Staphylococcus aureus lacking a functional MntABC manganese import system has increased resistance to copper.
Identifieur interne : 000038 ( Main/Exploration ); précédent : 000037; suivant : 000039Staphylococcus aureus lacking a functional MntABC manganese import system has increased resistance to copper.
Auteurs : Hassan Al-Tameemi [États-Unis] ; William N. Beavers [États-Unis] ; Javiera Norambuena [États-Unis] ; Eric P. Skaar [États-Unis] ; Jeffrey M. Boyd [États-Unis]Source :
- Molecular microbiology [ 1365-2958 ] ; 2020.
Abstract
S. aureus USA300 isolates utilize the copBL and copAZ gene products to prevent Cu intoxication. We created and examined a ΔcopAZ ΔcopBL mutant strain (cop-). The cop- strain was sensitive to Cu and accumulated intracellular Cu. We screened a transposon (Tn) mutant library in the cop- background and isolated strains with Tn insertions in the mntABC operon that permitted growth in the presence of Cu. The mutations were in mntA and they were recessive. Under the growth conditions utilized, MntABC functioned in manganese (Mn) import. When cultured with Cu, strains containing a mntA::Tn accumulated less Cu than the parent strain. Mn(II) supplementation improved growth when cop- was cultured with Cu and this phenotype was dependent upon the presence of MntR, which is a repressor of mntABC transcription. A ΔmntR strain had an increased Cu load and decreased growth in the presence of Cu, which was abrogated by the introduction of mntA::Tn. Over-expression of mntABC increased cellular Cu load and sensitivity to Cu. The presence of a mntA::Tn mutation protected iron-sulfur (FeS) enzymes from inactivation by Cu. The data presented are consistent with a model wherein defective MntABC results in decreased cellular Cu accumulation and protection to FeS enzymes from Cu poisoning.
DOI: 10.1111/mmi.14623
PubMed: 33034093
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Beavers</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Norambuena, Javiera" sort="Norambuena, Javiera" uniqKey="Norambuena J" first="Javiera" last="Norambuena">Javiera Norambuena</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Skaar, Eric P" sort="Skaar, Eric P" uniqKey="Skaar E" first="Eric P" last="Skaar">Eric P. Skaar</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Boyd, Jeffrey M" sort="Boyd, Jeffrey M" uniqKey="Boyd J" first="Jeffrey M" last="Boyd">Jeffrey M. Boyd</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:33034093</idno><idno type="pmid">33034093</idno><idno type="doi">10.1111/mmi.14623</idno><idno type="wicri:Area/Main/Corpus">000021</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000021</idno><idno type="wicri:Area/Main/Curation">000021</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000021</idno><idno type="wicri:Area/Main/Exploration">000021</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Staphylococcus aureus lacking a functional MntABC manganese import system has increased resistance to copper.</title><author><name sortKey="Al Tameemi, Hassan" sort="Al Tameemi, Hassan" uniqKey="Al Tameemi H" first="Hassan" last="Al-Tameemi">Hassan Al-Tameemi</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Beavers, William N" sort="Beavers, William N" uniqKey="Beavers W" first="William N" last="Beavers">William N. Beavers</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Norambuena, Javiera" sort="Norambuena, Javiera" uniqKey="Norambuena J" first="Javiera" last="Norambuena">Javiera Norambuena</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Skaar, Eric P" sort="Skaar, Eric P" uniqKey="Skaar E" first="Eric P" last="Skaar">Eric P. Skaar</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Boyd, Jeffrey M" sort="Boyd, Jeffrey M" uniqKey="Boyd J" first="Jeffrey M" last="Boyd">Jeffrey M. Boyd</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author></analytic><series><title level="j">Molecular microbiology</title><idno type="eISSN">1365-2958</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">S. aureus USA300 isolates utilize the copBL and copAZ gene products to prevent Cu intoxication. We created and examined a ΔcopAZ ΔcopBL mutant strain (cop-). The cop- strain was sensitive to Cu and accumulated intracellular Cu. We screened a transposon (Tn) mutant library in the cop- background and isolated strains with Tn insertions in the mntABC operon that permitted growth in the presence of Cu. The mutations were in mntA and they were recessive. Under the growth conditions utilized, MntABC functioned in manganese (Mn) import. When