently, depending on the site of infection and bacterial species involved (Lopez and Skaar, 2018).”
BackgroundZinc homeostasis in Pseudomonas
Ducret, V., González, D., & Perron, K. (2022) · BioMetals · doi:10.1007/s10534-022-00475-5 · Cited by 36 · see citing works
“As a consequence, zinc plays a major role in host–pathogen interactions across the eukaryotic world (Hood and Skaar 2012; Lopez and Skaar 2018).”
BackgroundYou’d Better Zinc—Trace Element Homeostasis in Infection and Inflammation
Haase, H., & Schomburg, L. (2019) · Nutrients · doi:10.3390/nu11092078 · Cited by 37 · see citing works
“, several cytokines affect the homeostasis of certain trace elements and conversely, certain trace elements control immune cell activity and the inflammatory response [35].”
BackgroundMańkowska-Wierzbicka, D., Stelmach-Mardas, M., Gabryel, M., Tomczak, H., Skrzypczak-Zielińska, M., Zakerska-Banaszak, O., Sowińska, A., Mahadea, D., Baturo, A., Wolko, Ł., et al. (2020) · Biomedicines · doi:10.3390/biomedicines8080268 · Cited by 39 · see citing works
“Calprotectin belongs to the antimicrobial proteins that inhibit the growth of microbial species [72,73].”
BackgroundCelis, A. I., & Relman, D. A. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.03.032 · Cited by 34 · see citing works
Huynh, U., Qiao, M., King, J., Trinh, B. K., Valdez, J., Haq, M., & Zastrow, M. L. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.01006-21 · Cited by 35 · see citing works
Machate, D. J. (2023) · Journal of Trace Elements and Minerals · doi:10.1016/j.jtemin.2023.100057 · Cited by 43 · see citing works
Trace metal elements: a bridge between host and intestinal microorganisms
Ma, Y., Fei, Y., Ding, S., Jiang, H., Fang, J. Q., & Liu, G. (2023) · Science China Life Sciences · doi:10.1007/s11427-022-2359-4 · Cited by 37 · see citing works
“increased T-cell recruitment alone is not sufficient to overcome other aspects of impairment, such as Fe-mediated immune responses (Lopez and Skaar, 2018).”
BackgroundBarisch, C., Kalinina, V. O., Lefrançois, L. H., Appiah, J., López-Jiménez, A. T., & Soldati, T. (2018) · Journal of Cell Science · doi:10.1242/jcs.222000 · Cited by 32 · see citing works
“Upon phagocytosis, the innate immune phagocyte restricts intravacuolar bacterial growth either by depleting essential metal ions (e.g. Fe2+ and Mn2+) or by accumulating others, such as Cu2+ and Zn2+, to intoxicating concentrations (Flannagan et al., 2015; Lopez and Skaar, 2018).”
BackgroundAlteration in Gut Microbiota Associated with Zinc Deficiency in School-Age Children
Chen, X., Jiang, Y. L., Wang, Z., Chen, Y., Tang, S., Wang, S., Li, S., Huang, X., Long, D., Wang, L., et al. (2022) · Nutrients · doi:10.3390/nu14142895 · Cited by 36 · see citing works
“Of these, micronutrients from the diet are of great importance for the human body and particularly for the resident population of gut microbes [18].”
BackgroundBrown, H. A., DeVeaux, A. L., Juliano, B. R., Photenhauer, A. L., Boulinguiez, M., Bornschein, R. E., Wawrzak, Z., Ruotolo, B. T., Terrapon, N., & Koropatkin, N. M. (2023) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-023-04812-w · Cited by 37 · see citing works
Foligné, B., George, F., Standaert‐Vitse, A., Garat, A., Poiret, S., Peucelle, V., Ferreira, S., Sobry, H., Muharram, G., Lucau‐Danila, A., et al. (2020) · The FASEB Journal · doi:10.1096/fj.202000562rr · Cited by 33 · see citing works
Candida Pathogenicity and Interplay with the Immune System
Valand, N., & Girija, U. V. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-67452-6_11 · Cited by 36 · see citing works
Hoffmann, A., Haschka, D., de Souza, L. V., Tymoszuk, P., Seifert, M., von Raffay, L., Hilbe, R., Petzer, V., Moser, P. L., Nairz, M., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103568 · Cited by 31 · see citing works
“Iron is an essential nutrient for both mammals and microbes [60].”
BackgroundSobel, M., Navas‐Acién, A., Powers, M., Grau-Pérez, M., Goessler, W., Best, L. G., Umans, J. G., Oelsner, E. C., Podolanczuk, A. J., & Sanchez, T. R. (2021) · Environmental Research · doi:10.1016/j.envres.2021.112194 · Cited by 31 · see citing works
Zinc homeostasis and redox alterations in obesity
Franco, C., & Canzoniero, L. M. T. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1273177 · Cited by 31 · see citing works
“In addition, zinc contributes to maintaining the integrity of the intestinal barrier (73) by regulating the activity of alkaline phosphatase (74).”
