Slc11a1 (Nramp1) impairs growth of Salmonella enterica serovar typhimurium in macrophages via stimulation of lipocalin-2 expression
Open accessAbstract
Nramp1 confers resistance of macrophages to Salmonella Typhimurium via NF-κB-dependent induction of the siderophore capturing peptide lipocalin-2. The expression of the cation transporter Nramp1 (Slc11a1) in late phagolysosomes confers resistance to infection with several intracellular pathogens, such as Salmonella enterica, in mice. The antimicrobial actions of Nramp1 are attributable, in part, to modulation of macrophage immune function and cellular iron metabolism—the latter affecting the availability of the essential nutrient iron for intraphagosomal bacteria. Here, we provide novel evidence that Nramp1 functionality increases the expression of the peptide Lcn2, which exerts its antimicrobial activity by scavenging iron-loaded bacterial siderophores and mediating iron efflux from macrophages. With the use of macrophage cell lines expressing functional or nonfunctional Nramp1, we found significantly elevated Lcn2 mRNA and protein levels in Nramp1-expressing cells. These resulted from Nramp1-mediated alterations in the production of ROS, which stimulated NF-κB activity and subsequently, Lcn2 transcription. We observed that increased Lcn2 levels in primary Nramp1-positive macrophages resulted in a significant suppression of S. enterica serovar typhimurium growth. Stimulation of Lcn2 expression is a novel mechanism by which Nramp1 confers resistance against infection with the intracellular bacterium S. typhimurium.
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Functional NRAMP1 stimulates the expression of NGAL.
“In addition functional NRAMP1 also stimulates the expression of NGAL, an independent nutritional immune mediator (Fritsche et al., 2012).”
From Iron in infection and immunity (2020) · cites this paper as Fritsche et al., 2012
Nramp1 expression increases Lcn2 formation, which contributes to the control of infection at least with intra-macrophage Salmonella.
“In addition, Nramp1 expression increases Lcn2 formation, which contributes to the control of infection at least with intra-macrophage Salmonella (228).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [228]
RAW264.7 macrophages expressing functional Nramp1 exhibited lower iron uptake via TfR and increased iron release via increased ferroportin expression, resulting in reduced cellular iron content.
“Investigations of RAW264.7 MO cell line stably transfected with functional or non-functional Nramp1 demonstrated that MΦs expressing functional Nramp1 exhibited a lower iron uptake via TfR and an increased iron release mediated via increased ferroportin expression, resulting in reduced cellular iron content (228).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [228]
NRAMP1 confers resistance to intracellular bacteria such as Salmonella via induction of Lcn2 expression, and Lcn2 can control proliferation of intracellular bacteria that do not produce siderophores, such as Chlamydia pneumoniae.
“There is at least one additional mechanism by which NRAMP1 confers resistance to intracellular bacteria such as Salmonella, namely via the induction of Lcn2 expression [156].Of note, Lcn2 can control the proliferation of intracellular bacteria that do not produce siderophores, such as Chlamydia pneumonia [157] (Fig 3).”
From The Iron age of host–microbe interactions (2015) · cites this paper as [156]
Functional Nramp1 expression in RAW264.7 macrophages is associated with significantly lower intracellular Salmonella multiplication than in macrophages lacking Nramp1 activity.
“As described in the literature the intracellular multiplication of Salmonella was significantly lower in RAW cells expressing the functional Nramp1 than in macrophages lacking Nramp1 activity (Cellier et al, 2007; Fritsche et al, 2012).”
From Heme oxygenase 1 controls early innate immune response of macrophages to<i>Salmonella</i>Typhimurium infection: Heme oxygenase 1 expression affects Salmonella<i>infection</i> (2016) · cites this paper as Fritsche et al, 2012
NRAMP1 expression impacts other iron-linked immune nutritional pathways such as lipocalin-2 and NO formation.
“Thereby, NRAMP1 expression also impacts on other iron linked immune nutritional pathways such as lipocalin-2 and NO formation”
From Iron in immune cell function and host defense (2021) · cites this paper as [35]
nramp1 expression in macrophages induces the host siderophore-sequestering protein lipocalin 2, uncovering a regulatory link between multiple mechanisms of nutritional immunity.
“Additionally, nramp1 expression in macrophages induces the host siderophore-sequestering protein lipocalin 2, uncovering a regulatory link between multiple mechanisms of nutritional immunity (45).”
From Transition Metals and Virulence in Bacteria (2016) · cites this paper as [45]
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“It is important to note that the strain of mouse used for most of these studies has been C57BL/6 mice, which has a non-functional allele of Nramp1, a divalent metal (iron and manganese) transporter that renders themmore susceptible to infections (Canonne-Hergaux et al., 1999; Fritsche et al., 2012; Loomis et al., 2014…”
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- Authors
- Fritsche, G., Nairz, M., Libby, S. J., Fang, F. C., & Weiss, G.
- Affiliations
- Innsbruck Medical University (AT)
- University of Washington (US)
- Corresponding author
- Weiss, Günter
- Venue
- Journal of Leukocyte Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-08-01
- Volume
- 92
- Issue
- 2
- Pages
- 353-359
- ISSN
- 0741-5400 (ISSN-L)
- 1938-3673
- PMC
- PMC3395419
- OpenAlex
- W2129432699
- Semantic Scholar
- c50a0036a36c0fba44de0529a57dac23d157cbd0
- Cited by
- 72
- References
- 41
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 5 · 2023: 4 · 2022: 4 · 2021: 5 · 2020: 5 · 2019: 4 · 2018: 4 · 2017: 3 · 2016: 4 · 2015: 5 · 2014: 10 · 2013: 11 · 2012: 4
- FWCI
- 13.82
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Journal of Leukocyte Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Austrian Science Fund (TRP188)
- Verein zur Förderung von Forschung und Weiterbildung in Infektiologie und Immunologie an der Medizinischen Universität Innsbruck
- U.S. National Institutes of Health (AI39557, AI48622, AI77629)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Keywords
- NRAMP1, SLC11A1, neutrophil gelatinase-associated lipocalin, Salmonella typhimurium, macrophages, iron metabolism, reactive oxygen species, NF-κB signaling, phagolysosomes, intracellular bacterial infection, antimicrobial resistance
- MeSH terms
- Lipocalin-2, Natural Resistance-associated Macrophage Protein 1, Acute-Phase Proteins, Animals, Cell Line, Deferoxamine, Hydrogen Peroxide, Immunity, Innate, Iron, Macrophages, Mice, Inbred BALB C, Mice, Inbred C57BL, Salmonella Infections, Animal, Salmonella typhimurium, Oncogene Proteins, NF-kappa B, Siderophores, Reactive Nitrogen Species, Cation Transport Proteins, Mice, Lipocalins
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