Crystal Structure and Functional Analysis of the SARS-Coronavirus RNA Cap 2′-O-Methyltransferase nsp10/nsp16 Complex
Identifieur interne : 001402 ( Pmc/Curation ); précédent : 001401; suivant : 001403Crystal Structure and Functional Analysis of the SARS-Coronavirus RNA Cap 2′-O-Methyltransferase nsp10/nsp16 Complex
Auteurs : Etienne Decroly [France] ; Claire Debarnot [France] ; François Ferron [France] ; Mickael Bouvet [France] ; Bruno Coutard [France] ; Isabelle Imbert [France] ; Laure Gluais [France] ; Nicolas Papageorgiou [France] ; Andrew Sharff [Royaume-Uni] ; Gérard Bricogne [Royaume-Uni] ; Miguel Ortiz-Lombardia [France] ; Julien Lescar [France] ; Bruno Canard [France]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2011.
Abstract
Cellular and viral S-adenosylmethionine-dependent methyltransferases are involved in many regulated processes such as metabolism, detoxification, signal transduction, chromatin remodeling, nucleic acid processing, and mRNA capping. The Severe Acute Respiratory Syndrome coronavirus nsp16 protein is a S-adenosylmethionine-dependent (nucleoside-2′-O)-methyltransferase only active in the presence of its activating partner nsp10. We report the nsp10/nsp16 complex structure at 2.0 Å resolution, which shows nsp10 bound to nsp16 through a ∼930 Å2 surface area in nsp10. Functional assays identify key residues involved in nsp10/nsp16 association, and in RNA binding or catalysis, the latter likely through a SN2-like mechanism. We present two other crystal structures, the inhibitor Sinefungin bound in the S-adenosylmethionine binding pocket and the tighter complex nsp10(Y96F)/nsp16, providing the first structural insight into the regulation of RNA capping enzymes in (+)RNA viruses.
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DOI: 10.1371/journal.ppat.1002059
PubMed: 21637813
PubMed Central: 3102710
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Julien Lescar<affiliation><nlm:aff id="aff3"><addr-line>School of Biological Sciences, Nanyang Technological University, Singapore, Republic of Singapore</addr-line></nlm:aff><wicri:noCountry code="subfield">Republic of Singapore</wicri:noCountry></affiliation>Le document en format XML
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wicri:step="Curation">001402</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Crystal Structure and Functional Analysis of the SARS-Coronavirus RNA Cap 2′-O-Methyltransferase nsp10/nsp16 Complex</title><author><name sortKey="Decroly, Etienne" sort="Decroly, Etienne" uniqKey="Decroly E" first="Etienne" last="Decroly">Etienne Decroly</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author><author><name sortKey="Debarnot, Claire" sort="Debarnot, Claire" uniqKey="Debarnot C" first="Claire" last="Debarnot">Claire Debarnot</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author><author><name sortKey="Ferron, Francois" sort="Ferron, Francois" uniqKey="Ferron F" first="François" last="Ferron">François Ferron</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author><author><name sortKey="Bouvet, Mickael" sort="Bouvet, Mickael" uniqKey="Bouvet M" first="Mickael" last="Bouvet">Mickael Bouvet</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author><author><name sortKey="Coutard, Bruno" sort="Coutard, Bruno" uniqKey="Coutard B" first="Bruno" last="Coutard">Bruno Coutard</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author><author><name sortKey="Imbert, Isabelle" sort="Imbert, Isabelle" uniqKey="Imbert I" first="Isabelle" last="Imbert">Isabelle Imbert</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author><author><name sortKey="Gluais, Laure" sort="Gluais, Laure" uniqKey="Gluais L" first="Laure" last="Gluais">Laure Gluais</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author><author><name sortKey="Papageorgiou, Nicolas" sort="Papageorgiou, Nicolas" uniqKey="Papageorgiou N" first="Nicolas" last="Papageorgiou">Nicolas Papageorgiou</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author><author><name sortKey="Sharff, Andrew" sort="Sharff, Andrew" uniqKey="Sharff A" first="Andrew" last="Sharff">Andrew Sharff</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Global Phasing Ltd., Sheraton House, Castle Park, Cambridge, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Global Phasing Ltd., Sheraton House, Castle Park, Cambridge</wicri:regionArea></affiliation></author><author><name sortKey="Bricogne, Gerard" sort="Bricogne, Gerard" uniqKey="Bricogne G" first="Gérard" last="Bricogne">Gérard Bricogne</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Global Phasing Ltd., Sheraton House, Castle Park, Cambridge, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Global