Nutrient Metal Sequestration by Calprotectin Inhibits Bacterial Superoxide Defense, Enhancing Neutrophil Killing of Staphylococcus aureus
Open accessAbstract
By sequestering manganese and zinc, the neutrophil protein calprotectin plays a crucial role in host defense against bacterial and fungal pathogens. However, the essential processes disrupted by calprotectin remain unknown. We report that calprotectin enhances the sensitivity of Staphylococcus aureus to superoxide through inhibition of manganese-dependent bacterial superoxide defenses, thereby increasing superoxide levels within the bacterial cell. Superoxide dismutase activity is required for full virulence in a systemic model of S. aureus infection, and disruption of staphylococcal superoxide defenses by calprotectin augments the antimicrobial activity of neutrophils promoting in vivo clearance. Calprotectin mutated in two transition metal binding sites and therefore defective in binding manganese and zinc does not inhibit microbial growth, unequivocally linking the antimicrobial properties of calprotectin to metal chelation. These results suggest that calprotectin contributes to host defense by rendering bacterial pathogens more sensitive to host immune effectors and reducing bacterial growth.
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Manganese limitation makes S. aureus more susceptible to oxidative stress.
“Manganese limitation therefore renders S. aureus more susceptible to oxidative stress (Fig. 2) [150].”
From Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity (2012) · cites this paper as [150]
Mutation of staphylococcal sodA and sodM decreases bacterial recovery from infected organs in a murine systemic infection model.
“Mutation of staphylococcal sodA and sodM results in decreased bacterial recovery from infected organs in a murine model of systemic infection.”
From Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity (2012) · cites this paper as [150]
Treatment of S. aureus with calprotectin enhances susceptibility to oxidative stress through inhibition of SodA and SodM.
“Treatment of S. aureus with calprotectin results in enhanced susceptibility to oxidative stress through inhibition of SodA and SodM.”
From Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity (2012) · cites this paper as [150]
In calprotectin-deficient mice, there is no difference in bacterial recovery between wild-type and sodAsodM-inactivated S. aureus.
“However, in calprotectin-deficient mice there is no difference in bacterial recovery between wild-type and sodAsodM-inactivated S. aureus.”
From Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity (2012) · cites this paper as [150]
In S. aureus, calprotectin-mediated manganese restriction inhibits the bacterium's oxidative stress defense program by limiting manganese superoxide dismutase activity.
“In S. aureus, calprotectin-mediated manganese restriction inhibits the bacterium's oxidative stress defense program by limiting manganese superoxide dismutase activity (72).”
From Transition Metals and Virulence in Bacteria (2016) · cites this paper as [72]
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Frye, K. A., Sendra, K. M., Waldron, K. J., & Kehl-Fie, T. E. (2022) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2022.111748 · Cited by 36 · see citing works
Self-citation
- Authors
- Kehl-Fie, T. E., Chitayat, S., Hood, M. I., Damo, S., Restrepo, N., Garcia, C., Munro, K. A., Chazin, W. J., & Skaar, E. P.
- Affiliations
- Vanderbilt University (US)
- Queen's University (CA)
- Corresponding author
- Chazin, Walter J.
- Skaar, Eric P.
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2011-08
- Volume
- 10
- Issue
- 2
- Pages
- 158-164
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC3157011
- OpenAlex
- W2156658768
- Cited by
- 419
- References
- 30
- Citations by year
- 2026: 20 · 2025: 25 · 2024: 24 · 2023: 27 · 2022: 31 · 2021: 38 · 2020: 30 · 2019: 40 · 2018: 27 · 2017: 29 · 2016: 29 · 2015: 30 · 2014: 19 · 2013: 21 · 2012: 24
- FWCI
- 8.95
- 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, 752 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)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (T32HL094296)
- National Cancer Institute (T32CA009582)
- National Institute of General Medical Sciences (T32-GM 07347, T32GM007347, 1 R01GM62112, R01GM062112)
- National Institute of Allergy and Infectious Diseases (R01AI069233, U54AI057157, R01AI073843)
- Division of Chemistry
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › S100 Proteins and Annexins
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Calpain Protease Function and Regulation
- Keywords
- calprotectin, Staphylococcus aureus, manganese superoxide dismutase, zinc, manganese, metal chelation, neutrophil killing, host defense, bacterial virulence, transition metal binding, antimicrobial activity
- MeSH terms
- Animals, Anti-Bacterial Agents, Disease Models, Animal, Male, Manganese, Mice, Inbred C57BL, Neutrophils, Staphylococcal Infections, Staphylococcus aureus, Superoxides, Superoxide Dismutase, Zinc, Oxidative Stress, Leukocyte L1 Antigen Complex, Mice
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