BackgroundInflammatory adipose activates a nutritional immunity pathway leading to retinal dysfunction
Sterling, J. K., Baumann, B. H., Foshe, S., Voigt, A. P., Guttha, S., Alnemri, A. G., McCright, S. J., Li, M., Zauhar, R. J., Montezuma, S. R., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110942 · Cited by 30 · see citing works
“To defend against pathogens, vertebrate immune systems can sequester iron as a bacteriostatic mechanism of host defense termed “nutritional immunity” (Lopez and Skaar, 2018; Soares and Weiss, 2015).”
BackgroundKundra, P., Rachmühl, C., Lacroix, C., & Geirnaert, A. (2020) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201901271 · Cited by 27 · see citing works
Overview of Yersinia pestis Metallophores: Yersiniabactin and Yersinopine
Taghrid Chaaban, A., Mohsen, Y., Ezzeddine, Z., & Ghssein, G. (2023) · Biology · doi:10.3390/biology12040598 · Cited by 30 · see citing works
“Therefore, bacteria require metal ions for their metabolism, virulence, and transcriptional regulation [18,19].”
BackgroundHaschka, D., Tymoszuk, P., Petzer, V., Hilbe, R., Heeke, S., Dichtl, S., Skvortsov, S., Demetz, E., Berger, S., Seifert, M., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.141760 · Cited by 29 · see citing works
Brunson, D. N., Colomer‐Winter, C., Lam, L. N., & Lemos, J. A. C. (2023) · Infection and Immunity · doi:10.1128/iai.00496-22 · Cited by 25 · see citing works
Advances in the study of selenium and human intestinal bacteria
Cai, J., Su, W., Chen, X., & Zheng, H. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.1059358 · Cited by 28 · see citing works
“In this process, an important role is played by selenium, one of the essential elements responsible for DNA replication and transcription, and a key cofactor for antioxidant and cellular respiratory bacterial enzymes (25).”
BackgroundCheng, J., Kolba, N., & Tako, E. (2023) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2023.2169857 · Cited by 27 · see citing works
“Dietary metals, such as Zn, cannot be synthesized, meaning that resident microbiota must compete with their host to obtain metals essential for survival (Lopez and Skaar 2018).”
BackgroundResultAkhter, F., Womack, E., Vidal, J. E., Breton, Y. S. L., McIver, K. S., Pawar, S., & Eichenbaum, Z. (2020) · Scientific Reports · doi:10.1038/s41598-020-71910-1 · Cited by 22 · see citing works
The putative role of ferroptosis in gastric cancer: a review
Wang, L., & Wang, H. (2023) · European Journal of Cancer Prevention · doi:10.1097/cej.0000000000000817 · Cited by 23 · see citing works
Remodeling of Paranasal Sinuses Mucosa Functions in Response to Biofilm-Induced Inflammation
Kaliniak, S., Fiedoruk, K., Spałek, J., Piktel, E., Durnaś, B., Góźdź, S. S., Bucki, R., & Okła, S. (2024) · Journal of Inflammation Research · doi:10.2147/jir.s443420 · Cited by 23 · see citing works
“73 It may be assumed that CRS-associated microbiota are under permanent Zn-mediated “nutritional immunity”, that is, the host’s mechanism for inhibiting bacterial growth by restricting the availability of essential metal ions.”
BackgroundUsing Enteric Pathogens to Probe the Gut Microbiota
Spiga, L., & Winter, S. (2018) · Trends in Microbiology · doi:10.1016/j.tim.2018.11.007 · Cited by 23 · see citing works
Riedelberger, M., Penninger, P., Tscherner, M., Hadriga, B., Brunnhofer, C., Jenull, S., Stoiber, A., Bourgeois, C., Petryshyn, A., Glaser, W., et al. (2020) · iScience · doi:10.1016/j.isci.2020.101121 · Cited by 23 · see citing works
“Indeed, Zn deficiency arising from malnutrition or mutations increases the susceptibility for infections and various other diseases (Ferreira and Gah, 2017; Lopez and Skaar, 2018; Vaeth and Feske, 2018).”
BackgroundIncorporating functional trade-offs into studies of the gut microbiota
Reese, A. T., & Kearney, S. M. (2019) · Current Opinion in Microbiology · doi:10.1016/j.mib.2019.09.003 · Cited by 21 · see citing works
How Pathogens Feel and Overcome Magnesium Limitation When in Host Tissues
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“One host defense strategy with broad specificity is nutritional immunity [5].”
BackgroundInfluentialNew Insights Into DAEC and EAEC Pathogenesis and Phylogeny
Meza-Segura, M., Zaidi, M., de León, A. V.-P., Morán-García, N., Martínez-Romero, E., Nataro, J., & Estrada-Garcia, T. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.572951 · Cited by 18 · see citing works
“genomes should be advantageous not only for its virulence, but to overcome the host “nutritional immunity” which limits bacterial growth by sequestering metals in the intestine (Lopez and Skaar, 2018).”
