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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Salmochelins serve as a competitive advantage for Salmonella to disrupt colonization resistance exerted by commensal E. coli, opening the route for intestinal infection.
“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
The Discussion (page unavailable) says salmochelin confers lipocalin-2 resistance, which benefits S. Typhimurium in the inflamed mouse cecum; it also notes that lipocalin-2 inhibits some commensal E. coli. It does not show salmochelins disrupting colonization resistance exerted by commensal E. coli or opening the route for initial intestinal infection. (LLM, conf=0.86)
Experimental — accuracy not yet measuredBacillus anthracis and Salmonella Typhimurium produce modified stealth siderophores that are not bound by siderocalin.
“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
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).”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Raffatellu et al., 2009
During 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).”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Raffatellu et al., 2009
LCN2 is an infection-induced host antimicrobial that blocks bacterial uptake of iron-loaded siderophores.
“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
Resistance to LCN2 defines a specific adaptation of Salmonella Typhimurium for growth in inflamed intestine.
“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]
Salmochelin facilitates pathogen iron acquisition and proliferation in infectious situations where inflammation induces LCN2 expression.
“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]
Some pathogens counter Lcn2 by making modified siderophores, such as glycosylated enterobactin salmochelin, or structurally unrelated siderophores not bound by Lcn2.
“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]
During Salmonella enterica gastrointestinal infection, salmochelin provides a competitive advantage over commensals, but the probiotic E. coli strain Nissle outcompetes S. enterica for siderophores and reduces its colonization.
“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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- 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 › Biochemistry, Genetics and Molecular Biology › Endocrinology › 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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