Slc11a1 limits intracellular growth of Salmonella enterica sv. Typhimurium by promoting macrophage immune effector functions and impairing bacterial iron acquisition

Nairz, Manfred; Fritsche, Gernot; Crouch, Marie-Laure V.; Barton, Howard C.; Fang, Ferric C.; Weiss, Günter

doi:10.1111/j.1462-5822.2009.01337.x

Cited by 100Salmonella and Campylobacter epidemiologyIron Metabolism and DisordersBacterial Genetics and Biotechnology

Slc11a1 limits intracellular growth of Salmonella enterica sv. Typhimurium by promoting macrophage immune effector functions and impairing bacterial iron acquisition

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Nairz, Manfred, Fritsche, Gernot, Crouch, Marie-Laure V., Barton, Howard C., Fang, Ferric C., Weiss, Günter·2009·Cellular Microbiology

DOI 10.1111/j.1462-5822.2009.01337.xPMC PMC3467104

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Abstract

The natural resistance-associated macrophage protein 1, Slc11a1, is a phagolysosomal transporter for protons and divalent ions including iron that confers host protection against diverse intracellular pathogens including Salmonella. We investigated and compared the regulation of iron homeostasis and immune function in RAW264.7 murine phagocytes stably transfected with non-functional Slc11a1 and functional Slc11a1 controls in response to an infection with Salmonella enterica serovar Typhimurium. We report that macrophages lacking functional Slc11a1 displayed an increased expression of transferrin receptor 1, resulting in enhanced acquisition of transferrin-bound iron. In contrast, cellular iron release mediated via ferroportin 1 was significantly lower in Salmonella-infected Slc11a1-negative macrophages in comparison with phagocytes bearing Slc11a1. Lack of Slc11a1 led to intracellular persistence of S. enterica serovar Typhimurium within macrophages, which was paralleled by a reduced formation of nitric oxide, tumour necrosis factor-alpha and interleukin-6 in Slc11a1-negative macrophages following Salmonella infection, whereas interleukin-10 production was increased. Moreover, Slc11a1-negative phagocytes exhibited higher cellular iron content, resulting in increased iron acquisition by intracellular Salmonella. Our observations indicate a bifunctional role for Slc11a1 within phagocytes. Slc11a restricts iron availability, which first augments pro-inflammatory macrophage effector functions and second concomitantly limits microbial iron access.

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By transporting divalent cations out of phagolysosomes, NRAMP1 deprives pathogens of these cations as essential nutrients.
“In doing so, it deprives pathogens of these cations as essential nutrients (Cunrath and Bumann, 2020;Nairz et al., 2009).”
From Iron in infection and immunity (2020) · cites this paper as Nairz et al., 2009
Nramp1 cation transport function is directly linked to antimicrobial activity of macrophages and DCs.
“Its cation transport function is directly linked to the antimicrobial activity of macrophages and DCs [74, 163, 219].”
From “Pumping iron”—how macrophages handle iron at the systemic, microenvironmental, and cellular levels (2017) · cites this paper as [163]
Murine macrophages lacking functional Nramp1 have higher intracellular iron content, whereas functional Nramp1 decreases intracellular iron content, conferring protection against intracellular infections, an effect traced to modulation of FPN expression.
“Murine Mø lacking functional Nramp1 have a higher intracellular Fe content, whereas functional Nramp1 decreases intracellular Fe content, conferring protection against intracellular infections [145,148,149], an effect traced back to modulation of FPN expression [150].”
From The Iron age of host–microbe interactions (2015) · cites this paper as [150]
NRAMP1 replacement can starve intracellular bacteria for metals such as iron, magnesium, zinc and manganese.
“This replacement can starve intracellular bacteria for these metals”
From Iron in immune cell function and host defense (2021) · cites this paper as [21]