Phasing Ltd., Sheraton House, Castle Park, Cambridge</wicri:regionArea></affiliation></author><author><name sortKey="Ortiz Lombardia, Miguel" sort="Ortiz Lombardia, Miguel" uniqKey="Ortiz Lombardia M" first="Miguel" last="Ortiz-Lombardia">Miguel Ortiz-Lombardia</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author><author><name sortKey="Lescar, Julien" sort="Lescar, Julien" uniqKey="Lescar J" first="Julien" last="Lescar">Julien Lescar</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation><affiliation><nlm:aff id="aff3"><addr-line>School of Biological Sciences, Nanyang Technological University, Singapore, Republic of Singapore</addr-line></nlm:aff><wicri:noCountry code="subfield">Republic of Singapore</wicri:noCountry></affiliation></author><author><name sortKey="Canard, Bruno" sort="Canard, Bruno" uniqKey="Canard B" first="Bruno" last="Canard">Bruno Canard</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS Pathogens</title><idno type="ISSN">1553-7366</idno><idno type="eISSN">1553-7374</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Cellular and viral S-adenosylmethionine-dependent methyltransferases are involved in many regulated processes such as metabolism, detoxification, signal transduction, chromatin remodeling, nucleic acid processing, and mRNA capping. The Severe Acute Respiratory Syndrome coronavirus nsp16 protein is a S-adenosylmethionine-dependent (nucleoside-2′-O)-methyltransferase only active in the presence of its activating partner nsp10. We report the nsp10/nsp16 complex structure at 2.0 Å resolution, which shows nsp10 bound to nsp16 through a ∼930 Å<sup>2</sup> surface area in nsp10. Functional assays identify key residues involved in nsp10/nsp16 association, and in RNA binding or catalysis, the latter likely through a SN2-like mechanism. We present two other crystal structures, the inhibitor Sinefungin bound in the S-adenosylmethionine binding pocket and the tighter complex nsp10(Y96F)/nsp16, providing the first structural insight into the regulation of RNA capping enzymes in (+)RNA viruses.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Gu, M" uniqKey="Gu M">M Gu</name></author><author><name sortKey="Lima, Cd" uniqKey="Lima C">CD Lima</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shuman, S" uniqKey="Shuman S">S Shuman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shuman, S" uniqKey="Shuman S">S Shuman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yoneyama, M" uniqKey="Yoneyama M">M Yoneyama</name></author><author><name sortKey="Fujita, T" uniqKey="Fujita T">T Fujita</name></author></analytic></biblStruct><biblStruct><analytic><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id><journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plospath</journal-id><journal-title-group><journal-title>PLoS Pathogens</journal-title></journal-title-group><issn pub-type="ppub">1553-7366</issn><issn pub-type="epub">1553-7374</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">21637813</article-id><article-id pub-id-type="pmc">3102710</article-id><article-id pub-id-type="publisher-id">PPATHOGENS-D-10-00474</article-id><article-id pub-id-type="doi">10.1371/journal.ppat.1002059</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Protein Structure</subject></subj-group></subj-group><subj-group><subject>Biomacromolecule-Ligand Interactions</subject><subject>Enzymes</subject></subj-group></subj-group><subj-group><subject>Microbiology</subject><subj-group><subject>Virology</subject><subj-group><subject>Antivirals</subject><subject>Emerging Viral Diseases</subject><subject>Viral Enzymes</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Crystal Structure and Functional Analysis of the SARS-Coronavirus RNA Cap 2′-O-Methyltransferase nsp10/nsp16 Complex</article-title><alt-title alt-title-type="running-head">SARS-CoV nsp10/16 MTase Complex Structure</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Decroly</surname><given-names>Etienne</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Debarnot</surname><given-names>Claire</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ferron</surname><given-names>François</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bouvet</surname><given-names>Mickael</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Coutard</surname><given-names>Bruno</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Imbert</surname><given-names>Isabelle</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gluais</surname><given-names>Laure</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Papageorgiou</surname><given-names>Nicolas</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sharff</surname><given-names>Andrew</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bricogne</surname><given-names>Gérard</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ortiz-Lombardia</surname><given-names>Miguel</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lescar</surname><given-names>Julien</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Canard</surname><given-names>Bruno</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Centre