A Novel P1B-type Mn2+-transporting ATPase Is Required for Secreted Protein Metallation in Mycobacteria
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Transition metals are central for bacterial virulence and host defense. P(1B)-ATPases are responsible for cytoplasmic metal efflux and play roles either in limiting cytosolic metal concentrations or in the maturation of secreted metalloproteins. The P(1B)-ATPase, CtpC, is required for Mycobacterium tuberculosis survival in a mouse model (Sassetti, C. M., and Rubin, E. J. (2003) Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. U.S.A. 100, 12989-12994). CtpC prevents Zn(2+) toxicity, suggesting a role in Zn(2+) export from the cytosol (Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I., Wang, C., Tailleux, L., Tilleul, S., Charriere, G. M., Waddell, S. J., Foti, M., Lugo-Villarino, G., Gao, Q., Maridonneau-Parini, I., Butcher, P. D., Castagnoli, P. R., Gicquel, B., de Chastellièr, C., and Neyrolles, O. (2011) Mycobacterial P1-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10, 248-259). However, key metal-coordinating residues and the overall structure of CtpC are distinct from Zn(2+)-ATPases. We found that isolated CtpC has metal-dependent ATPase activity with a strong preference for Mn(2+) over Zn(2+). In vivo, CtpC is unable to complement Escherichia coli lacking a functional Zn(2+)-ATPase. Deletion of M. tuberculosis or Mycobacterium smegmatis ctpC leads to cytosolic Mn(2+) accumulation but no alterations in other metals levels. Whereas ctpC-deficient M. tuberculosis is sensitive to extracellular Zn(2+), the M. smegmatis mutant is not. Both ctpC mutants are sensitive to oxidative stress, which might explain the Zn(2+)-sensitive phenotype of the M. tuberculosis ctpC mutant. CtpC is a high affinity/slow turnover ATPase, suggesting a role in protein metallation. Consistent with this hypothesis, mutation of CtpC leads to a decrease of Mn(2+) bound to secreted proteins and of the activity of secreted Fe/Mn-superoxide dismutase, particularly in M. smegmatis. Alterations in the assembly of metalloenzymes involved in redox stress response might explain the sensitivity of M. tuberculosis ctpC mutants to oxidative stress and growth and persistence defects in mice infection models.
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Such ATPases may also transport other divalent metals such as manganese, contributing to strengthening bacterial resistance to oxidative stress.
“Such ATPases may also transport other divalent metals such as manganese, thereby contributing to strengthening of bacterial resistance to oxidative stress (243).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [243]
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- Authors
- Padilla-Benavides, T., Long, J. E., Raimunda, D., Sassetti, C. M., & Argüello, J. M.
- Affiliations
- University of Massachusetts Chan Medical School (US)
- Worcester Polytechnic Institute (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Argüello, José M.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2013-04
- Volume
- 288
- Issue
- 16
- Pages
- 11334-11347
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3630897
- OpenAlex
- W2034435585
- Cited by
- 91
- References
- 69
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 6 · 2023: 6 · 2022: 12 · 2021: 8 · 2020: 11 · 2019: 7 · 2018: 4 · 2017: 6 · 2016: 5 · 2015: 8 · 2014: 6 · 2013: 5
- FWCI
- 5.81
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Americanae (AECID Library) (submittedVersion, cc-by-nc-sa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-sa)
- Funders
- Howard Hughes Medical Institute
- U.S. Public Health Service (F32A1093049)
- National Institute of Allergy and Infectious Diseases (F32AI093049, R21AI082484)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Keywords
- P1B-type ATPase, manganese transport, Mycobacterium tuberculosis, Mycobacterium smegmatis, zinc toxicity, metalloproteins, oxidative stress, metal homeostasis, virulence factors
- MeSH terms
- Adenosine Triphosphatases, Animals, Bacterial Proteins, Disease Models, Animal, Humans, Mycobacterium tuberculosis, Superoxide Dismutase, Tuberculosis, Oxidative Stress, Mycobacterium smegmatis, Cation Transport Proteins, Mice
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