Adaptive Evolution of MERS-CoV to Species Variation in DPP4
Identifieur interne : 000665 ( Pmc/Curation ); précédent : 000664; suivant : 000666Adaptive Evolution of MERS-CoV to Species Variation in DPP4
Auteurs : Michael Letko [États-Unis] ; Kerri Miazgowicz [États-Unis] ; Rebekah Mcminn [États-Unis] ; Stephanie N. Seifert [États-Unis] ; Isabel Sola [Espagne] ; Luis Enjuanes [Espagne] ; Aaron Carmody [États-Unis] ; Neeltje Van Doremalen [États-Unis] ; Vincent Munster [États-Unis]Source :
- Cell Reports [ 2211-1247 ] ; 2018.
Abstract
Middle East Respiratory Syndrome Coronavirus (MERS-CoV) likely originated in bats and passed to humans through dromedary camels; however, the genetic mechanisms underlying cross-species adaptation remain poorly understood. Variation in the host receptor, dipeptidyl peptidase 4 (DPP4), can block the interaction with the MERS-CoV spike protein and form a species barrier to infection. To better understand the species adaptability of MERS-CoV, we identified a suboptimal species-derived variant of DPP4 to study viral adaption. Passaging virus on cells expressing this DPP4 variant led to accumulation of mutations in the viral spike which increased replication. Parallel passages revealed distinct paths of viral adaptation to the same DPP4 variant. Structural analysis and functional assays showed that these mutations enhanced viral entry with suboptimal DPP4 by altering the surface charge of spike. These findings demonstrate that MERS-CoV spike can utilize multiple paths to rapidly adapt to novel species variation in DPP4.
Url:
DOI: 10.1016/j.celrep.2018.07.045
PubMed: 30110630
PubMed Central: 7104223
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Autónoma de Madrid, Cantoblanco, Madrid</wicri:regionArea></affiliation></author><author><name sortKey="Enjuanes, Luis" sort="Enjuanes, Luis" uniqKey="Enjuanes L" first="Luis" last="Enjuanes">Luis Enjuanes</name><affiliation wicri:level="1"><nlm:aff id="aff5">Department of Molecular and Cell Biology, Centro Nacional de Biotecnología (CNB-CSIC), Campus Universidad Autónoma de Madrid, Cantoblanco, Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Department of Molecular and Cell Biology, Centro Nacional de Biotecnología (CNB-CSIC), Campus Universidad Autónoma de Madrid, Cantoblanco, Madrid</wicri:regionArea></affiliation></author><author><name sortKey="Carmody, Aaron" sort="Carmody, Aaron" uniqKey="Carmody A" first="Aaron" last="Carmody">Aaron Carmody</name><affiliation wicri:level="1"><nlm:aff id="aff2">Research Technologies Branch, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, 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Kerri" sort="Miazgowicz, Kerri" uniqKey="Miazgowicz K" first="Kerri" last="Miazgowicz">Kerri Miazgowicz</name><affiliation wicri:level="1"><nlm:aff id="aff1">Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Infectious Diseases, College of Veterinary Medicine, The University of Georgia, Athens, GA 30602, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Infectious Diseases, College of Veterinary Medicine, The University of Georgia, Athens, GA 30602</wicri:regionArea></affiliation></author><author><name 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Stephanie N" sort="Seifert, Stephanie N" uniqKey="Seifert S" first="Stephanie N." last="Seifert">Stephanie N. Seifert</name><affiliation wicri:level="1"><nlm:aff id="aff1">Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840</wicri:regionArea></affiliation></author><author><name sortKey="Sola, Isabel" sort="Sola, Isabel" uniqKey="Sola I" first="Isabel" last="Sola">Isabel Sola</name><affiliation wicri:level="1"><nlm:aff id="aff5">Department of Molecular and Cell Biology, Centro Nacional de Biotecnología (CNB-CSIC), Campus Universidad Autónoma de Madrid, Cantoblanco, Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Department of Molecular and Cell Biology, Centro Nacional de Biotecnología (CNB-CSIC), Campus Universidad Autónoma de Madrid, Cantoblanco, Madrid</wicri:regionArea></affiliation></author><author><name sortKey="Enjuanes, Luis" sort="Enjuanes, Luis" uniqKey="Enjuanes L" first="Luis" last="Enjuanes">Luis Enjuanes</name><affiliation wicri:level="1"><nlm:aff id="aff5">Department of Molecular and Cell Biology, Centro Nacional de Biotecnología (CNB-CSIC), Campus Universidad Autónoma de Madrid, Cantoblanco, Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Department of Molecular and Cell Biology, Centro Nacional de Biotecnología (CNB-CSIC), Campus Universidad Autónoma de Madrid, Cantoblanco, Madrid</wicri:regionArea></affiliation></author><author><name sortKey="Carmody, Aaron" sort="Carmody, Aaron" uniqKey="Carmody