Structural Definition of a Neutralization-Sensitive Epitope on the MERS-CoV S1-NTD
Identifieur interne : 000174 ( Pmc/Checkpoint ); précédent : 000173; suivant : 000175Structural Definition of a Neutralization-Sensitive Epitope on the MERS-CoV S1-NTD
Auteurs : Nianshuang Wang [États-Unis] ; Osnat Rosen [États-Unis] ; Lingshu Wang [États-Unis] ; Hannah L. Turner [États-Unis] ; Laura J. Stevens [États-Unis] ; Kizzmekia S. Corbett [États-Unis] ; Charles A. Bowman [États-Unis] ; Jesper Pallesen [États-Unis] ; Wei Shi [États-Unis] ; Yi Zhang [États-Unis] ; Kwanyee Leung [États-Unis] ; Robert N. Kirchdoerfer [États-Unis] ; Michelle M. Becker [États-Unis] ; Mark R. Denison [États-Unis] ; James D. Chappell [États-Unis] ; Andrew B. Ward [États-Unis] ; Barney S. Graham [États-Unis] ; Jason S. Mclellan [États-Unis]Source :
- Cell Reports [ 2211-1247 ] ; 2019.
Abstract
Middle East respiratory syndrome coronavirus (MERS-CoV) emerged into the human population in 2012 and has caused substantial morbidity and mortality. Potently neutralizing antibodies targeting the receptor-binding domain (RBD) on MERS-CoV spike (S) protein have been characterized, but much less is known about antibodies targeting non-RBD epitopes. Here, we report the structural and functional characterization of G2, a neutralizing antibody targeting the MERS-CoV S1 N-terminal domain (S1-NTD). Structures of G2 alone and in complex with the MERS-CoV S1-NTD define a site of vulnerability comprising two loops, each of which contain a residue mutated in G2-escape variants. Cell-surface binding studies and
Url:
DOI: 10.1016/j.celrep.2019.08.052
PubMed: 31553909
PubMed Central: 6935267
Affiliations:
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<author><name sortKey="Zhang, Yi" sort="Zhang, Yi" uniqKey="Zhang Y" first="Yi" last="Zhang">Yi Zhang</name>
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<author><name sortKey="Becker, Michelle M" sort="Becker, Michelle M" uniqKey="Becker M" first="Michelle M." last="Becker">Michelle M. Becker</name>
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<author><name sortKey="Denison, Mark R" sort="Denison, Mark R" uniqKey="Denison M" first="Mark R." last="Denison">Mark R. Denison</name>
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</placeName>
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<affiliation wicri:level="2"><nlm:aff id="aff5">Department of Pathology, Microbiology, and Immunology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA</nlm:aff>
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<wicri:regionArea>Department of Pathology, Microbiology, and Immunology, Vanderbilt University School of Medicine, Nashville, TN 37232</wicri:regionArea>
<placeName><region type="state">Tennessee</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Chappell, James D" sort="Chappell, James D" uniqKey="Chappell J" first="James D." last="Chappell">James D. Chappell</name>
<affiliation wicri:level="2"><nlm:aff id="aff4">Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, TN 37232, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, TN 37232</wicri:regionArea>
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</placeName>
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<author><name sortKey="Ward, Andrew B" sort="Ward, Andrew B" uniqKey="Ward A" first="Andrew B." last="Ward">Andrew B. Ward</name>
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<author><name sortKey="Graham, Barney S" sort="Graham, Barney S" uniqKey="Graham B" first="Barney S." last="Graham">Barney S. Graham</name>
<affiliation wicri:level="2"><nlm:aff id="aff2">Vaccine Research Center, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Vaccine Research Center, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892</wicri:regionArea>
<placeName><region type="state">Maryland</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Mclellan, Jason S" sort="Mclellan, Jason S" uniqKey="Mclellan J" first="Jason S." last="Mclellan">Jason S. Mclellan</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX 78712, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX 78712</wicri:regionArea>
<placeName><region type="state">Texas</region>
<settlement type="city">Austin (Texas)</settlement>
</placeName>
<orgName type="university">Université du Texas à Austin</orgName>
</affiliation>
</author>
</analytic>