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Macrophage defense mechanisms against intracellular bacteria
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The Iron age of host–microbe interactions
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Host resistance factor SLC11A1 restricts Salmonella growth through magnesium deprivation
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“Pumping iron”—how macrophages handle iron at the systemic, microenvironmental, and cellular levels
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Absence of functional Hfe protects mice from invasive Salmonella enterica Serovar Typhimurium infection via induction of lipocalin-2
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Mechanisms of resistance and susceptibility to experimental visceral leishmaniosis: BALB/c mouse versus syrian hamster model
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The phage shock protein PspA facilitates divalent metal transport and is required for virulence of Salmonella enterica sv. Typhimurium
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The ferric enterobactin transporter Fep is required for persistent Salmonella enterica serovar Typhimurium infection
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Role of Ferroportin in Macrophage-Mediated Immunity
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The hepcidin-ferroportin axis controls the iron content of Salmonella-containing vacuoles in macrophages
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Iron and Heme Metabolism at the Leishmania–Host Interface
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Iron deficiency impairs Intra-hepatic lymphocyte mediated immune response
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Hepcidin as a Major Component of Renal Antibacterial Defenses against Uropathogenic Escherichia coli
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Impact of iron treatment on immune effector function and cellular iron status of circulating monocytes in dialysis patients
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The bacterial siderophore enterobactin confers survival advantage to Salmonella in macrophages
Saha, P., Xiao, X., Yeoh, B. S., Chen, Q., Katkere, B., Kirimanjeswara, G. S., & Vijay–Kumar, M. (2018) · Gut Microbes · doi:10.1080/19490976.2018.1546519 · Cited by 54 · see citing works
Estrogen contributes to regulating iron metabolism through governing ferroportin signaling via an estrogen response element
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Salmonella enterica Causes More Severe Inflammatory Disease in C57/BL6 Nramp1 G169 Mice Than Sv129S6 Mice
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Iron Metabolism and the Inflammatory Response
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Low‐molecular‐weight thiol‐dependent antioxidant and antinitrosative defences in S almonella pathogenesis
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Methionine biosynthesis and transport are functionally redundant for the growth and virulence of Salmonella Typhimurium
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A cell-based infection assay identifies efflux pump modulators that reduce bacterial intracellular load
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The Role of Iron Metabolism in Lung Inflammation and Injury
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The role of endocytic pathways in cellular uptake of plasma non-transferrin iron
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Salmonella Typhimurium general virulence factors: A battle of David against Goliath?
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The iron link between malaria and invasive non-typhoid Salmonella infections
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Nifedipine Affects the Course of Salmonella enterica Serovar Typhimurium Infection by Modulating Macrophage Iron Homeostasis
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A glycine betaine importer limitsSalmonellastress resistance and tissue colonization by reducing trehalose production
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Long-term live-cell imaging reveals new roles forSalmonellaeffector proteins SseG and SteA
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Increased ferroportin-1 expression and rapid splenic iron loss occur with anemia caused by Salmonella enterica serovar Typhimurium infection in mice
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Elemental Ingredients in the Macrophage Cocktail: Role of ZIP8 in Host Response to Mycobacterium tuberculosis
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Comprehensive Single Cell Analyses of the Nutritional Environment of Intracellular Salmonella enterica
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The ferrous iron transporter FtrABCD is required for the virulence of B rucella abortus 2308 in mice
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Severe anaemia, iron deficiency, and susceptibility to invasive bacterial infections
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The late endosomal adaptor p14 is a macrophage host defense factor against Salmonella Typhimurium infection
