Evaluation of the Biological Properties and Cross-Reactive Antibody Response to H10 Influenza Viruses in Ferrets
Identifieur interne : 000698 ( Pmc/Curation ); précédent : 000697; suivant : 000699Evaluation of the Biological Properties and Cross-Reactive Antibody Response to H10 Influenza Viruses in Ferrets
Auteurs : Troy C. Sutton ; Elaine W. Lamirande ; Rita Czako ; Kanta SubbaraoSource :
- Journal of Virology [ 0022-538X ] ; 2017.
Abstract
The recent outbreak of avian origin H10N7 influenza among seals in northern Europe and two fatal human infections with an avian H10N8 virus in China have demonstrated that H10 viruses can spread between mammals and cause severe disease in humans. To gain insight into the potential for H10 viruses to cross the species barrier and to identify a candidate vaccine strain, we evaluated the
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DOI: 10.1128/JVI.00895-17
PubMed: 28701401
PubMed Central: 5599738
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Evaluation of the Biological Properties and Cross-Reactive Antibody Response to H10 Influenza Viruses in Ferrets</title>
<author><name sortKey="Sutton, Troy C" sort="Sutton, Troy C" uniqKey="Sutton T" first="Troy C." last="Sutton">Troy C. Sutton</name>
</author>
<author><name sortKey="Lamirande, Elaine W" sort="Lamirande, Elaine W" uniqKey="Lamirande E" first="Elaine W." last="Lamirande">Elaine W. Lamirande</name>
</author>
<author><name sortKey="Czako, Rita" sort="Czako, Rita" uniqKey="Czako R" first="Rita" last="Czako">Rita Czako</name>
</author>
<author><name sortKey="Subbarao, Kanta" sort="Subbarao, Kanta" uniqKey="Subbarao K" first="Kanta" last="Subbarao">Kanta Subbarao</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Evaluation of the Biological Properties and Cross-Reactive Antibody Response to H10 Influenza Viruses in Ferrets</title>
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<author><name sortKey="Lamirande, Elaine W" sort="Lamirande, Elaine W" uniqKey="Lamirande E" first="Elaine W." last="Lamirande">Elaine W. Lamirande</name>
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<author><name sortKey="Czako, Rita" sort="Czako, Rita" uniqKey="Czako R" first="Rita" last="Czako">Rita Czako</name>
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<author><name sortKey="Subbarao, Kanta" sort="Subbarao, Kanta" uniqKey="Subbarao K" first="Kanta" last="Subbarao">Kanta Subbarao</name>
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<series><title level="j">Journal of Virology</title>
<idno type="ISSN">0022-538X</idno>
<idno type="eISSN">1098-5514</idno>
<imprint><date when="2017">2017</date>
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<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>The recent outbreak of avian origin H10N7 influenza among seals in northern Europe and two fatal human infections with an avian H10N8 virus in China have demonstrated that H10 viruses can spread between mammals and cause severe disease in humans. To gain insight into the potential for H10 viruses to cross the species barrier and to identify a candidate vaccine strain, we evaluated the <italic>in vitro</italic>
and <italic>in vivo</italic>
properties and antibody response in ferrets to 20 diverse H10 viruses. H10 virus infection of ferrets caused variable weight loss, and all 20 viruses replicated throughout the respiratory tract; however, replication in the lungs was highly variable. In glycan-binding assays, the H10 viruses preferentially bound “avian-like” α2,3-linked sialic acids. Importantly, several isolates also displayed strong binding to long-chain “human-like” α2,6-linked sialic acids and exhibited comparable or elevated neuraminidase activity relative to human H1N1, H2N2, and H3N2 viruses. In hemagglutination inhibition assays, 12 antisera cross-reacted with ≥14 of 20 H10 viruses, and 7 viruses induced neutralizing activity against ≥15 of the 20 viruses. By combining data on weight loss, viral replication, and the cross-reactive antibody response, we identified A/mallard/Portugal/79906/2009 (H10N7) as a suitable virus for vaccine development. Collectively, our findings suggest that H10 viruses may continue to sporadically infect humans and other mammals, underscoring the importance of developing an H10 vaccine for pandemic preparedness.</p>
<p><bold>IMPORTANCE</bold>
Avian origin H10 influenza viruses sporadically infect humans and other mammals; however, little is known about viruses of this subtype. Thus, we characterized the biological properties of 20 H10 viruses <italic>in vitro</italic>
and in ferrets. Infection caused mild to moderate weight loss (5 to 15%), with robust viral replication in the nasal tissues and variable replication in the lung. H10 viruses preferentially bind “avian-like” sialic acids, although several isolates also displayed binding to “human-like” sialic acid receptors. This is consistent with the ability of H10 viruses to cross the species barrier and warrants selection of an H10 vaccine strain. By evaluating the cross-reactive antibody response to the H10 viruses and combining this analysis with viral replication and weight loss findings, we identified A/mallard/Portugal/79906/2009 (H10N7) as a suitable H10 vaccine strain.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Virol</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Virol</journal-id>
<journal-id journal-id-type="hwp">jvi</journal-id>
<journal-id journal-id-type="pmc">jvi</journal-id>
<journal-id journal-id-type="publisher-id">JVI</journal-id>
<journal-title-group><journal-title>Journal of Virology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-538X</issn>
<issn pub-type="epub">1098-5514</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">28701401</article-id>
<article-id pub-id-type="pmc">5599738</article-id>
<article-id pub-id-type="publisher-id">00895-17</article-id>
<article-id pub-id-type="doi">10.1128/JVI.00895-17</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Vaccines and Antiviral Agents</subject>
</subj-group>
<subj-group subj-group-type="editorial-class"><subject>Spotlight</subject>
</subj-group>
</article-categories>
<title-group><article-title>Evaluation of the Biological Properties and Cross-Reactive Antibody Response to H10 Influenza Viruses in Ferrets</article-title>