cultured with Cu, strains containing a mntA::Tn accumulated less Cu than the parent strain. Mn(II) supplementation improved growth when cop- was cultured with Cu and this phenotype was dependent upon the presence of MntR, which is a repressor of mntABC transcription. A ΔmntR strain had an increased Cu load and decreased growth in the presence of Cu, which was abrogated by the introduction of mntA::Tn. Over-expression of mntABC increased cellular Cu load and sensitivity to Cu. The presence of a mntA::Tn mutation protected iron-sulfur (FeS) enzymes from inactivation by Cu. The data presented are consistent with a model wherein defective MntABC results in decreased cellular Cu accumulation and protection to FeS enzymes from Cu poisoning.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33034093</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>25</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1365-2958</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Oct</Month><Day>08</Day></PubDate></JournalIssue><Title>Molecular microbiology</Title><ISOAbbreviation>Mol Microbiol</ISOAbbreviation></Journal><ArticleTitle>Staphylococcus aureus lacking a functional MntABC manganese import system has increased resistance to copper.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/mmi.14623</ELocationID><Abstract><AbstractText>S. aureus USA300 isolates utilize the copBL and copAZ gene products to prevent Cu intoxication. We created and examined a ΔcopAZ ΔcopBL mutant strain (cop-). The cop- strain was sensitive to Cu and accumulated intracellular Cu. We screened a transposon (Tn) mutant library in the cop- background and isolated strains with Tn insertions in the mntABC operon that permitted growth in the presence of Cu. The mutations were in mntA and they were recessive. Under the growth conditions utilized, MntABC functioned in manganese (Mn) import. When cultured with Cu, strains containing a mntA::Tn accumulated less Cu than the parent strain. Mn(II) supplementation improved growth when cop- was cultured with Cu and this phenotype was dependent upon the presence of MntR, which is a repressor of mntABC transcription. A ΔmntR strain had an increased Cu load and decreased growth in the presence of Cu, which was abrogated by the introduction of mntA::Tn. Over-expression of mntABC increased cellular Cu load and sensitivity to Cu. The presence of a mntA::Tn mutation protected iron-sulfur (FeS) enzymes from inactivation by Cu. The data presented are consistent with a model wherein defective MntABC results in decreased cellular Cu accumulation and protection to FeS enzymes from Cu poisoning.</AbstractText><CopyrightInformation>© 2020 John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Al-Tameemi</LastName><ForeName>Hassan</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Beavers</LastName><ForeName>William N</ForeName><Initials>WN</Initials><AffiliationInfo><Affiliation>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Norambuena</LastName><ForeName>Javiera</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Skaar</LastName><ForeName>Eric P</ForeName><Initials>EP</Initials><AffiliationInfo><Affiliation>Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Boyd</LastName><ForeName>Jeffrey M</ForeName><Initials>JM</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-7721-3926</Identifier><AffiliationInfo><Affiliation>Department of Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>1R01AI139100-01</GrantID><Agency>Division of Intramural Research, National Institute of Allergy and Infectious Diseases</Agency><Country></Country></Grant><Grant><GrantID>MCB-1750624</GrantID><Agency>NSF</Agency><Country></Country></Grant><Grant><GrantID>NE-1028</GrantID><Agency>USDA MRF</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>08</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Mol Microbiol</MedlineTA><NlmUniqueID>8712028</NlmUniqueID><ISSNLinking>0950-382X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Staphylococcus aureus