BackgroundRibeiro, M. M., Fonseca, L. D. S., dos Anjos, J. S., Capo-Chichi, J. C. C., Borges, N. A., Burrowes, J. D., & Mafra, D. (2021) · Nutrition in Clinical Practice · doi:10.1002/ncp.10662 · Cited by 22 · see citing works
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Metal transporter SLC39A14/ZIP14 modulates regulation between the gut microbiome and host metabolism
Mitchell, S. B., Thorn, T. L., Lee, M.-T., Kim, Y., Comrie, J. M. C., Bai, Z. S., Johnson, E. L., & Aydemir, T. B. (2023) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00091.2023 · Cited by 18 · see citing works
Iron restriction induces the small-colony variant phenotype in Staphylococcus aureus
Islam, S., Callender, A. C., Ho, Q. N., & Wakeman, C. A. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.978859 · Cited by 17 · see citing works
“Therefore, bacteria evolve their strategies to access those metal nutrients to counteract the hostinduced defense mechanisms (Lopez and Skaar, 2018).”
BackgroundReese, A. T., & Carmody, R. N. (2018) · Applied and Environmental Microbiology · doi:10.1128/aem.02246-18 · Cited by 19 · see citing works
“Better understood are trace metals, which are essential micronutrients for animals and can also contribute to gut microbial dynamics (138).”
BackgroundTransition metals and host-microbe interactions in the inflamed intestine
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“Such effect may modulate the bioavailability of other metals such as iron and zinc, brain trophic key nutrients, that may also regulate intestinal bacterial overgrowth (Lopez and Skaar, 2018).”
BackgroundPseudomonas Synergizes with Fluconazole against Candida during Treatment of Polymicrobial Infection
Hattab, S., Dagher, A.-M., & Wheeler, R. T. (2022) · Infection and Immunity · doi:10.1128/iai.00626-21 · Cited by 17 · see citing works
Infections as ecosystems: community metabolic interactions in microbial pathogenesis
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“Iron is an important trace element for many metabolic processes (16, 159); however, the host uses nutritional immunity with the production of numerous iron-binding proteins, such as heme, hemoglobin, ferritin, lactoferrin, and transferrin, to limit microbial access to free iron (20, 21, 160, 161).”
Iron homeostasis in Bacillus subtilis relies on three differentially expressed efflux systems
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“One common theme, however, is that fitness in the host environment, and therefore virulence, is heavily reliant on the ability of bacteria to both compete with the host for essential metal ions, and to balance high-affinity import with specific efflux systems [50, 63, 67–69].”
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“coli.(127) Indeed, low zinc causes increased virulence of enteroaggregative E.”
BackgroundIL-17C Protects Nasal Epithelium from Pseudomonas aeruginosa Infection
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Dietary zinc deficiency promotes Acinetobacter baumannii lung infection via IL-13 in mice
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“stress conditions; Mn is required as a co-factor for many bacterial enzymes involved in the detoxification of reactive oxygen species (reviewed by [65,66]).”
BackgroundN ‐Acyl Amides from Neisseria meningitidis and Their Role in Sphingosine Receptor Signaling
Cho, W., York, A. G., Wang, R., Wyche, T. P., Piizzi, G., Flavell, R. A., & Crawford, J. M. (2022) · ChemBioChem · doi:10.1002/cbic.202200490 · Cited by 13 · see citing works
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- Authors
- Lopez, C. A., & Skaar, E. P.
- Affiliations
- Vanderbilt University Medical Center (US)
- Vanderbilt University (US)
- Corresponding author
- Skaar, Eric P.
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2018-06
- Volume
- 23
- Issue
- 6
- Pages
- 737-748
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC6007885
- OpenAlex
- W2808070375
- Semantic Scholar
- 3f6a09c4bd415ea237ec2be38ce6eec04e70d834
- Cited by
- 190
- References
- 135
- Citations by year
- 2026: 14 · 2025: 19 · 2024: 21 · 2023: 22 · 2022: 29 · 2021: 29 · 2020: 31 · 2019: 16 · 2018: 9
- FWCI
- 2.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Host & Microbe (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Jane Coffin Childs Memorial Fund for Medical Research
- National Institutes of Health (R01 AI073843, T32AI095202, R01 AI101171, R01 AI069233)
- Burroughs Wellcome Fund
- Simons Foundation
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- host-microbe interactions, nutritional immunity, zinc, iron, manganese, metal sequestration, immune proteins, bacterial pathogenesis, host defense against bacteria
- MeSH terms
- Host Microbial Interactions, Animals, Bacteria, Diet, Humans, Immunity, Iron, Manganese, Metals, Molybdenum, Respiratory System, Virulence, Zinc, Gastrointestinal Tract, Host-Pathogen Interactions, Microbial Interactions, Microbiota
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