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Lipocalin-2 Resistance Confers an Advantage to Salmonella enterica Serotype Typhimurium for Growth and Survival in the Inflamed Intestine
Open accessAbstract
In response to enteric pathogens, the inflamed intestine produces antimicrobial proteins, a process mediated by the cytokines IL-17 and IL-22. Salmonella enterica serotype Typhimurium thrives in the inflamed intestinal environment, suggesting that the pathogen is resistant to antimicrobials it encounters in the intestinal lumen. However, the identity of these antimicrobials and corresponding bacterial resistance mechanisms remain unknown. Here, we report that enteric infection of rhesus macaques and mice with S. Typhimurium resulted in marked Il-17- and IL-22-dependent intestinal epithelial induction and luminal accumulation of lipocalin-2, an antimicrobial protein that prevents bacterial iron acquisition. Resistance to lipocalin-2, mediated by the iroBCDE iroN locus, conferred a competitive advantage to the bacterium in colonizing the inflamed intestine of wild-type but not of lipocalin-2-deficient mice. Thus, resistance to lipocalin-2 defines a specific adaptation of S. Typhimurium for growth in the inflamed intestine.
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In the citing paper
“The latter serve as competitive advantage for Salmonella to disrupt the colonization resistance exerted by commensal E. coli, opening the route for intestinal infection (Raffatellu et al., 2009).”
From Iron in infection and immunity (2020) · cites this paper as Raffatellu et al., 2009
Experimental — accuracy not yet measuredIn the citing paper
“For instance, this strategy is used by B. anthracis and Salmonella Typhimurium, both of which produce modified siderophores that are not bound by siderocalin (Abergel et al., 2006; Raffatellu et al., 2009).”
From Iron in infection and immunity (2013) · cites this paper as Raffatellu et al., 2009
In the citing paper
“The ability of S. Typhimurium to avoid lipocalin-2 mediated defenses provides a selective advantage during inflammation (Raffatellu et al., 2009).”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Raffatellu et al., 2009
In the citing paper
“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).”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Raffatellu et al., 2009
In the citing paper
“Lipocalin 2 (LCN2) is a host antimicrobial factor induced upon infection that inhibits bacterial uptake of iron-laden siderophores (Flo et al., 2004, Raffatellu et al., 2009, Deriu et al., 2013).”
From Iron Regulatory Proteins Mediate Host Resistance to Salmonella Infection (2015) · cites this paper as Raffatellu et al., 2009
In the citing paper
“resistance to LCN2 defines a specific adaptation of Salmonella Typhimurium for growth in inflamed intestine”
From Iron in immune cell function and host defense (2021) · cites this paper as [41]
In the citing paper
“In particular, salmochelin facilitates pathogen iron acquisition and proliferation in infectious situations where inflammation induces LCN2 expression. 133”
From The battle for iron in enteric infections (2020) · cites this paper as [133]
In the citing paper
“This defense strategy is countered by some pathogens, via a mechanism that relies on the production of modified siderophores, such as for example the glycosylated enterobactin salmochelin or the production of structurally unrelated siderophores not bound by Lnc2 (92–94).”
From Innate Nutritional Immunity (2018) · cites this paper as [94]
In the citing paper
“During S. enterica gastrointestinal infection, S. enterica uses salmochelin to gain a competitive advantage over commensals but is outcompeted for siderophores by the probiotic E. coli strain Nissle, which reduces S. enterica colonization (33, 113).”
From Transition Metals and Virulence in Bacteria (2016) · cites this paper as [113]
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Metadata
- Authors
- Raffatellu, M., George, M. D., Akiyama, Y., Hornsby, M. J., Nuccio, S.-P., Paixao, T. A., Butler, B. P., Chu, H., Santos, R. L., Berger, T., Mak, T. W., Tsolis, R. M., Bevins, C. L., Solnick, J. V., Dandekar, S., & Bäumler, A. J.
- Affiliations
- University of California, Irvine (US)
- University of California, Davis (US)
- University Health Network (CA)
- Corresponding author
- Bäumler, Andreas J.
- ORCID
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2009-05
- Volume
- 5
- Issue
- 5
- Pages
- 476-486
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC2768556
- OpenAlex
- W2000707384
- Cited by
- 525
- References
- 54
- Citations by year
- 2026: 20 · 2025: 31 · 2024: 21 · 2023: 21 · 2022: 28 · 2021: 23 · 2020: 38 · 2019: 28 · 2018: 27 · 2017: 33 · 2016: 37 · 2015: 41 · 2014: 39 · 2013: 37 · 2012: 28
- FWCI
- 53.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Host & Microbe (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (T32-AI60555, R01AI044170, R01AI042081, AI 43274, AI 040124, AI044170, AI079173, R21AI079173, AI 42081, R01AI043274, R29AI040124, R01AI050843, AI50843, R01AI076246, R01AI040124, R01AI050553, AI050553, R37AI032738, T32AI060555)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK43183, R01DK043183, DK 61297, R01DK061297)
- National Institute of Dental and Craniofacial Research (DE018097, R21DE018097)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
- Keywords
- Salmonella typhimurium, neutrophil gelatinase-associated lipocalin, iron acquisition, IL-17, IL-22, intestinal inflammation, antimicrobial proteins, bacterial colonization, rhesus monkeys, mice, host-pathogen interaction
- MeSH terms
- Interleukin-22, Animals, Cell Line, Disease Models, Animal, Humans, Interleukins, Intestines, Macaca mulatta, Mice, Inbred C57BL, Salmonella Infections, Salmonella typhimurium, Gene Expression, Siderophores, Interleukin-17, Mice, Lipocalins, Host-Pathogen Interactions
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