</Keyword><Keyword MajorTopicYN="N">MntABC</Keyword><Keyword MajorTopicYN="N">copper</Keyword><Keyword MajorTopicYN="N">iron-sulfur cluster</Keyword><Keyword MajorTopicYN="N">manganese</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>08</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>09</Month><Day>28</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>10</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>10</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>10</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>10</Month><Day>9</Day><Hour>5</Hour><Minute>42</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33034093</ArticleId><ArticleId IdType="doi">10.1111/mmi.14623</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Achard, M.E., Stafford, S.L., Bokil, N.J., Chartres, J., Bernhardt, P.V., Schembri, M.A., et al. (2012) Copper redistribution in murine macrophages in response to Salmonella infection. The Biochemical Journal, 444, 51-57.</Citation></Reference><Reference><Citation>Andreini, C., Banci, L., Bertini, I. and Rosato, A. (2008) Occurrence of copper proteins through the three domains of life: a bioinformatic approach. Journal of Proteome Research, 7, 209-216.</Citation></Reference><Reference><Citation>Anjem, A. and Imlay, J.A. (2012) Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. Journal of Biological Chemistry, 287, 15544-15556.</Citation></Reference><Reference><Citation>Arguello, J.M., Eren, E. and Gonzalez-Guerrero, M. (2007) The structure and function of heavy metal transport P1B-ATPases. BioMetals, 20, 233-248.</Citation></Reference><Reference><Citation>Bae, T., Banger, A.K., Wallace, A., Glass, E.M., Aslund, F., Schneewind, O., et al. (2004) Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proceedings of the National Academy of Sciences, 101, 12312-12317.</Citation></Reference><Reference><Citation>Bae, T., Glass, E.M., Schneewind, O. and Missiakas, D. (2008) Generating a collection of insertion mutations in the Staphylococcus aureus genome using bursa aurealis. Methods in Molecular Biology, 416, 103-116.</Citation></Reference><Reference><Citation>Baker, J., Sitthisak, S., Sengupta, M., Johnson, M., Jayaswal, R.K. and Morrissey, J.A. (2010) Copper stress induces a global stress response in Staphylococcus aureus and represses sae and agr expression and biofilm formation. Applied and Environment Microbiology, 76, 150-160.</Citation></Reference><Reference><Citation>Banci, L., Bertini, I., Del Conte, R., Markey, J. and Ruiz-Duenas, F.J. (2001) Copper trafficking: the solution structure of Bacillus subtilis CopZ. Biochemistry, 40, 15660-15668.</Citation></Reference><Reference><Citation>Becker, K.W. and Skaar, E.P. (2014) Metal limitation and toxicity at the interface between host and pathogen. FEMS Microbiology Reviews, 38, 1235-1249.</Citation></Reference><Reference><Citation>Begg, S.L. (2019) The role of metal ions in the virulence and viability of bacterial pathogens. Biochemical Society Transactions, 47, 77-87.</Citation></Reference><Reference><Citation>Beinert, H., Kennedy, M.C. and Stout, C.D. (1996) Aconitase as iron-sulfur protein, enzyme, and iron-regulatory protein. Chemical reviews, 96, 2335-2373.</Citation></Reference><Reference><Citation>Beveridge, S.J., Garrett, I.R., Whitehouse, M.W., Vernon-Roberts, B. and Brooks, P.M. (1985) Biodistribution of 64Cu in inflamed rats following administration of two anti-inflammatory copper complexes. Agents and Actions, 17, 104-111.</Citation></Reference><Reference><Citation>Borremans, B., Hobman, J.L., Provoost, A., Brown, N.L. and van Der Lelie, D. (2001) Cloning and functional analysis of the pbr lead resistance determinant of Ralstonia metallidurans CH34. Journal of Bacteriology, 183, 5651-5658.</Citation></Reference><Reference><Citation>Bose, J.L., Fey, P.D. and Bayles, K.W. (2013) Genetic tools to enhance the study of gene function and regulation in Staphylococcus aureus. Applied and Environment Microbiology, 79, 2218-2224.</Citation></Reference><Reference><Citation>Brancaccio, D., Gallo, A., Piccioli, M., Novellino, E., Ciofi-Baffoni, S. and Banci, L. (2017) [4Fe-4S] Cluster assembly in mitochondria and its impairment by copper. Journal of the American Chemical Society, 139, 719-730.</Citation></Reference><Reference><Citation>Chandrangsu, P. and Helmann, J.D. (2016) Intracellular Zn(II) intoxication leads to dysregulation of the PerR regulon resulting in heme toxicity in Bacillus subtilis. PLoS Genetics, 12, e1006515.</Citation></Reference><Reference><Citation>Chandrangsu, P., Rensing, C. and Helmann, J.D. (2017) Metal homeostasis and resistance in bacteria. Nature Reviews Microbiology, 15, 338-350.</Citation></Reference><Reference><Citation>Chillappagari, S., Seubert, A., Trip, H., Kuipers, O.P., Marahiel, M.A. and Miethke, M. (2010) Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis. Journal of Bacteriology, 192, 2512-2524.</Citation></Reference><Reference><Citation>Claverys, J.P. (2001) A new family of high-affinity ABC manganese and zinc permeases. Research in Microbiology, 152, 231-243.