Coupling of Peptidoglycan Synthesis to Central Metabolism in Mycobacteria: Post-transcriptional Control of CwlM by Aconitase.
Identifieur interne : 000152 ( Main/Exploration ); précédent : 000151; suivant : 000153Coupling of Peptidoglycan Synthesis to Central Metabolism in Mycobacteria: Post-transcriptional Control of CwlM by Aconitase.
Auteurs : Peter J. Bancroft [Royaume-Uni] ; Obolbek Turapov [Royaume-Uni] ; Heena Jagatia [Royaume-Uni] ; Kristine B. Arnvig [Royaume-Uni] ; Galina V. Mukamolova [Royaume-Uni] ; Jeffrey Green [Royaume-Uni]Source :
- Cell reports [ 2211-1247 ] ; 2020.
Abstract
Mycobacterium tuberculosis causes human tuberculosis, and a better understanding of its biology is required to identify vulnerabilities that might be exploited in developing new therapeutics. The iron-sulfur cluster of the essential M. tuberculosis central metabolic enzyme, aconitase (AcnA), disassembles when exposed to oxidative/nitrosative stress or iron chelators. The catalytically inactive apo-AcnA interacts with a sequence resembling an iron-responsive element (IRE) located within the transcript of another essential protein, CwlM, a regulator of peptidoglycan synthesis. A Mycobacterium smegmatis cwlM conditional mutant complemented with M. tuberculosis cwlM with a disrupted IRE is unable to recover from combinations of oxidative, nitrosative, and iron starvation stresses. An equivalent M. tuberculosis cwlM conditional mutant complemented with the cwlM gene lacking a functional IRE exhibits a growth defect in THP-1 macrophages. It appears that AcnA acts to couple peptidoglycan synthesis and central metabolism, and disruption of this coupling potentially leaves mycobacteria vulnerable to attack by macrophages.
DOI: 10.1016/j.celrep.2020.108209
PubMed: 32997986
PubMed Central: PMC7527780
Affiliations:
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Bancroft</name><affiliation wicri:level="1"><nlm:affiliation>Molecular Biology and Biotechnology, University of Sheffield, Sheffield, S10 2TN, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Molecular Biology and Biotechnology, University of Sheffield, Sheffield, S10 2TN</wicri:regionArea><wicri:noRegion>S10 2TN</wicri:noRegion></affiliation></author><author><name sortKey="Turapov, Obolbek" sort="Turapov, Obolbek" uniqKey="Turapov O" first="Obolbek" last="Turapov">Obolbek Turapov</name><affiliation wicri:level="1"><nlm:affiliation>Leicester Tuberculosis Research Group, Department of Respiratory Sciences, University of Leicester, Maurice Shock Medical Sciences Building, University Road, Leicester, LE1 9HN, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Leicester Tuberculosis Research Group, Department of Respiratory Sciences, University of Leicester, Maurice Shock Medical Sciences Building, University Road, Leicester, LE1 9HN</wicri:regionArea><wicri:noRegion>LE1 9HN</wicri:noRegion></affiliation></author><author><name sortKey="Jagatia, Heena" sort="Jagatia, Heena" uniqKey="Jagatia H" first="Heena" last="Jagatia">Heena Jagatia</name><affiliation wicri:level="1"><nlm:affiliation>Leicester Tuberculosis Research Group, Department of Respiratory Sciences, University of Leicester, Maurice Shock Medical Sciences Building, University Road, Leicester, LE1 9HN, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Leicester Tuberculosis Research Group, Department of Respiratory Sciences, University of Leicester, Maurice Shock Medical Sciences Building, University Road, Leicester, LE1 9HN</wicri:regionArea><wicri:noRegion>LE1 9HN</wicri:noRegion></affiliation></author><author><name sortKey="Arnvig, Kristine B" sort="Arnvig, Kristine B" uniqKey="Arnvig K" first="Kristine B" last="Arnvig">Kristine B. Arnvig</name><affiliation wicri:level="4"><nlm:affiliation>Institute for Structural and Molecular Biology, University College London, London, WC1E 6BT, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Institute for Structural and Molecular Biology, University College London, London, WC1E 6BT</wicri:regionArea><orgName type="university">University College de Londres</orgName><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Mukamolova, Galina V" sort="Mukamolova, Galina V" uniqKey="Mukamolova G" first="Galina V" last="Mukamolova">Galina V. Mukamolova</name><affiliation wicri:level="1"><nlm:affiliation>Leicester Tuberculosis Research Group, Department of Respiratory Sciences, University of Leicester, Maurice Shock Medical Sciences Building, University Road, Leicester, LE1 9HN, UK. Electronic address: gvm4@leicester.ac.uk.