National de la Recherche Scientifique and Université de la Méditerranée, UMR 6098, Architecture et Fonction des Macromolécules Biologiques, Marseille, France</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Global Phasing Ltd., Sheraton House, Castle Park, Cambridge, United Kingdom</addr-line></aff><aff id="aff3"><label>3</label><addr-line>School of Biological Sciences, Nanyang Technological University, Singapore, Republic of Singapore</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Rey</surname><given-names>Félix A.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1">Institut Pasteur, France</aff><author-notes><corresp id="cor1">* E-mail: <email>etienne.decroly@afmb.univ-mrs.fr</email> (ED); <email>bruno.canard@afmb.univ-mrs.fr</email> (BC)</corresp><fn fn-type="con"><p>Conceived and designed the experiments: E. Decroly, B. Canard. Performed the experiments: E. Decroly, C. Debarnot, F. Ferron, M. Bouvet, B. Coutard, I. Imbert, L. Gluais, N. Papageorgiou, B. Canard. Analyzed the data: E. Decroly, F. Ferron, I. Imbert, N. Papageorgiou, A. Sharff, G. Bricogne, M. Ortiz-Lombardia, J. Lescar, B. Canard. Wrote the paper: E. Decroly, B. Canard.</p></fn></author-notes><pub-date pub-type="collection"><month>5</month><year>2011</year></pub-date><pub-date pub-type="epub"><day>26</day><month>5</month><year>2011</year></pub-date><volume>7</volume><issue>5</issue><elocation-id>e1002059</elocation-id><history><date date-type="received"><day>7</day><month>12</month><year>2010</year></date><date date-type="accepted"><day>23</day><month>3</month><year>2011</year></date></history><permissions><copyright-statement>Decroly et al.</copyright-statement><copyright-year>2011</copyright-year><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p></license></permissions><abstract><p>Cellular and viral S-adenosylmethionine-dependent methyltransferases are involved in many regulated processes such as metabolism, detoxification, signal transduction, chromatin remodeling, nucleic acid processing, and mRNA capping. The Severe Acute Respiratory Syndrome coronavirus nsp16 protein is a S-adenosylmethionine-dependent (nucleoside-2′-O)-methyltransferase only active in the presence of its activating partner nsp10. We report the nsp10/nsp16 complex structure at 2.0 Å resolution, which shows nsp10 bound to nsp16 through a ∼930 Å<sup>2</sup> surface area in nsp10. Functional assays identify key residues involved in nsp10/nsp16 association, and in RNA binding or catalysis, the latter likely through a SN2-like mechanism. We present two other crystal structures, the inhibitor Sinefungin bound in the S-adenosylmethionine binding pocket and the tighter complex nsp10(Y96F)/nsp16, providing the first structural insight into the regulation of RNA capping enzymes in (+)RNA viruses.</p></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>A novel coronavirus emerged in 2003 and was identified as the etiological agent of the deadly disease called Severe Acute Respiratory Syndrome. This coronavirus replicates and transcribes its giant genome using sixteen non-structural proteins (nsp1-16). Viral RNAs are capped to ensure stability, efficient translation, and evading the innate immunity system of the host cell. The nsp16 protein is a RNA cap modifying enzyme only active in the presence of its activating partner nsp10. We have crystallized the nsp10/16 complex and report its crystal structure at atomic resolution. Nsp10 binds to nsp16 through a ∼930 Å<sup>2</sup> activation surface area in nsp10, and the resulting complex exhibits RNA cap (nucleoside-2′-O)-methyltransferase activity. We have performed mutational and functional assays to identify key residues involved in catalysis and/or in RNA binding, and in the association of nsp10 to nsp16. We present two additional crystal structures, that of the known inhibitor Sinefungin bound in the SAM binding pocket, and that of a tighter complex made of the mutant nsp10(Y96F) bound to nsp16. Our study provides a basis for antiviral drug design as well as the first structural insight into the regulation of RNA capping enzymes in (+)RNA viruses.</p></abstract><counts><page-count count="14"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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