</Citation></Reference><Reference><Citation>Cotruvo, J.A. Jr and Stubbe, J. (2012) Metallation and mismetallation of iron and manganese proteins in vitro and in vivo: the class I ribonucleotide reductases as a case study. Metallomics, 4, 1020-1036.</Citation></Reference><Reference><Citation>Counago, R.M., Ween, M.P., Begg, S.L., Bajaj, M., Zuegg, J., O'Mara, M.L., et al. (2014) Imperfect coordination chemistry facilitates metal ion release in the Psa permease. Nature Chemical Biology, 10, 35-41.</Citation></Reference><Reference><Citation>Dintilhac, A., Alloing, G., Granadel, C. and Claverys, J.P. (1997) Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Molecular Microbiology, 25, 727-739.</Citation></Reference><Reference><Citation>Djoko, K.Y. and McEwan, A.G. (2013) Antimicrobial action of copper is amplified via inhibition of heme biosynthesis. ACS Chemical Biology, 8, 2217-2223.</Citation></Reference><Reference><Citation>Dollwet, H.H. and Sorenson, J.R. (1985) Historic uses of copper compounds in medicine (pp. 80-87). Arkansas: Humana Press Inc.</Citation></Reference><Reference><Citation>Ekici, S., Yang, H., Koch, H.G. and Daldal, F. (2012) Novel transporter required for biogenesis of cbb3-type cytochrome c oxidase in Rhodobacter capsulatus. mBio, 3, e00293-11.</Citation></Reference><Reference><Citation>Fey, P.D., Endres, J.L., Yajjala, V.K., Widhelm, T.J., Boissy, R.J., Bose, J.L., et al. (2013) A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. mBio, 4, e00537-12</Citation></Reference><Reference><Citation>Forsyth, R.A., Haselbeck, R.J., Ohlsen, K.L., Yamamoto, R.T., Xu, H., Trawick, J.D., et al. (2002) A genome-wide strategy for the identification of essential genes in Staphylococcus aureus. Molecular Microbiology, 43, 1387-1400.</Citation></Reference><Reference><Citation>Gaballa, A. and Helmann, J.D. (2003) Bacillus subtilis CPx-type ATPases: characterization of Cd, Zn, Co and Cu efflux systems. BioMetals, 16, 497-505.</Citation></Reference><Reference><Citation>Gardner, P.R. and Fridovich, I. (1991) Superoxide sensitivity of the Escherichia coli aconitase. Journal of Biological Chemistry, 266, 19328-19333.</Citation></Reference><Reference><Citation>Glasfeld, A., Guedon, E., Helmann, J.D. and Brennan, R.G. (2003) Structure of the manganese-bound manganese transport regulator of Bacillus subtilis. Natural Structural Biology, 10, 652-657.</Citation></Reference><Reference><Citation>Grass, G., Franke, S., Taudte, N., Nies, D.H., Kucharski, L.M., Maguire, M.E., et al. (2005) The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. Journal of Bacteriology, 187, 1604-1611.</Citation></Reference><Reference><Citation>Grass, G., Rensing, C. and Solioz, M. (2011) Metallic copper as an antimicrobial surface. Applied and Environment Microbiology, 77, 1541-1547.</Citation></Reference><Reference><Citation>Gribenko, A., Mosyak, L., Ghosh, S., Parris, K., Svenson, K., Moran, J., et al. (2013) Three-dimensional structure and biophysical characterization of Staphylococcus aureus cell surface antigen-manganese transporter MntC. Journal of Molecular Biology, 425, 3429-3445.</Citation></Reference><Reference><Citation>Grosser, M.R., Paluscio, E., Thurlow, L.R., Dillon, M.M., Cooper, V.S., Kawula, T.H., et al. (2018) Genetic requirements for Staphylococcus aureus nitric oxide resistance and virulence. PLOS Pathogens, 14, e1006907.</Citation></Reference><Reference><Citation>Grosser, M.R. and Richardson, A.R. (2016) Method for Preparation and Electroporation of S. aureus and S. epidermidis. Methods in Molecular Biology, 1373, 51-57.</Citation></Reference><Reference><Citation>Grossoehme, N., Kehl-Fie, T.E., Ma, Z., Adams, K.W., Cowart, D.M., Scott, R.A., et al. (2011) Control of copper resistance and inorganic sulfur metabolism by paralogous regulators in Staphylococcus aureus. Journal of Biological Chemistry, 286, 13522-13531.</Citation></Reference><Reference><Citation>Gu, M. and Imlay, J.A. (2013) Superoxide poisons mononuclear iron enzymes by causing mismetallation. Molecular Microbiology, 89, 123-134.</Citation></Reference><Reference><Citation>Guan, G., Pinochet-Barros, A., Gaballa, A., Patel, S.J., Arguello, J.M. and Helmann, J.D. (2015) PfeT, a P1B4 -type ATPase, effluxes ferrous iron and protects Bacillus subtilis against iron intoxication. Molecular Microbiology, 98, 787-803.</Citation></Reference><Reference><Citation>Gupta, A., Matsui, K., Lo, J.F. and Silver, S. (1999) Molecular basis for resistance to silver cations in Salmonella. Nature medicine, 5, 183-188.