<series><title level="j">Cell Reports</title>
<idno type="eISSN">2211-1247</idno>
<imprint><date when="2019">2019</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
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<profileDesc><textClass></textClass>
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</teiHeader>
<front><div type="abstract" xml:lang="en"><title>Summary</title>
<p>Middle East respiratory syndrome coronavirus (MERS-CoV) emerged into the human population in 2012 and has caused substantial morbidity and mortality. Potently neutralizing antibodies targeting the receptor-binding domain (RBD) on MERS-CoV spike (S) protein have been characterized, but much less is known about antibodies targeting non-RBD epitopes. Here, we report the structural and functional characterization of G2, a neutralizing antibody targeting the MERS-CoV S1 N-terminal domain (S1-NTD). Structures of G2 alone and in complex with the MERS-CoV S1-NTD define a site of vulnerability comprising two loops, each of which contain a residue mutated in G2-escape variants. Cell-surface binding studies and <italic>in vitro</italic>
competition experiments demonstrate that G2 strongly disrupts the attachment of MERS-CoV S to its receptor, dipeptidyl peptidase-4 (DPP4), with the inhibition requiring the native trimeric S conformation. These results advance our understanding of antibody-mediated neutralization of coronaviruses and should facilitate the development of immunotherapeutics and vaccines against MERS-CoV.</p>
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</name>
<email>jmclellan@austin.utexas.edu</email>
<xref rid="aff1" ref-type="aff">1</xref>
<xref rid="fn2" ref-type="fn">7</xref>
<xref rid="cor1" ref-type="corresp">∗</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX 78712, USA</aff>
<aff id="aff2"><label>2</label>
Vaccine Research Center, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA</aff>
<aff id="aff3"><label>3</label>
Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA 92037, USA</aff>
<aff id="aff4"><label>4</label>
Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, TN 37232, USA</aff>
<aff id="aff5"><label>5</label>
Department of Pathology, Microbiology, and Immunology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA</aff>
<author-notes><corresp id="cor1"><label>∗</label>
Corresponding author <email>jmclellan@austin.utexas.edu</email>
</corresp>
<fn id="fn1"><label>6</label>
<p id="ntpara0010">Present address: Department of Biotechnology, Israel Institute for Biological Research, Ness-ziona, Israel</p>
</fn>
<fn id="fn2"><label>7</label>
<p id="ntpara0015">Lead Contact</p>
</fn>
</author-notes>
<pub-date pub-type="pmc-release"><day>24</day>
<month>9</month>
<year>2019</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>24</day>
<month>9</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>24</day>
<month>9</month>
<year>2019</year>
</pub-date>
<volume>28</volume>
<issue>13</issue>
<fpage>3395</fpage>
<lpage>3405.e6</lpage>
<history><date date-type="received"><day>6</day>
<month>2</month>
<year>2019</year>
</date>
<date date-type="rev-recd"><day>6</day>
<month>6</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>16</day>
<month>8</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 The Author(s)</copyright-statement>
<copyright-year>2019</copyright-year>
<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) emerged into the human population in 2012 and has caused substantial morbidity and mortality. Potently neutralizing antibodies targeting the receptor-binding domain (RBD) on MERS-CoV spike (S) protein have been characterized, but much less is known about antibodies targeting non-RBD epitopes. Here, we report the structural and functional characterization of G2, a neutralizing antibody targeting the MERS-CoV S1 N-terminal domain (S1-NTD). Structures of G2 alone and in complex with the MERS-CoV S1-NTD define a site of vulnerability comprising two loops, each of which contain a residue mutated in G2-escape variants. Cell-surface binding studies and <italic>in vitro</italic>
competition experiments demonstrate that G2 strongly disrupts the attachment of MERS-CoV S to its receptor, dipeptidyl peptidase-4 (DPP4), with the inhibition requiring the native trimeric S conformation. These results advance our understanding of antibody-mediated neutralization of coronaviruses and should facilitate the development of immunotherapeutics and vaccines against MERS-CoV.</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">The epitope for the neutralizing antibody G2 is confined to the apex of the MERS-CoV S1-NTD</p>
