Glycan-binding preferences and genetic evolution of human seasonal influenza A(H3N2) viruses during 1999-2007 in Taiwan
Identifieur interne : 000A80 ( Pmc/Curation ); précédent : 000A79; suivant : 000A81Glycan-binding preferences and genetic evolution of human seasonal influenza A(H3N2) viruses during 1999-2007 in Taiwan
Auteurs : Ya-Fang Wang [Taïwan] ; Chuan-Fa Chang [Taïwan] ; Huey-Pin Tsai [Taïwan] ; Chia-Yu Chi [Taïwan] ; Ih-Jen Su [Taïwan] ; Jen-Ren Wang [Taïwan]Source :
- PLoS ONE [ 1932-6203 ] ; 2018.
Abstract
It is generally agreed that human influenza virus preferentially binds to α-2,6-linked sialic acid-containing receptors, and mutations that change the binding preference may alter virus infectivity and host tropism. Limited information is available on the glycan-binding specificity of epidemic influenza viruses. In this study, we systemically investigated the glycan-binding preferences of human influenza A(H3N2) viruses isolated from 1999 to 2007 in Taiwan using a high-throughput carbohydrate array. The binding patterns of 37 H3N2 viruses were classified into three groups with significant binding-pattern variations. The results showed that the carbohydrate-binding patterns of H3N2 varied over time. A phylogenetic analysis of the hemagglutinin gene also revealed progressive drift year to year. Of note, the viruses that caused large outbreaks in 1999 and 2003 showed glycan-binding preferences to both α-2,3 and α-2,6 sialylated glycans. Twenty amino acid substitutions were identified primarily at antigenic sites that might contribute to H3N2 virus evolution and the change in the glycan-binding patterns. This study provides not only a systematic analysis of the receptor-binding specificity of influenza clinical isolates but also information that could help to monitor the outbreak potential and virus evolution of influenza viruses.
Url:
DOI: 10.1371/journal.pone.0196727
PubMed: 29746492
PubMed Central: 5945028
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Biotechnology, College of Medicine, National Cheng Kung University, Tainan, Taiwan</addr-line></nlm:aff><country xml:lang="fr">Taïwan</country><wicri:regionArea>Department of Medical Laboratory Science and Biotechnology, College of Medicine, National Cheng Kung University, Tainan</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Center of Infectious Disease and Signaling Research, National Cheng Kung University, Tainan, Taiwan</addr-line></nlm:aff><country xml:lang="fr">Taïwan</country><wicri:regionArea>Center of Infectious Disease and Signaling Research, National Cheng Kung University, Tainan</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Department of Pathology, National Cheng Kung University Hospital, Tainan, Taiwan</addr-line></nlm:aff><country xml:lang="fr">Taïwan</country><wicri:regionArea>Department of Pathology, National Cheng Kung University Hospital, 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Limited information is available on the glycan-binding specificity of epidemic influenza viruses. In this study, we systemically investigated the glycan-binding preferences of human influenza A(H3N2) viruses isolated from 1999 to 2007 in Taiwan using a high-throughput carbohydrate array. The binding patterns of 37 H3N2 viruses were classified into three groups with significant binding-pattern variations. The results showed that the carbohydrate-binding patterns of H3N2 varied over time. A phylogenetic analysis of the hemagglutinin gene also revealed progressive drift year to year. Of note, the viruses that caused large outbreaks in 1999 and 2003 showed glycan-binding preferences to both α-2,3 and α-2,6 sialylated glycans. Twenty amino acid substitutions were identified primarily at antigenic sites that might contribute to H3N2 virus evolution and the change in the glycan-binding patterns. This study provides not only a systematic analysis of the receptor-binding specificity of influenza clinical isolates but also information that could help to monitor the outbreak potential and virus evolution of influenza viruses.