</Citation></Reference><Reference><Citation>Handke, L.D., Hawkins, J.C., Miller, A.A., Jansen, K.U. and Anderson, A.S. (2013) Regulation of Staphylococcus aureus MntC expression and its role in response to oxidative stress. PLoS One, 8, e77874.</Citation></Reference><Reference><Citation>Hao, Z., Chen, S. and Wilson, D.B. (1999) Cloning, expression, and characterization of cadmium and manganese uptake genes from Lactobacillus plantarum. Applied and Environment Microbiology, 65, 4746-4752.</Citation></Reference><Reference><Citation>Hodgkinson, V. and Petris, M.J. (2012) Copper homeostasis at the host-pathogen interface. Journal of Biological Chemistry, 287, 13549-13555.</Citation></Reference><Reference><Citation>Horsburgh, M.J., Ingham, E. and Foster, S.J. (2001) In Staphylococcus aureus, Fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. Journal of Bacteriology, 183, 468-475.</Citation></Reference><Reference><Citation>Horsburgh, M.J., Wharton, S.J., Cox, A.G., Ingham, E., Peacock, S. and Foster, S.J. (2002) MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Molecular Microbiology, 44, 1269-1286.</Citation></Reference><Reference><Citation>Huang, X., Shin, J.H., Pinochet-Barros, A., Su, T.T. and Helmann, J.D. (2017) Bacillus subtilis MntR coordinates the transcriptional regulation of manganese uptake and efflux systems. Molecular Microbiology, 103, 253-268.</Citation></Reference><Reference><Citation>Imlay, J.A. (2014) The mismetallation of enzymes during oxidative stress. Journal of Biological Chemistry, 289, 28121-28128.</Citation></Reference><Reference><Citation>Jaroslawiecka, A. and Piotrowska-Seget, Z. (2014) Lead resistance in micro-organisms. Microbiology, 160, 12-25.</Citation></Reference><Reference><Citation>Johnson, M.D., Kehl-Fie, T.E. and Rosch, J.W. (2015) Copper intoxication inhibits aerobic nucleotide synthesis in Streptococcus pneumoniae. Metallomics, 7, 786-794.</Citation></Reference><Reference><Citation>Johnston, J.W., Briles, D.E., Myers, L.E. and Hollingshead, S.K. (2006) Mn2+-dependent regulation of multiple genes in Streptococcus pneumoniae through PsaR and the resultant impact on virulence. Infection and Immunity, 74, 1171-1180.</Citation></Reference><Reference><Citation>Joska, T.M., Mashruwala, A., Boyd, J.M. and Belden, W.J. (2014) A universal cloning method based on yeast homologous recombination that is simple, efficient, and versatile. Journal of Microbiol Methods, 100, 46-51.</Citation></Reference><Reference><Citation>Kehl-Fie, T.E., Zhang, Y., Moore, J.L., Farrand, A.J., Hood, M.I., Rathi, S., et al. (2013) MntABC and MntH contribute to systemic Staphylococcus aureus infection by competing with calprotectin for nutrient manganese. Infection and Immunity, 81, 3395-3405.</Citation></Reference><Reference><Citation>Kim, J., Senadheera, D.B., Levesque, C.M. and Cvitkovitch, D.G. (2012) TcyR regulates L-cystine uptake via the TcyABC transporter in Streptococcus mutans. FEMS Microbiology Letters, 328, 114-121.</Citation></Reference><Reference><Citation>Kreiswirth, B.N., Lofdahl, S., Betley, M.J., O'Reilly, M., Schlievert, P.M., Bergdoll, M.S., et al. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature, 305, 709-712.</Citation></Reference><Reference><Citation>Laddaga, R.A. and Silver, S. (1985) Cadmium uptake in Escherichia coli K-12. Journal of Bacteriology, 162, 1100-1105.</Citation></Reference><Reference><Citation>Ladomersky, E., Khan, A., Shanbhag, V., Cavet, J.S., Chan, J., Weisman, G.A., et al. (2017) Host and pathogen copper-transporting P-type ATPases function antagonistically during Salmonella infection. Infection and Immunity, 85, e00351-17.</Citation></Reference><Reference><Citation>Lalaouna, D., Baude, J., Wu, Z., Tomasini, A., Chicher, J., Marzi, S., et al. (2019) RsaC sRNA modulates the oxidative stress response of Staphylococcus aureus during manganese starvation. Nucleic Acids Research, 47, 9871-9887.</Citation></Reference><Reference><Citation>Lei, M.G., Cue, D., Roux, C.M., Dunman, P.M. and Lee, C.Y. (2011) Rsp inhibits attachment and biofilm formation by repressing fnbA in Staphylococcus aureus MW2. Journal of Bacteriology, 193, 5231-5241.</Citation></Reference><Reference><Citation>Li, N., Yang, X.Y., Guo, Z., Zhang, J., Cao, K., Han, J., et al. (2014) Varied metal-binding properties of lipoprotein PsaA in Streptococcus pneumoniae. Journal of Biological Inorganic Chemistry, 19, 829-838.