A" first="Aaron" last="Carmody">Aaron Carmody</name><affiliation wicri:level="1"><nlm:aff id="aff2">Research Technologies Branch, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Research Technologies Branch, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840</wicri:regionArea></affiliation></author><author><name sortKey="Van Doremalen, Neeltje" sort="Van Doremalen, Neeltje" uniqKey="Van Doremalen N" first="Neeltje" last="Van Doremalen">Neeltje Van Doremalen</name><affiliation wicri:level="1"><nlm:aff id="aff1">Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840</wicri:regionArea></affiliation></author><author><name sortKey="Munster, Vincent" sort="Munster, Vincent" uniqKey="Munster V" first="Vincent" last="Munster">Vincent Munster</name><affiliation wicri:level="1"><nlm:aff id="aff1">Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840</wicri:regionArea></affiliation></author></analytic><series><title level="j">Cell Reports</title><idno type="eISSN">2211-1247</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Summary</title><p>Middle East Respiratory Syndrome Coronavirus (MERS-CoV) likely originated in bats and passed to humans through dromedary camels; however, the genetic mechanisms underlying cross-species adaptation remain poorly understood. Variation in the host receptor, dipeptidyl peptidase 4 (DPP4), can block the interaction with the MERS-CoV spike protein and form a species barrier to infection. To better understand the species adaptability of MERS-CoV, we identified a suboptimal species-derived variant of DPP4 to study viral adaption. Passaging virus on cells expressing this DPP4 variant led to accumulation of mutations in the viral spike which increased replication. Parallel passages revealed distinct paths of viral adaptation to the same DPP4 variant. Structural analysis and functional assays showed that these mutations enhanced viral entry with suboptimal DPP4 by altering the surface charge of spike. These findings demonstrate that MERS-CoV spike can utilize multiple paths to rapidly adapt to novel species variation in DPP4.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Adney, D R" uniqKey="Adney D">D.R. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Cell Rep</journal-id><journal-id journal-id-type="iso-abbrev">Cell Rep</journal-id><journal-title-group><journal-title>Cell Reports</journal-title></journal-title-group><issn pub-type="epub">2211-1247</issn><publisher><publisher-name>Cell Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30110630</article-id><article-id pub-id-type="pmc">7104223</article-id><article-id pub-id-type="publisher-id">S2211-1247(18)31148-3</article-id><article-id pub-id-type="doi">10.1016/j.celrep.2018.07.045</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Adaptive Evolution of MERS-CoV to Species Variation in DPP4</article-title></title-group><contrib-group><contrib contrib-type="author" id="au1"><name><surname>Letko</surname><given-names>Michael</given-names></name><email>michael.letko@nih.gov</email><xref rid="aff1" ref-type="aff">1</xref><xref rid="fn1" ref-type="fn">6</xref><xref rid="cor1" ref-type="corresp">∗</xref></contrib><contrib contrib-type="author" id="au2"><name><surname>Miazgowicz</surname><given-names>Kerri</given-names></name><xref rid="aff1" ref-type="aff">1</xref><xref rid="aff3" ref-type="aff">3</xref><xref rid="fn1" ref-type="fn">6</xref></contrib><contrib contrib-type="author" id="au3"><name><surname>McMinn</surname><given-names>Rebekah</given-names></name><xref rid="aff1" ref-type="aff">1</xref><xref rid="aff4" ref-type="aff">4</xref></contrib><contrib contrib-type="author" id="au4"><name><surname>Seifert</surname><given-names>Stephanie N.</given-names></name><xref rid="aff1" ref-type="aff">1</xref></contrib><contrib contrib-type="author" id="au5"><name><surname>Sola</surname><given-names>Isabel</given-names></name><xref rid="aff5" ref-type="aff">5</xref></contrib><contrib contrib-type="author" id="au6"><name><surname>Enjuanes</surname><given-names>Luis</given-names></name><xref rid="aff5" ref-type="aff">5</xref></contrib><contrib contrib-type="author" id="au7"><name><surname>Carmody</surname><given-names>Aaron</given-names></name><xref rid="aff2" ref-type="aff">2</xref></contrib><contrib contrib-type="author" id="au8"><name><surname>van Doremalen</surname><given-names>Neeltje</given-names></name><xref rid="aff1" ref-type="aff">1</xref></contrib><contrib contrib-type="author" id="au9"><name><surname>Munster</surname><given-names>Vincent</given-names></name><email>vincent.munster@nih.gov</email><xref rid="aff1" ref-type="aff">1</xref><xref rid="fn2" ref-type="fn">7</xref><xref