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Kobayashi, Y" uniqKey="Kobayashi Y">Y Kobayashi</name></author><author><name sortKey="Suzuki, Y" uniqKey="Suzuki Y">Y Suzuki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Viswanathan, K" uniqKey="Viswanathan K">K Viswanathan</name></author><author><name sortKey="Koh, X" uniqKey="Koh X">X Koh</name></author><author><name sortKey="Chandrasekaran, A" uniqKey="Chandrasekaran A">A Chandrasekaran</name></author><author><name sortKey="Pappas, C" uniqKey="Pappas C">C Pappas</name></author><author><name sortKey="Raman, R" uniqKey="Raman R">R Raman</name></author><author><name sortKey="Srinivasan, A" uniqKey="Srinivasan A">A 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">29746492</article-id><article-id pub-id-type="pmc">5945028</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0196727</article-id><article-id pub-id-type="publisher-id">PONE-D-17-23902</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza Viruses</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical Microbiology</subject><subj-group><subject>Microbial Pathogens</subject><subj-group><subject>Viral Pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza Viruses</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Pathology and Laboratory Medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial Pathogens</subject><subj-group><subject>Viral Pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza Viruses</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral Pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza Viruses</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Infectious Diseases</subject><subj-group><subject>Viral Diseases</subject><subj-group><subject>Influenza</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Microbial Evolution</subject><subj-group><subject>Viral Evolution</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Evolutionary Biology</subject><subj-group><subject>Organismal Evolution</subject><subj-group><subject>Microbial Evolution</subject><subj-group><subject>Viral Evolution</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Virology</subject><subj-group><subject>Viral Evolution</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Evolutionary Biology</subject><subj-group><subject>Evolutionary Systematics</subject><subj-group><subject>Phylogenetics</subject><subj-group><subject>Phylogenetic Analysis</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Taxonomy</subject><subj-group><subject>Evolutionary Systematics</subject><subj-group><subject>Phylogenetics</subject><subj-group><subject>Phylogenetic Analysis</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Computer and Information Sciences</subject><subj-group><subject>Data Management</subject><subj-group><subject>Taxonomy</subject><subj-group><subject>Evolutionary Systematics</subject><subj-group><subject>Phylogenetics</subject><subj-group><subject>Phylogenetic Analysis</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Database and Informatics Methods</subject><subj-group><subject>Bioinformatics</subject><subj-group><subject>Sequence Analysis</subject><subj-group><subject>Sequence Alignment</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Evolutionary Biology</subject><subj-group><subject>Evolutionary Genetics</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Physical Sciences</subject><subj-group><subject>Chemistry</subject><subj-group><subject>Chemical Compounds</subject><subj-group><subject>Organic Compounds</subject><subj-group><subject>Amino Acids</subject><subj-group><subject>Amino Acid Substitution</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Physical Sciences</subject><subj-group><subject>Chemistry</subject><subj-group><subject>Organic Chemistry</subject><subj-group><subject>Organic Compounds</subject><subj-group><subject>Amino Acids</subject><subj-group><subject>Amino Acid Substitution</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Amino Acids</subject><subj-group><subject>Amino Acid Substitution</subject></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Glycan-binding preferences and genetic evolution of human seasonal influenza A(H3N2) viruses during 1999-2007 in Taiwan</article-title><alt-title alt-title-type="running-head">Glycan-binding preferences and genetic evolution of human influenza A(H3N2) virus</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Ya-Fang</given-names></name><role content-type="http://credit.casrai.org/">Writing – original draft</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Chang</surname><given-names>Chuan-Fa</given-names></name><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Methodology</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Tsai</surname><given-names>Huey-Pin</given-names></name><role content-type="http://credit.casrai.org/">Resources</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Chi</surname><given-names>Chia-Yu</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Su</surname><given-names>Ih-Jen</given-names></name><role content-type="http://credit.casrai.org/">Supervision</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-4127-4046</contrib-id><name><surname>Wang</surname><given-names>Jen-Ren</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref><xref ref-type="aff" rid="aff004"><sup>4</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>National Institute of Infectious Diseases and Vaccinology, National Health Research