</Citation></Reference><Reference><Citation>Lim, K.H., Jones, C.E., vanden Hoven, R.N., Edwards, J.L., Falsetta, M.L., Apicella, M.A., et al. (2008) Metal binding specificity of the MntABC permease of Neisseria gonorrhoeae and its influence on bacterial growth and interaction with cervical epithelial cells. Infection and Immunity, 76, 3569-3576.</Citation></Reference><Reference><Citation>Lisher, J.P., Higgins, K.A., Maroney, M.J. and Giedroc, D.P. (2013) Physical characterization of the manganese-sensing pneumococcal surface antigen repressor from Streptococcus pneumoniae. Biochemistry, 52, 7689-7701.</Citation></Reference><Reference><Citation>Luong, T.T. and Lee, C.Y. (2007) Improved single-copy integration vectors for Staphylococcus aureus. Journal of Microbiol Methods, 70, 186-190.</Citation></Reference><Reference><Citation>Ma, Z., Cowart, D.M., Scott, R.A. and Giedroc, D.P. (2009) Molecular insights into the metal selectivity of the copper(I)-sensing repressor CsoR from Bacillus subtilis. Biochemistry, 48, 3325-3334.</Citation></Reference><Reference><Citation>Macomber, L. and Imlay, J.A. (2009) The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proceedings of the National Academy of Sciences, 106, 8344-8349.</Citation></Reference><Reference><Citation>Malachowa, N. and DeLeo, F.R. (2010) Mobile genetic elements of Staphylococcus aureus. Cellular and Molecular Life Sciences, 67, 3057-3071.</Citation></Reference><Reference><Citation>Martin, J.E. and Imlay, J.A. (2011) The alternative aerobic ribonucleotide reductase of Escherichia coli, NrdEF, is a manganese-dependent enzyme that enables cell replication during periods of iron starvation. Molecular Microbiology, 80, 319-334.</Citation></Reference><Reference><Citation>Mashruwala, A.A., Bhatt, S., Poudel, S., Boyd, E.S. and Boyd, J.M. (2016a) The DUF59 containing protein SufT is involved in the maturation of iron-sulfur (FeS) proteins during conditions of High FeS cofactor demand in Staphylococcus aureus. PLoS Genetics, 12, e1006233.</Citation></Reference><Reference><Citation>Mashruwala, A.A. and Boyd, J.M. (2015) De Novo assembly of plasmids using yeast recombinational cloning. Methods in Molecular Biology, 1373, 33-41.</Citation></Reference><Reference><Citation>Mashruwala, A.A. and Boyd, J.M. (2017) The Staphylococcus aureus SrrAB regulatory system modulates hydrogen peroxide resistance factors, which imparts protection to aconitase during aerobic growth. PLoS One, 12, e0170283.</Citation></Reference><Reference><Citation>Mashruwala, A.A., Pang, Y.Y., Rosario-Cruz, Z., Chahal, H.K., Benson, M.A., Mike, L.A., et al. (2015) Nfu facilitates the maturation of iron-sulfur proteins and participates in virulence in Staphylococcus aureus. Molecular Microbiology, 95, 383-409.</Citation></Reference><Reference><Citation>Mashruwala, A.A., Roberts, C.A., Bhatt, S., May, K.L., Carroll, R.K., Shaw, L.N., et al. (2016b) Staphylococcus aureus SufT: An essential iron-sulfur cluster assembly factor in cells experiencing a high-demand for lipoic acid. Molecular Microbiology, 102, 1099-1119.</Citation></Reference><Reference><Citation>McAllister, L.J., Tseng, H.J., Ogunniyi, A.D., Jennings, M.P., McEwan, A.G. and Paton, J.C. (2004) Molecular analysis of the psa permease complex of Streptococcus pneumoniae. Molecular Microbiology, 53, 889-901.</Citation></Reference><Reference><Citation>McDevitt, C.A., Ogunniyi, A.D., Valkov, E., Lawrence, M.C., Kobe, B., McEwan, A.G., et al. (2011) A molecular mechanism for bacterial susceptibility to zinc. PLoS Path, 7, e1002357.</Citation></Reference><Reference><Citation>Moore, C.M., Gaballa, A., Hui, M., Ye, R.W. and Helmann, J.D. (2005) Genetic and physiological responses of Bacillus subtilis to metal ion stress. Molecular Microbiology, 57, 27-40.</Citation></Reference><Reference><Citation>Ngamchuea, K., Batchelor-McAuley, C. and Compton, R.G. (2016) The copper(II)-catalyzed oxidation of glutathione. Chemistry, 22, 15937-15944.</Citation></Reference><Reference><Citation>Norambuena, J., Hanson, T.E., Barkay, T. and Boyd, J.M. (2019) Superoxide dismutase and pseudocatalase increase tolerance to Hg(II) in Thermus thermophilus HB27 by maintaining the reduced bacillithiol pool. mBio, 10, e00183-19.</Citation></Reference><Reference><Citation>Norambuena, J., Wang, Y., Hanson, T., Boyd, J.M. and Barkay, T. (2017) Low molecular weight thiols and thioredoxins are important players in Hg(II) resistance in Thermus thermophilus HB27. Applied and Environment Microbiology, 84, e01931-17.</Citation></Reference><Reference><Citation>Novak, R., Braun, J.S., Charpentier, E. and Tuomanen, E. (1998) Penicillin tolerance genes of Streptococcus pneumoniae: the ABC-type manganese permease complex Psa. Molecular Microbiology, 29, 1285-1296.