rid="cor2" ref-type="corresp">∗∗</xref></contrib></contrib-group><aff id="aff1"><label>1</label>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840, USA</aff><aff id="aff2"><label>2</label>Research Technologies Branch, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840, USA</aff><aff id="aff3"><label>3</label>Department of Infectious Diseases, College of Veterinary Medicine, The University of Georgia, Athens, GA 30602, USA</aff><aff id="aff4"><label>4</label>Department of Microbiology, Immunology, & Pathology, Colorado State University, Fort Collins, CO 80523, USA</aff><aff id="aff5"><label>5</label>Department of Molecular and Cell Biology, Centro Nacional de Biotecnología (CNB-CSIC), Campus Universidad Autónoma de Madrid, Cantoblanco, Madrid, Spain</aff><author-notes><corresp id="cor1"><label>∗</label>Corresponding author <email>michael.letko@nih.gov</email></corresp><corresp id="cor2"><label>∗∗</label>Corresponding author <email>vincent.munster@nih.gov</email></corresp><fn id="fn1"><label>6</label><p id="ntpara0010">These authors contributed equally</p></fn><fn id="fn2"><label>7</label><p id="ntpara0015">Lead Contact</p></fn></author-notes><pub-date pub-type="pmc-release"><day>14</day><month>8</month><year>2018</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><day>14</day><month>8</month><year>2018</year></pub-date><pub-date pub-type="epub"><day>14</day><month>8</month><year>2018</year></pub-date><volume>24</volume><issue>7</issue><fpage>1730</fpage><lpage>1737</lpage><history><date date-type="received"><day>3</day><month>4</month><year>2018</year></date><date date-type="rev-recd"><day>13</day><month>6</month><year>2018</year></date><date date-type="accepted"><day>12</day><month>7</month><year>2018</year></date></history><permissions><license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p></license></permissions><abstract id="abs0010"><title>Summary</title><p>Middle East Respiratory Syndrome Coronavirus (MERS-CoV) likely originated in bats and passed to humans through dromedary camels; however, the genetic mechanisms underlying cross-species adaptation remain poorly understood. Variation in the host receptor, dipeptidyl peptidase 4 (DPP4), can block the interaction with the MERS-CoV spike protein and form a species barrier to infection. To better understand the species adaptability of MERS-CoV, we identified a suboptimal species-derived variant of DPP4 to study viral adaption. Passaging virus on cells expressing this DPP4 variant led to accumulation of mutations in the viral spike which increased replication. Parallel passages revealed distinct paths of viral adaptation to the same DPP4 variant. Structural analysis and functional assays showed that these mutations enhanced viral entry with suboptimal DPP4 by altering the surface charge of spike. These findings demonstrate that MERS-CoV spike can utilize multiple paths to rapidly adapt to novel species variation in DPP4.</p></abstract><abstract abstract-type="graphical" id="abs0015"><title>Graphical Abstract</title><fig id="undfig1" position="anchor"><graphic xlink:href="fx1_lrg"></graphic></fig></abstract><abstract abstract-type="author-highlights" id="abs0020"><title>Highlights</title><p><list list-type="simple" id="ulist0010"><list-item id="u0010"><label>•</label><p id="p0010">MERS-CoV infected cells expressing DPP4 from 16 bat species</p></list-item><list-item id="u0015"><label>•</label><p id="p0015">MERS-CoV spike rapidly adapted to species variation in DPP4</p></list-item><list-item id="u0020"><label>•</label><p id="p0020">Viral adaptations modified the surface charge of viral spike</p></list-item><list-item id="u0025"><label>•</label><p id="p0025">Different routes of spike adaptation enhanced entry with the same DPP4 variant</p></list-item></list></p></abstract><abstract abstract-type="teaser" id="abs0025"><p>MERS-CoV is a zoonotic pathogen capable of infecting numerous species. However, our understanding of how this virus adapts to new species remains unclear. Letko et al. experimentally observe several different routes in the stepwise, adaptive evolution of MERS-CoV to a unique host-species variant of the viral receptor.</p></abstract><kwd-group id="kwrds0010"><title>Keywords</title><kwd>MERS</kwd><kwd>Coronavirus</kwd><kwd>Spike</kwd><kwd>DPP4</kwd><kwd>Dipeptidyl peptidase IV</kwd><kwd>Evolution</kwd><kwd>Zoonosis</kwd><kwd>Species barrier</kwd><kwd>Adaptation</kwd><kwd>Bat</kwd><kwd>Desmodus rotundus</kwd></kwd-group></article-meta><notes><p id="misc0010">Published: August 14, 2018</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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