Distinct Roles for Sialoside and Protein Receptors in Coronavirus Infection
Identifieur interne : 000091 ( Pmc/Checkpoint ); précédent : 000090; suivant : 000092Distinct Roles for Sialoside and Protein Receptors in Coronavirus Infection
Auteurs : Enya Qing [États-Unis] ; Michael Hantak [États-Unis] ; Stanley Perlman [États-Unis] ; Tom Gallagher [États-Unis]Source :
- mBio [ 2150-7511 ] ; 2020.
Abstract
CoVs can transmit from animals to humans to cause serious disease. This zoonotic transmission uses spike proteins, which bind CoVs to cells with two receptor-binding domains. Here, we identified the roles for the two binding processes in the CoV infection process. Binding to sialic acids promoted infection and also supported the intercellular expansion of CoV infections through syncytial development. Adaptive mutations in the sialic acid-binding spike domains increased the intercellular expansion process. These findings raise the possibility that the lectin-like properties of many CoVs contribute to facile zoonotic transmission and intercellular spread within infected organisms.
Url:
DOI: 10.1128/mBio.02764-19
PubMed: 32047128
PubMed Central: 7018658
Affiliations:
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Gallagher</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois</wicri:regionArea><placeName><region type="state">Illinois</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">32047128</idno><idno type="pmc">7018658</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7018658</idno><idno type="RBID">PMC:7018658</idno><idno type="doi">10.1128/mBio.02764-19</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">001249</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001249</idno><idno type="wicri:Area/Pmc/Curation">001249</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">001249</idno><idno type="wicri:Area/Pmc/Checkpoint">000091</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000091</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Distinct Roles for Sialoside and Protein Receptors in Coronavirus Infection</title><author><name sortKey="Qing, Enya" sort="Qing, Enya" uniqKey="Qing E" first="Enya" last="Qing">Enya Qing</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois</wicri:regionArea><placeName><region type="state">Illinois</region></placeName></affiliation></author><author><name sortKey="Hantak, Michael" sort="Hantak, Michael" uniqKey="Hantak M" first="Michael" last="Hantak">Michael Hantak</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois</wicri:regionArea><placeName><region type="state">Illinois</region></placeName></affiliation></author><author><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation></author><author><name sortKey="Gallagher, Tom" sort="Gallagher, Tom" uniqKey="Gallagher T" first="Tom" last="Gallagher">Tom Gallagher</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois</wicri:regionArea><placeName><region type="state">Illinois</region></placeName></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>CoVs can transmit from animals to humans to cause serious disease. This zoonotic transmission uses spike proteins, which bind CoVs to cells with two receptor-binding domains. Here, we identified the roles for the two binding processes in the CoV infection process. Binding to sialic acids promoted infection and also supported the intercellular expansion of CoV infections through syncytial development. Adaptive mutations in the sialic acid-binding spike domains increased the intercellular expansion process. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">mBio</journal-id><journal-id journal-id-type="iso-abbrev">mBio</journal-id><journal-id journal-id-type="hwp">mbio</journal-id><journal-id journal-id-type="pmc">mbio</journal-id><journal-id journal-id-type="publisher-id">mBio</journal-id><journal-title-group><journal-title>mBio</journal-title></journal-title-group><issn pub-type="epub">2150-7511</issn><publisher><publisher-name>American Society for Microbiology</publisher-name><publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">32047128</article-id><article-id pub-id-type="pmc">7018658</article-id><article-id pub-id-type="publisher-id">mBio02764-19</article-id><article-id pub-id-type="doi">10.1128/mBio.02764-19</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="overline"><subject>Host-Microbe Biology</subject></subj-group></article-categories><title-group><article-title>Distinct Roles for Sialoside and Protein Receptors in Coronavirus Infection</article-title><alt-title alt-title-type="running-head">Sialic Acids Facilitate Coronavirus Dissemination</alt-title><alt-title alt-title-type="short-authors">Qing et al.</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Qing</surname><given-names>Enya</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Hantak</surname><given-names>Michael</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn1">*</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-4213-2354</contrib-id><name><surname>Perlman</surname><given-names>Stanley</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Gallagher</surname><given-names>Tom</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><aff id="aff1"><label>a</label><addr-line>Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois, USA</addr-line></aff><aff id="aff2"><label>b</label><addr-line>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA</addr-line></aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Denison</surname><given-names>Mark R.