</Citation></Reference><Reference><Citation>Novick, R.P. (1991) Genetic systems in staphylococci. Methods in Enzymology, 204, 587-636.</Citation></Reference><Reference><Citation>Palmer, L.D. and Skaar, E.P. (2016) Transition metals and virulence in bacteria. Annual Review of Genetics, 50, 67-91.</Citation></Reference><Reference><Citation>Pang, Y.Y., Schwartz, J., Bloomberg, S., Boyd, J.M., Horswill, A.R. and Nauseef, W.M. (2013) Methionine sulfoxide reductases protect against oxidative stress in Staphylococcus aureus encountering exogenous oxidants and human neutrophils. Journal of Innate Immunity, 6, 353-364.</Citation></Reference><Reference><Citation>Papp-Wallace, K.M. and Maguire, M.E. (2006) Manganese transport and the role of manganese in virulence. Annual Review of Microbiology, 60, 187-209.</Citation></Reference><Reference><Citation>Perry, R.D. and Silver, S. (1982) Cadmium and manganese transport in Staphylococcus aureus membrane vesicles. Journal of Bacteriology, 150, 973-976.</Citation></Reference><Reference><Citation>Purves, J., Thomas, J., Riboldi, G.P., Zapotoczna, M., Tarrant, E., Andrew, P.W., et al. (2018) A horizontally gene transferred copper resistance locus confers hyper-resistance to antibacterial copper toxicity and enables survival of community acquired methicillin resistant Staphylococcus aureus USA300 in macrophages. Environmental Microbiology, 20, 1576-1589.</Citation></Reference><Reference><Citation>Que, Q. and Helmann, J.D. (2000) Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins. Molecular Microbiology, 35, 1454-1468.</Citation></Reference><Reference><Citation>Quintana, J., Novoa-Aponte, L. and Arguello, J.M. (2017) Copper homeostasis networks in the bacterium Pseudomonas aeruginosa. Journal of Biological Chemistry, 292, 15691-15704.</Citation></Reference><Reference><Citation>Rabinovitch, I., Yanku, M., Yeheskel, A., Cohen, G., Borovok, I. and Aharonowitz, Y. (2010) Staphylococcus aureus NrdH redoxin is a reductant of the class Ib ribonucleotide reductase. Journal of Bacteriology, 192, 4963-4972.</Citation></Reference><Reference><Citation>Rigo, A., Corazza, A., di Paolo, M.L., Rossetto, M., Ugolini, R. and Scarpa, M. (2004) Interaction of copper with cysteine: stability of cuprous complexes and catalytic role of cupric ions in anaerobic thiol oxidation. Journal of inorganic biochemistry, 98, 1495-1501.</Citation></Reference><Reference><Citation>Roberts, C.A., Al-Tameemi, H.M., Mashruwala, A.A., Rosario-Cruz, Z., Chauhan, U., Sause, W.E., et al. (2017) The Suf iron-sulfur cluster biosynthetic system is essential in Staphylococcus aureus and decreased Suf function results in global metabolic defects and reduced survival in human neutrophils. Infection and Immunity, 85(6), e00100-17.</Citation></Reference><Reference><Citation>Rosario-Cruz, Z., Chahal, H.K., Mike, L.A., Skaar, E.P. and Boyd, J.M. (2015) Bacillithiol has a role in Fe-S cluster biogenesis in Staphylococcus aureus. Molecular Microbiology, 98, 218-242.</Citation></Reference><Reference><Citation>Rosario-Cruz, Z., Eletsky, A., Daigham, N.S., Al-Tameemi, H., Swapna, G.V.T., Kahn, P.C., et al. (2019) The copBL operon protects Staphylococcus aureus from copper toxicity: CopL is an extracellular membrane-associated copper-binding protein. Journal of Biological Chemistry, 294, 4027-4044.</Citation></Reference><Reference><Citation>Sabri, M., Leveille, S. and Dozois, C.M. (2006) A SitABCD homologue from an avian pathogenic Escherichia coli strain mediates transport of iron and manganese and resistance to hydrogen peroxide. Microbiology, 152, 745-758.</Citation></Reference><Reference><Citation>Scarpa, M., Momo, F., Viglino, P. and Rigo, A. (1996) Activated oxygen species in the oxidation of glutathione A kinetic study. Biophysical Chemistry, 60, 53-61.</Citation></Reference><Reference><Citation>Shafeeq, S., Yesilkaya, H., Kloosterman, T.G., Narayanan, G., Wandel, M., Andrew, P.W., et al. (2011) The cop operon is required for copper homeostasis and contributes to virulence in Streptococcus pneumoniae. Molecular Microbiology, 81, 1255-1270.</Citation></Reference><Reference><Citation>Singleton, C., Hearnshaw, S., Zhou, L., Le Brun, N.E. and Hemmings, A.M. (2009) Mechanistic insights into Cu(I) cluster transfer between the chaperone CopZ and its cognate Cu(I)-transporting P-type ATPase, CopA. The Biochemical Journal, 424, 347-356.