</list-item>
<list-item id="u0015"><label>•</label>
<p id="p0015">G2 epitope is relatively well conserved</p>
</list-item>
<list-item id="u0020"><label>•</label>
<p id="p0020">G2 IgG and Fab both neutralize pseudotyped and authentic MERS-CoV</p>
</list-item>
<list-item id="u0025"><label>•</label>
<p id="p0025">G2 neutralizes by preventing the binding of DPP4 to trimeric S protein</p>
</list-item>
</list>
</p>
</abstract>
<abstract abstract-type="teaser" id="abs0025"><p>Wang et al. report the structural and functional characterization of the Middle East respiratory syndrome coronavirus (MERS-CoV)-neutralizing antibody G2. G2 recognizes a conserved epitope on the MERS-CoV S1 N-terminal domain (S1-NTD) and neutralizes MERS-CoV by interfering with binding to host receptor dipeptidyl peptidase-4 (DPP4). The findings are relevant for understanding the viral attachment mechanism and for the development of S1-NTD-based vaccines.</p>
</abstract>
<kwd-group id="kwrds0010"><title>Keywords</title>
<kwd>MERS-CoV</kwd>
<kwd>coronavirus</kwd>
<kwd>crystal structure</kwd>
<kwd>electron microscopy</kwd>
<kwd>DPP4</kwd>
<kwd>receptor-binding</kwd>
<kwd>membrane fusion</kwd>
</kwd-group>
</article-meta>
<notes><p id="misc0010">Published: September 24, 2019</p>
</notes>
</front>
</pmc>
<affiliations><list><country><li>États-Unis</li>
</country>
<region><li>Californie</li>
<li>Maryland</li>
<li>Tennessee</li>
<li>Texas</li>
</region>
<settlement><li>Austin (Texas)</li>
</settlement>
<orgName><li>Université du Texas à Austin</li>
</orgName>
</list>
<tree><country name="États-Unis"><region name="Texas"><name sortKey="Wang, Nianshuang" sort="Wang, Nianshuang" uniqKey="Wang N" first="Nianshuang" last="Wang">Nianshuang Wang</name>
</region>
<name sortKey="Becker, Michelle M" sort="Becker, Michelle M" uniqKey="Becker M" first="Michelle M." last="Becker">Michelle M. Becker</name>
<name sortKey="Bowman, Charles A" sort="Bowman, Charles A" uniqKey="Bowman C" first="Charles A." last="Bowman">Charles A. Bowman</name>
<name sortKey="Chappell, James D" sort="Chappell, James D" uniqKey="Chappell J" first="James D." last="Chappell">James D. Chappell</name>
<name sortKey="Corbett, Kizzmekia S" sort="Corbett, Kizzmekia S" uniqKey="Corbett K" first="Kizzmekia S." last="Corbett">Kizzmekia S. Corbett</name>
<name sortKey="Denison, Mark R" sort="Denison, Mark R" uniqKey="Denison M" first="Mark R." last="Denison">Mark R. Denison</name>
<name sortKey="Denison, Mark R" sort="Denison, Mark R" uniqKey="Denison M" first="Mark R." last="Denison">Mark R. Denison</name>
<name sortKey="Graham, Barney S" sort="Graham, Barney S" uniqKey="Graham B" first="Barney S." last="Graham">Barney S. Graham</name>
<name sortKey="Kirchdoerfer, Robert N" sort="Kirchdoerfer, Robert N" uniqKey="Kirchdoerfer R" first="Robert N." last="Kirchdoerfer">Robert N. Kirchdoerfer</name>
<name sortKey="Leung, Kwanyee" sort="Leung, Kwanyee" uniqKey="Leung K" first="Kwanyee" last="Leung">Kwanyee Leung</name>
<name sortKey="Mclellan, Jason S" sort="Mclellan, Jason S" uniqKey="Mclellan J" first="Jason S." last="Mclellan">Jason S. Mclellan</name>
<name sortKey="Pallesen, Jesper" sort="Pallesen, Jesper" uniqKey="Pallesen J" first="Jesper" last="Pallesen">Jesper Pallesen</name>
<name sortKey="Rosen, Osnat" sort="Rosen, Osnat" uniqKey="Rosen O" first="Osnat" last="Rosen">Osnat Rosen</name>
<name sortKey="Shi, Wei" sort="Shi, Wei" uniqKey="Shi W" first="Wei" last="Shi">Wei Shi</name>
<name sortKey="Stevens, Laura J" sort="Stevens, Laura J" uniqKey="Stevens L" first="Laura J." last="Stevens">Laura J. Stevens</name>
<name sortKey="Turner, Hannah L" sort="Turner, Hannah L" uniqKey="Turner H" first="Hannah L." last="Turner">Hannah L. Turner</name>
<name sortKey="Wang, Lingshu" sort="Wang, Lingshu" uniqKey="Wang L" first="Lingshu" last="Wang">Lingshu Wang</name>
<name sortKey="Ward, Andrew B" sort="Ward, Andrew B" uniqKey="Ward A" first="Andrew B." last="Ward">Andrew B. Ward</name>
<name sortKey="Zhang, Yi" sort="Zhang, Yi" uniqKey="Zhang Y" first="Yi" last="Zhang">Yi Zhang</name>
</country>
</tree>
</affiliations>
</record>
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