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Living with Stress
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Indoleamine 2,3-dioxygenase and iron are required for Mycobacterium leprae survival
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Virulence of 32 Salmonella Strains in Mice
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Ammonia exposure causes the disruption of the solute carrier family gene network in pigs
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Leishmania donovani inhibits ferroportin translation by modulating FBXL5-IRP2 axis for its growth within host macrophages
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Tackling microbial iron homeostasis: novel antimicrobial strategies
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Comparative responses of chicken macrophages to infection with Salmonella enterica serovars
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Autophagy Induction by a Small Molecule Inhibits Salmonella Survival in Macrophages and Mice
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Novel insights into cytochrome P450 enzyme and solute carrier families in cadmium-induced liver injury of pigs
Wang, H., Han, Q., Chen, Y., Hu, G., & Xing, H. (2021) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2021.111910 · Cited by 18 · see citing works
Immunometabolic involvement of hepcidin genes in iron homeostasis, storage, and regulation in gilthead seabream (Sparus aurata)
Serna-Duque, J. A., Espinosa‐Ruíz, C., Martínez-López, S., Sánchez‐Ferrer, Á., & Esteban, M. Á. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.1073060 · Cited by 17 · see citing works
Solute carrier protein family 11 member 1 (Slc11a1) activation efficiently inhibits Leishmania donovani survival in host macrophages
Singh, N. K., Gedda, M. R., Tiwari, N. K., Singh, S. P., Bajpai, S., & Singh, S. P. (2016) · Journal of Parasitic Diseases · doi:10.1007/s12639-016-0864-4 · Cited by 17 · see citing works
ZnO-Cu/Mn nanozyme for rescuing the intestinal homeostasis in Salmonella-induced colitis
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Slc11a1 Limits the Intracellular Growth of Salmonella typhimurium by Impairing Bacterial Iron Uptake and Strengthening Macrophage Effector Functions
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Slc11a1 (Nramp1) impairs growth of Salmonella enterica serovar typhimurium in macrophages via stimulation of lipocalin-2 expression
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The co-ordinated regulation of iron homeostasis in murine macrophages limits the availability of iron for intracellularSalmonella typhimurium
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A Salmonella subset exploits erythrophagocytosis to subvert SLC11A1-imposed iron deprivation
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Solute carrier 11a1 (Slc11a1; formerly Nramp1) regulates metabolism and release of iron acquired by phagocytic, but not transferrin-receptor-mediated, iron uptake
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Authors: Nairz, M., Fritsche, G., Crouch, M.-L. V., Barton, H. C., Fang, F. C., & Weiss, G.
Affiliations: Innsbruck Medical University (AT)
University of Southampton (GB)
University of Washington (US)
Corresponding author: Weiss, Günter
ORCID: Nairz, Manfred
Fritsche, Gernot
Fang, Ferric C.
Weiss, Günter
Venue: Cellular Microbiology
Publisher: Hindawi Limited
Published: 2009-09
Volume: 11
Issue: 9
Pages: 1365-1381
ISSN: 1462-5814 (ISSN-L)
1462-5822
DOI: 10.1111/j.1462-5822.2009.01337.x
PMC: PMC3467104
OpenAlex: W1966633800
Cited by: 100
References: 89
Citations by year: 2026: 3 · 2025: 4 · 2024: 2 · 2023: 4 · 2022: 3 · 2021: 6 · 2020: 7 · 2019: 2 · 2018: 9 · 2017: 7 · 2016: 5 · 2015: 8 · 2014: 3 · 2013: 13 · 2012: 8
FWCI: 12.71
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: doi.wiley.com/10.1002/tdm_license_1.1 (tdm, 2191 d)
Locations: Cellular Microbiology (publishedVersion)
PubMed (publishedVersion)
ePrints Soton (University of Southampton) (acceptedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: European Commission
Austrian Science Fund (P 19664)
Universität Innsbruck
National Institutes of Health
National Institute of Allergy and Infectious Diseases (R01AI077629, R01AI039557, F32AI054052)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: SLC11A1, Salmonella typhimurium, macrophages, iron homeostasis, bacterial iron acquisition, transferrin receptor 1, ferroportin 1, intracellular bacterial growth, nitric oxide, TNF-α, interleukin-6, IL-10, host-pathogen interaction
MeSH terms: Ferroportin, Natural Resistance-associated Macrophage Protein 1, Animals, Cell Line, Iron, Macrophages, Nitric Oxide, Receptors, Transferrin, Salmonella Infections, Animal, Salmonella typhimurium, Tumor Necrosis Factor-alpha, Colony Count, Microbial, Interleukin-6, Interleukin-10, Cation Transport Proteins, Microbial Viability, Mice

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Slc11a1 limits intracellular growth of Salmonella enterica sv. Typhimurium by promoting macrophage immune effector functions and impairing bacterial iron acquisition

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