</Citation></Reference><Reference><Citation>Sitthisak, S., Knutsson, L., Webb, J.W. and Jayaswal, R.K. (2007) Molecular characterization of the copper transport system in Staphylococcus aureus. Microbiology, 153, 4274-4283.</Citation></Reference><Reference><Citation>Somerville, G.A., Chaussee, M.S., Morgan, C.I., Fitzgerald, J.R., Dorward, D.W., Reitzer, L.J., et al. (2002) Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival. Infection and Immunity, 70, 6373-6382.</Citation></Reference><Reference><Citation>Tan, G., Cheng, Z., Pang, Y., Landry, A.P., Li, J., Lu, J., et al. (2014) Copper binding in IscA inhibits iron-sulphur cluster assembly in Escherichia coli. Molecular Microbiology, 93, 629-644.</Citation></Reference><Reference><Citation>Tan, G., Yang, J., Li, T., Zhao, J., Sun, S., Li, X., et al. (2017) Anaerobic copper toxicity and iron-sulfur cluster biogenesis in Escherichia coli. Applied and Environment Microbiology, 83.</Citation></Reference><Reference><Citation>Tarrant, E., Riboldi, G.P., McIlvin, M.R., Stevenson, J., Barwinska-Sendra, A., Stewart, L.J., et al. (2019) Copper stress in Staphylococcus aureus leads to adaptive changes in central carbon metabolism. Metallomics, 11, 183-200.</Citation></Reference><Reference><Citation>Tenover, F.C., McDougal, L.K., Goering, R.V., Killgore, G., Projan, S.J., Patel, J.B., et al. (2006) Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States. Journal of Clinical Microbiology, 44, 108-118.</Citation></Reference><Reference><Citation>Tottey, S., Rich, P.R., Rondet, S.A. and Robinson, N.J. (2001) Two Menkes-type atpases supply copper for photosynthesis in Synechocystis PCC 6803. Journal of Biological Chemistry, 276, 19999-20004.</Citation></Reference><Reference><Citation>Turner, N.A., Sharma-Kuinkel, B.K., Maskarinec, S.A., Eichenberger, E.M., Shah, P.P., Carugati, M., et al. (2019) Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nature Reviews Microbiology, 17, 203-218.</Citation></Reference><Reference><Citation>Tynecka, Z., Gos, Z. and Zajac, J. (1981) Reduced cadmium transport determined by a resistance plasmid in Staphylococcus aureus. Journal of Bacteriology, 147, 305-312.</Citation></Reference><Reference><Citation>Wagner, D., Maser, J., Lai, B., Cai, Z., Barry, C.E. 3rd, Bentrup, H.Z., et al. (2005) Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. The Journal of Immunology, 174, 1491-1500.</Citation></Reference><Reference><Citation>Waldron, K.J. and Robinson, N.J. (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nature Reviews Microbiology, 7, 25-35.</Citation></Reference><Reference><Citation>White, C., Lee, J., Kambe, T., Fritsche, K. and Petris, M.J. (2009) A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. Journal of Biological Chemistry, 284, 33949-33956.</Citation></Reference><Reference><Citation>Wilkens, S. (2015) Structure and mechanism of ABC transporters. F1000Prime Rep, 7, 14.</Citation></Reference><Reference><Citation>Winston, F., Dollard, C. and Ricupero-Hovasse, S.L. (1995) Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast, 11(1), 53-5. https://pubmed.ncbi.nlm.nih.gov/7762301/.</Citation></Reference><Reference><Citation>Xu, F.F. and Imlay, J.A. (2012) Silver(I), mercury(II), cadmium(II), and zinc(II) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli. Applied and Environment Microbiology, 78, 3614-3621.</Citation></Reference><Reference><Citation>Zapotoczna, M., Riboldi, G.P., Moustafa, A.M., Dickson, E., Narechania, A., Morrissey, J.A., et al. (2018) Mobile-genetic-element-encoded hypertolerance to copper protects Staphylococcus aureus from killing by host phagocytes. mBio, 9, e00550-18.</Citation></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>États-Unis</li></country><region><li>New Jersey</li><li>Tennessee</li></region></list><tree><country name="États-Unis"><region name="New Jersey"><name sortKey="Al Tameemi, Hassan" sort="Al Tameemi, Hassan" uniqKey="Al Tameemi H" first="Hassan" last="Al-Tameemi">Hassan Al-Tameemi</name></region><name sortKey="Beavers, William N" sort="Beavers, William N" uniqKey="Beavers W" first="William N" last="Beavers">William N. Beavers</name><name sortKey="Boyd, Jeffrey M" sort="Boyd, Jeffrey M" uniqKey="Boyd J" first="Jeffrey M" last="Boyd">Jeffrey M. Boyd</name><name sortKey="Norambuena, Javiera" sort="Norambuena, Javiera" uniqKey="Norambuena J" first="Javiera" last="Norambuena">Javiera Norambuena</name><name sortKey="Skaar, Eric P" sort="Skaar, Eric P" uniqKey="Skaar E" first="Eric P" last="Skaar">Eric P. Skaar</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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