<alt-title alt-title-type="running-head">Characterization of H10 Influenza Viruses</alt-title>
<alt-title alt-title-type="short-authors">Sutton et al.</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Sutton</surname>
<given-names>Troy C.</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Lamirande</surname>
<given-names>Elaine W.</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Czako</surname>
<given-names>Rita</given-names>
</name>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Subbarao</surname>
<given-names>Kanta</given-names>
</name>
<xref ref-type="author-notes" rid="fn1">*</xref>
</contrib>
<aff>Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA</aff>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Dermody</surname>
<given-names>Terence S.</given-names>
</name>
<role>Editor</role>
<aff>University of Pittsburgh School of Medicine</aff>
</contrib>
</contrib-group>
<author-notes><corresp id="cor1">Address correspondence to Kanta Subbarao, <email>ksubbarao@niaid.nih.gov</email>
.</corresp>
<fn id="fn1" fn-type="present-address"><label>*</label>
<p>Present address: Kanta Subbarao, WHO Collaborating Centre for Reference and Research on Influenza and University of Melbourne, Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.</p>
</fn>
<fn fn-type="other"><p><bold>Citation</bold>
Sutton TC, Lamirande EW, Czako R, Subbarao K. 2017. Evaluation of the biological properties and cross-reactive antibody response to H10 influenza viruses in ferrets. J Virol 91:e00895-17. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/JVI.00895-17">https://doi.org/10.1128/JVI.00895-17</ext-link>
.</p>
</fn>
</author-notes>
<pub-date pub-type="epreprint"><day>12</day>
<month>7</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="epub"><day>12</day>
<month>9</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection"><day>1</day>
<month>10</month>
<year>2017</year>
</pub-date>
<volume>91</volume>
<issue>19</issue>
<elocation-id>e00895-17</elocation-id>
<history><date date-type="received"><day>31</day>
<month>5</month>
<year>2017</year>
</date>
<date date-type="accepted"><day>5</day>
<month>7</month>
<year>2017</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2017 American Society for Microbiology.</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>American Society for Microbiology</copyright-holder>
<license license-type="asm" xlink:href="https://doi.org/10.1128/ASMCopyrightv1"><license-p><ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/ASMCopyrightv1">All Rights Reserved</ext-link>
.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="zjv019172918001.pdf"></self-uri>
<abstract><title>ABSTRACT</title>
<p>The recent outbreak of avian origin H10N7 influenza among seals in northern Europe and two fatal human infections with an avian H10N8 virus in China have demonstrated that H10 viruses can spread between mammals and cause severe disease in humans. To gain insight into the potential for H10 viruses to cross the species barrier and to identify a candidate vaccine strain, we evaluated the <italic>in vitro</italic>
and <italic>in vivo</italic>
properties and antibody response in ferrets to 20 diverse H10 viruses. H10 virus infection of ferrets caused variable weight loss, and all 20 viruses replicated throughout the respiratory tract; however, replication in the lungs was highly variable. In glycan-binding assays, the H10 viruses preferentially bound “avian-like” α2,3-linked sialic acids. Importantly, several isolates also displayed strong binding to long-chain “human-like” α2,6-linked sialic acids and exhibited comparable or elevated neuraminidase activity relative to human H1N1, H2N2, and H3N2 viruses. In hemagglutination inhibition assays, 12 antisera cross-reacted with ≥14 of 20 H10 viruses, and 7 viruses induced neutralizing activity against ≥15 of the 20 viruses. By combining data on weight loss, viral replication, and the cross-reactive antibody response, we identified A/mallard/Portugal/79906/2009 (H10N7) as a suitable virus for vaccine development. Collectively, our findings suggest that H10 viruses may continue to sporadically infect humans and other mammals, underscoring the importance of developing an H10 vaccine for pandemic preparedness.</p>
<p><bold>IMPORTANCE</bold>
Avian origin H10 influenza viruses sporadically infect humans and other mammals; however, little is known about viruses of this subtype. Thus, we characterized the biological properties of 20 H10 viruses <italic>in vitro</italic>
and in ferrets. Infection caused mild to moderate weight loss (5 to 15%), with robust viral replication in the nasal tissues and variable replication in the lung. H10 viruses preferentially bind “avian-like” sialic acids, although several isolates also displayed binding to “human-like” sialic acid receptors. This is consistent with the ability of H10 viruses to cross the species barrier and warrants selection of an H10 vaccine strain. By evaluating the cross-reactive antibody response to the H10 viruses and combining this analysis with viral replication and weight loss findings, we identified A/mallard/Portugal/79906/2009 (H10N7) as a suitable H10 vaccine strain.</p>
</abstract>
<kwd-group><title>KEYWORDS</title>
<kwd>avian viruses</kwd>
<kwd>influenza</kwd>
<kwd>influenza vaccines</kwd>
</kwd-group>
<funding-group><award-group id="award1"><funding-source id="gs1">NIAID Intramural Research Program</funding-source>
<principal-award-recipient>Kanta Subbarao</principal-award-recipient>
<principal-award-recipient>Troy Sutton</principal-award-recipient>
<principal-award-recipient>Elaine Lamirande</principal-award-recipient>
<principal-award-recipient>Rita Czako</principal-award-recipient>
</award-group>
</funding-group>
<counts><fig-count count="6"></fig-count>
<table-count count="4"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="58"></ref-count>
<page-count count="18"></page-count>
<word-count count="10803"></word-count>
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<custom-meta-group><custom-meta><meta-name>cover-date</meta-name>
<meta-value>October 2017</meta-value>
</custom-meta>
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</front>
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