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Leicester Tuberculosis Research Group, Department of Respiratory Sciences, University of Leicester, Maurice Shock Medical Sciences Building, University Road, Leicester, LE1 9HN</wicri:regionArea><wicri:noRegion>LE1 9HN</wicri:noRegion></affiliation></author><author><name sortKey="Green, Jeffrey" sort="Green, Jeffrey" uniqKey="Green J" first="Jeffrey" last="Green">Jeffrey Green</name><affiliation wicri:level="1"><nlm:affiliation>Molecular Biology and Biotechnology, University of Sheffield, Sheffield, S10 2TN, UK. Electronic address: jeff.green@sheffield.ac.uk.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Molecular Biology and Biotechnology, University of Sheffield, Sheffield, S10 2TN</wicri:regionArea><wicri:noRegion>S10 2TN</wicri:noRegion></affiliation></author></analytic><series><title level="j">Cell reports</title><idno type="eISSN">2211-1247</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">Mycobacterium tuberculosis causes human tuberculosis, and a better understanding of its biology is required to identify vulnerabilities that might be exploited in developing new therapeutics. The iron-sulfur cluster of the essential M. tuberculosis central metabolic enzyme, aconitase (AcnA), disassembles when exposed to oxidative/nitrosative stress or iron chelators. The catalytically inactive apo-AcnA interacts with a sequence resembling an iron-responsive element (IRE) located within the transcript of another essential protein, CwlM, a regulator of peptidoglycan synthesis. A Mycobacterium smegmatis cwlM conditional mutant complemented with M. tuberculosis cwlM with a disrupted IRE is unable to recover from combinations of oxidative, nitrosative, and iron starvation stresses. An equivalent M. tuberculosis cwlM conditional mutant complemented with the cwlM gene lacking a functional IRE exhibits a growth defect in THP-1 macrophages. It appears that AcnA acts to couple peptidoglycan synthesis and central metabolism, and disruption of this coupling potentially leaves mycobacteria vulnerable to attack by macrophages.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">32997986</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>22</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">2211-1247</ISSN><JournalIssue CitedMedium="Internet"><Volume>32</Volume><Issue>13</Issue><PubDate><Year>2020</Year><Month>Sep</Month><Day>29</Day></PubDate></JournalIssue><Title>Cell reports</Title><ISOAbbreviation>Cell Rep</ISOAbbreviation></Journal><ArticleTitle>Coupling of Peptidoglycan Synthesis to Central Metabolism in Mycobacteria: Post-transcriptional Control of CwlM by Aconitase.</ArticleTitle><Pagination><MedlinePgn>108209</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S2211-1247(20)31198-0</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.celrep.2020.108209</ELocationID><Abstract><AbstractText>Mycobacterium tuberculosis causes human tuberculosis, and a better understanding of its biology is required to identify vulnerabilities that might be exploited in developing new therapeutics. The iron-sulfur cluster of the essential M. tuberculosis central metabolic enzyme, aconitase (AcnA), disassembles when exposed to oxidative/nitrosative stress or iron chelators. The catalytically inactive apo-AcnA interacts with a sequence resembling an iron-responsive element (IRE) located within the transcript of another essential protein, CwlM, a regulator of peptidoglycan synthesis. A Mycobacterium smegmatis cwlM conditional mutant complemented with M. tuberculosis cwlM with a disrupted IRE is unable to recover from combinations of oxidative, nitrosative, and iron starvation stresses. An equivalent M. tuberculosis cwlM conditional mutant complemented with the cwlM gene lacking a functional IRE exhibits a growth defect in THP-1 macrophages. It appears that AcnA acts to couple peptidoglycan synthesis and central metabolism, and disruption of this coupling potentially leaves mycobacteria vulnerable to attack by macrophages.