Institutes, Tainan, Taiwan</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Department of Medical Laboratory Science and Biotechnology, College of Medicine, National Cheng Kung University, Tainan, Taiwan</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Center of Infectious Disease and Signaling Research, National Cheng Kung University, Tainan, Taiwan</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Department of Pathology, National Cheng Kung University Hospital, Tainan, Taiwan</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Department of Pediatrics, National Cheng Kung University Hospital, Tainan, Taiwan</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Menéndez-Arias</surname><given-names>Luis</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Consejo Superior de Investigaciones Cientificas, SPAIN</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><corresp id="cor001">* E-mail: <email>jrwang@mail.ncku.edu.tw</email></corresp></author-notes><pub-date pub-type="epub"><day>10</day><month>5</month><year>2018</year></pub-date><pub-date pub-type="collection"><year>2018</year></pub-date><volume>13</volume><issue>5</issue><elocation-id>e0196727</elocation-id><history><date date-type="received"><day>23</day><month>6</month><year>2017</year></date><date date-type="accepted"><day>18</day><month>4</month><year>2018</year></date></history><permissions><copyright-statement>© 2018 Wang et al</copyright-statement><copyright-year>2018</copyright-year><copyright-holder>Wang et al</copyright-holder><license xlink:href="http://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="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0196727.pdf"></self-uri><abstract><p>It is generally agreed that human influenza virus preferentially binds to α-2,6-linked sialic acid-containing receptors, and mutations that change the binding preference may alter virus infectivity and host tropism. Limited information is available on the glycan-binding specificity of epidemic influenza viruses. In this study, we systemically investigated the glycan-binding preferences of human influenza A(H3N2) viruses isolated from 1999 to 2007 in Taiwan using a high-throughput carbohydrate array. The binding patterns of 37 H3N2 viruses were classified into three groups with significant binding-pattern variations. The results showed that the carbohydrate-binding patterns of H3N2 varied over time. A phylogenetic analysis of the hemagglutinin gene also revealed progressive drift year to year. Of note, the viruses that caused large outbreaks in 1999 and 2003 showed glycan-binding preferences to both α-2,3 and α-2,6 sialylated glycans. Twenty amino acid substitutions were identified primarily at antigenic sites that might contribute to H3N2 virus evolution and the change in the glycan-binding patterns. This study provides not only a systematic analysis of the receptor-binding specificity of influenza clinical isolates but also information that could help to monitor the outbreak potential and virus evolution of influenza viruses.</p></abstract><funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100004737</institution-id><institution>National Health Research Institutes</institution></institution-wrap></funding-source><award-id>99A1-IDPP13-014</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-4127-4046</contrib-id><name><surname>Wang</surname><given-names>Jen-Ren</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100004663</institution-id><institution>Ministry of Science and Technology, Taiwan</institution></institution-wrap></funding-source><award-id>MOST 104-2321-B006-002</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-4127-4046</contrib-id><name><surname>Wang</surname><given-names>Jen-Ren</given-names></name></principal-award-recipient></award-group><funding-statement>This study was financially supported by grants from the National Health Research Institutes (99A1-IDPP13-014, 05A1-IVPP09-014), Center of Infectious Diseases and Signal Research, National Cheng Kung University, Aim for the Top University Project, Ministry of Education, and Ministry of Science and Technology (MOST) (grant no. MOST 104-2321-B006-002).</funding-statement></funding-group><counts><fig-count count="5"></fig-count><table-count count="3"></table-count><page-count count="15"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All sequence data are available from the GenBank database (accession numbers KU662097-KU662129 and MG309818-MG309872) and also in Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All sequence data are available from the GenBank database (accession numbers KU662097-KU662129 and MG309818-MG309872) and also in Supporting Information files.</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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