Cited by 328Salmonella and Campylobacter epidemiologyS100 Proteins and AnnexinsBacterial Genetics and Biotechnology

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Zinc Sequestration by the Neutrophil Protein Calprotectin Enhances Salmonella Growth in the Inflamed Gut

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Liu, Janet Z., Jellbauer, Stefan, Poe, Adam J., Ton, Vivian, Pesciaroli, Michele, Kehl-Fie, Thomas E., Restrepo, Nicole A., Hosking, Martin P., Edwards, Robert A., Battistoni, Andrea, Pasquali, Paolo, Lane, Thomas E., Chazin, Walter J., Vogl, Thomas, Roth, Johannes, Skaar, Eric P., Raffatellu, Manuela·2012·Cell Host & Microbe

DOI 10.1016/j.chom.2012.01.017PMC PMC3308348

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Abstract

Neutrophils are innate immune cells that counter pathogens by many mechanisms, including release of antimicrobial proteins such as calprotectin to inhibit bacterial growth. Calprotectin sequesters essential micronutrient metals such as zinc, thereby limiting their availability to microbes, a process termed nutritional immunity. We find that while calprotectin is induced by neutrophils during infection with the gut pathogen Salmonella Typhimurium, calprotectin-mediated metal sequestration does not inhibit S. Typhimurium proliferation. Remarkably, S. Typhimurium overcomes calprotectin-mediated zinc chelation by expressing a high affinity zinc transporter (ZnuABC). A S. Typhimurium znuA mutant impaired for growth in the inflamed gut was rescued in the absence of calprotectin. ZnuABC was also required to promote the growth of S. Typhimurium over that of competing commensal bacteria. Thus, our findings indicate that Salmonella thrives in the inflamed gut by overcoming the zinc sequestration of calprotectin and highlight the importance of zinc acquisition in bacterial intestinal colonization.

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Authors: Liu, J. Z., Jellbauer, S., Poe, A. J., Ton, V., Pesciaroli, M., Kehl-Fie, T. E., Restrepo, N. A., Hosking, M. P., Edwards, R. A., Battistoni, A., Pasquali, P., Lane, T. E., Chazin, W. J., Vogl, T., Roth, J., Skaar, E. P., & Raffatellu, M.
Affiliations: University of California, Irvine (US)
Vanderbilt University (US)
University of Rome Tor Vergata (IT)
Istituto Superiore di Sanità (IT)
University of Münster (DE)
Corresponding author: Raffatellu, Manuela
ORCID: Liu, Janet Z.
Ton, Vivian
Pesciaroli, Michele
Hosking, Martin P.
Edwards, Robert A.
Battistoni, Andrea
Pasquali, Paolo
Lane, Thomas E.
Chazin, Walter J.
Vogl, Thomas
Roth, Johannes
Skaar, Eric P.
Raffatellu, Manuela
Venue: Cell Host & Microbe
Publisher: Elsevier BV
Published: 2012-03
Volume: 11
Issue: 3
Pages: 227-239
ISSN: 1931-3128 (ISSN-L)
DOI: 10.1016/j.chom.2012.01.017
PMC: PMC3308348
OpenAlex: W2039176236
Cited by: 328
References: 50
Citations by year: 2026: 13 · 2025: 23 · 2024: 11 · 2023: 15 · 2022: 21 · 2021: 25 · 2020: 21 · 2019: 20 · 2018: 21 · 2017: 26 · 2016: 29 · 2015: 32 · 2014: 30 · 2013: 26 · 2012: 15
FWCI: 50.66
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 539 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell Host & Microbe (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion, cc-by-nc-nd)
Funders: National Cancer Institute (P30CA062203)
National Institute of General Medical Sciences (R01GM062112, GM62112-08S1)
National Institute of Allergy and Infectious Diseases (AI083663, AI083619, T32 AI60573, AI073843, AI091771, R01AI083663, R21AI083619, T32AI060573, R56AI091771, R01AI073843)
National Institute of Neurological Disorders and Stroke (R01NS041249, NS 041249)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › S100 Proteins and Annexins
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: calprotectin, zinc sequestration, Salmonella typhimurium, nutritional immunity, neutrophils, intestinal inflammation, intestinal colonization, innate immunity
MeSH terms: Animals, Bacterial Proteins, Cecum, Diarrhea, Feces, Immunity, Innate, Inflammation, Mice, Inbred C57BL, Neutrophils, Protein Binding, Salmonella Infections, Animal, Salmonella typhimurium, Transcription, Genetic, Zinc, Mice, Knockout, ATP-Binding Cassette Transporters, Leukocyte L1 Antigen Complex, Mice, Host-Pathogen Interactions

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Zinc Sequestration by the Neutrophil Protein Calprotectin Enhances Salmonella Growth in the Inflamed Gut

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