</given-names></name><role>Editor</role><aff>Vanderbilt University Medical Center</aff></contrib></contrib-group><author-notes><corresp id="cor1">Address correspondence to Tom Gallagher, <email>tgallag@luc.edu</email>.</corresp><fn id="fn1" fn-type="present-address"><label>*</label><p>Present address: Michael Hantak, Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, Utah, USA.</p></fn></author-notes><pub-date pub-type="epub"><day>11</day><month>2</month><year>2020</year></pub-date><pub-date pub-type="collection"><season>Jan-Feb</season><year>2020</year></pub-date><volume>11</volume><issue>1</issue><elocation-id>e02764-19</elocation-id><history><date date-type="received"><day>15</day><month>10</month><year>2019</year></date><date date-type="accepted"><day>21</day><month>1</month><year>2020</year></date></history><permissions><copyright-statement>Copyright © 2020 Qing et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Qing et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="mBio.02764-19.pdf"></self-uri><abstract abstract-type="precis"><p>CoVs can transmit from animals to humans to cause serious disease. This zoonotic transmission uses spike proteins, which bind CoVs to cells with two receptor-binding domains. Here, we identified the roles for the two binding processes in the CoV infection process. Binding to sialic acids promoted infection and also supported the intercellular expansion of CoV infections through syncytial development. Adaptive mutations in the sialic acid-binding spike domains increased the intercellular expansion process. These findings raise the possibility that the lectin-like properties of many CoVs contribute to facile zoonotic transmission and intercellular spread within infected organisms.</p></abstract><abstract><title>ABSTRACT</title><p>Coronaviruses (CoVs) are common human and animal pathogens that can transmit zoonotically and cause severe respiratory disease syndromes. CoV infection requires spike proteins, which bind viruses to host cell receptors and catalyze virus-cell membrane fusion. Several CoV strains have spike proteins with two receptor-binding domains, an S1A that engages host sialic acids and an S1B that recognizes host transmembrane proteins. As this bivalent binding may enable broad zoonotic CoV infection, we aimed to identify roles for each receptor in distinct infection stages. Focusing on two betacoronaviruses, murine JHM-CoV and human Middle East respiratory syndrome coronavirus (MERS-CoV), we found that virus particle binding to cells was mediated by sialic acids; however, the transmembrane protein receptors were required for a subsequent virus infection. These results favored a two-step process in which viruses first adhere to sialic acids and then require subsequent engagement with protein receptors during infectious cell entry. However, sialic acids sufficiently facilitated the later stages of virus spread through cell-cell membrane fusion, without requiring protein receptors. This virus spread in the absence of the prototype protein receptors was increased by adaptive S1A mutations. Overall, these findings reveal roles for sialic acids in virus-cell binding, viral spike protein-directed cell-cell fusion, and resultant spread of CoV infections.</p></abstract><kwd-group><title>KEYWORDS</title><kwd>coronavirus</kwd><kwd>virus entry</kwd><kwd>virus receptors</kwd><kwd>virus glycoproteins</kwd><kwd>sialic acids</kwd><kwd>membrane fusion</kwd></kwd-group><funding-group><award-group id="award1"><funding-source><institution-wrap><institution>HHS | National Institutes of Health (NIH)</institution><institution-id>https://doi.org/10.13039/100000002</institution-id></institution-wrap></funding-source><award-id>P01 AI060699</award-id><principal-award-recipient><name><surname>Gallagher</surname><given-names>Tom</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Perlman</surname><given-names>Stanley</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Qing</surname><given-names>Enya</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Hantak</surname><given-names>Michael</given-names></name></principal-award-recipient></award-group></funding-group><counts><count count="5" count-type="supplementary-material"></count><fig-count count="7"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="90"></ref-count><page-count count="18"></page-count><word-count count="11332"></word-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>January/February 2020</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Illinois</li><li>Iowa</li></region><settlement><li>Iowa City</li></settlement><orgName><li>Université de l'Iowa</li></orgName></list><tree><country name="États-Unis"><region name="Illinois"><name sortKey="Qing, Enya" sort="Qing, Enya" uniqKey="Qing E" first="Enya" last="Qing">Enya Qing</name></region><name sortKey="Gallagher, Tom" sort="Gallagher, Tom" uniqKey="Gallagher T" first="Tom" last="Gallagher">Tom Gallagher</name><name sortKey="Hantak, Michael" sort="Hantak, Michael" uniqKey="Hantak M" first="Michael" last="Hantak">Michael Hantak</name><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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