</AbstractText><CopyrightInformation>Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Bancroft</LastName><ForeName>Peter J</ForeName><Initials>PJ</Initials><AffiliationInfo><Affiliation>Molecular Biology and Biotechnology, University of Sheffield, Sheffield, S10 2TN, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Turapov</LastName><ForeName>Obolbek</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>Leicester Tuberculosis Research Group, Department of Respiratory Sciences, University of Leicester, Maurice Shock Medical Sciences Building, University Road, Leicester, LE1 9HN, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jagatia</LastName><ForeName>Heena</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Leicester Tuberculosis Research Group, Department of Respiratory Sciences, University of Leicester, Maurice Shock Medical Sciences Building, University Road, Leicester, LE1 9HN, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Arnvig</LastName><ForeName>Kristine B</ForeName><Initials>KB</Initials><AffiliationInfo><Affiliation>Institute for Structural and Molecular Biology, University College London, London, WC1E 6BT, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mukamolova</LastName><ForeName>Galina V</ForeName><Initials>GV</Initials><AffiliationInfo><Affiliation>Leicester Tuberculosis Research Group, Department of Respiratory Sciences, University of Leicester, Maurice Shock Medical Sciences Building, University Road, Leicester, LE1 9HN, UK. Electronic address: gvm4@leicester.ac.uk.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Green</LastName><ForeName>Jeffrey</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Molecular Biology and Biotechnology, University of Sheffield, Sheffield, S10 2TN, UK. Electronic address: jeff.green@sheffield.ac.uk.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>BB/P001513/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Cell Rep</MedlineTA><NlmUniqueID>101573691</NlmUniqueID></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">CwlM</Keyword><Keyword MajorTopicYN="N">Mycobacterium tuberculosis</Keyword><Keyword MajorTopicYN="N">aconitase</Keyword><Keyword MajorTopicYN="N">iron-responsive element</Keyword><Keyword MajorTopicYN="N">macrophage infection</Keyword><Keyword MajorTopicYN="N">nitrosative stress</Keyword><Keyword MajorTopicYN="N">oxidative stress</Keyword><Keyword MajorTopicYN="N">peptidoglycan</Keyword><Keyword MajorTopicYN="N">post-transcriptional regulation</Keyword><Keyword MajorTopicYN="N">protein kinase B (PknB)</Keyword></KeywordList><CoiStatement>Declaration of Interests The authors declare no competing interests.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>02</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>06</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>09</Month><Day>09</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>9</Month><Day>30</Day><Hour>20</Hour><Minute>5</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>10</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>10</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32997986</ArticleId><ArticleId IdType="pii">S2211-1247(20)31198-0</ArticleId><ArticleId IdType="doi">10.1016/j.celrep.2020.108209</ArticleId><ArticleId IdType="pmc">PMC7527780</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>Microbiology (Reading). 1996 Apr;142 ( Pt 4):915-25</Citation><ArticleIdList><ArticleId IdType="pubmed">8936318</ArticleId></ArticleIdList></Reference><Reference><Citation>Microbiology (Reading). 1999 Nov;145 ( Pt 11):3069-3079</Citation><ArticleIdList><ArticleId IdType="pubmed">10589714</ArticleId></ArticleIdList></Reference><Reference><Citation>Cell Rep. 2013 Nov 27;5(4):1121-31</Citation><ArticleIdList><ArticleId IdType="pubmed">24268774</ArticleId></ArticleIdList></Reference><Reference><Citation>J Biol Inorg Chem. 2003 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name="Royaume-Uni"><noRegion><name sortKey="Bancroft, Peter J" sort="Bancroft, Peter J" uniqKey="Bancroft P" first="Peter J" last="Bancroft">Peter J. Bancroft</name></noRegion><name sortKey="Arnvig, Kristine B" sort="Arnvig, Kristine B" uniqKey="Arnvig K" first="Kristine B" last="Arnvig">Kristine B. Arnvig</name><name sortKey="Green, Jeffrey" sort="Green, Jeffrey" uniqKey="Green J" first="Jeffrey" last="Green">Jeffrey Green</name><name sortKey="Jagatia, Heena" sort="Jagatia, Heena" uniqKey="Jagatia H" first="Heena" last="Jagatia">Heena Jagatia</name><name sortKey="Mukamolova, Galina V" sort="Mukamolova, Galina V" uniqKey="Mukamolova G" first="Galina V" last="Mukamolova">Galina V. Mukamolova</name><name sortKey="Turapov, Obolbek" sort="Turapov, Obolbek" uniqKey="Turapov O" first="Obolbek" last="Turapov">Obolbek Turapov</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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