Anti-neuraminidase antibodies against pandemic A/H1N1 influenza viruses in healthy and influenza-infected individuals
Identifieur interne : 000A79 ( Pmc/Curation ); précédent : 000A78; suivant : 000A80Anti-neuraminidase antibodies against pandemic A/H1N1 influenza viruses in healthy and influenza-infected individuals
Auteurs : Yulia Desheva [Russie] ; Ivan Sychev [Russie] ; Tatiana Smolonogina [Russie] ; Andrey Rekstin [Russie] ; Natalia Ilyushina [États-Unis] ; Vladimir Lugovtsev [États-Unis] ; Anastasia Samsonova [États-Unis] ; Aleksey Go [Russie] ; Anna Lerner [Russie]Source :
- PLoS ONE [ 1932-6203 ] ; 2018.
Abstract
The main objective of the study was to evaluate neuraminidase inhibiting (NI) antibodies against A/H1N1pdm09 influenza viruses in the community as a whole and after infection. We evaluated NI serum antibodies against A/California/07/09(H1N1)pdm and A/South Africa/3626/2013(H1N1)pdm in 134 blood donors of different ages using enzyme-linked lectin assay and in 15 paired sera from convalescents with laboratory confirmed influenza. The neuraminidase (NA) proteins of both A/H1N1pdm09 viruses had minimal genetic divergence, but demonstrated different enzymatic and antigenic properties. 5.2% of individuals had NI antibody titers ≥1:20 against A/South Africa/3626/2013(H1N1)pdm compared to 53% of those who were positive to A/California/07/2009(H1N1)pdm NA. 2% of individuals had detectable NI titers against A/South Africa/3626/13(H1N1)pdm and 47.3% were positive to A/California/07/2009(H1N1)pdm NA among participants negative to hemagglutinin (HA) of A/H1N1pdm09 but positive to seasonal A/H1N1. The lowest NI antibody levels to both A/H1N1pdm09 viruses were detected in individuals born between 1956 and 1968. Our data suggest that NI antibodies against A/South Africa/3626/13 (H1N1)pdm found in the blood donors could have resulted from direct infection with a new antigenic A/H1N1pdm09 variant rather than from cross-reaction as a result of contact with previously circulating seasonal A/H1N1 variants. The immune responses against HA and NA were formed simultaneously right after natural infection with A/H1N1pdm09. NI antibodies correlated with virus-neutralizing antibodies when acquired shortly after influenza infection. A group of middle-aged patients with the lowest level of anti-NA antibodies against A/California/07/2009 (H1N1)pdm was identified, indicating the highest-priority vaccination against A/H1N1pdm09 viruses.
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DOI: 10.1371/journal.pone.0196771
PubMed: 29742168
PubMed Central: 5942809
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Desheva</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Department, Federal State Budgetary Scientific Institution “Institute of Experimental Medicine”, Saint Petersburg, Russian Federation</addr-line></nlm:aff><country xml:lang="fr">Russie</country><wicri:regionArea>Virology Department, Federal State Budgetary Scientific Institution “Institute of Experimental Medicine”, Saint Petersburg</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Department of Fundamental Problems of Medicine and Medical Technologies, Saint Petersburg State University, Saint Petersburg, Russian Federation</addr-line></nlm:aff><country xml:lang="fr">Russie</country><wicri:regionArea>Department of Fundamental Problems of Medicine and Medical Technologies, Saint Petersburg State University, Saint Petersburg</wicri:regionArea></affiliation></author><author><name sortKey="Sychev, Ivan" sort="Sychev, Ivan" uniqKey="Sychev I" first="Ivan" last="Sychev">Ivan Sychev</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Department, Federal State Budgetary Scientific Institution “Institute of Experimental Medicine”, Saint Petersburg, Russian Federation</addr-line></nlm:aff><country xml:lang="fr">Russie</country><wicri:regionArea>Virology Department, Federal State Budgetary Scientific Institution “Institute of Experimental Medicine”, Saint Petersburg</wicri:regionArea></affiliation></author><author><name sortKey="Smolonogina, Tatiana" sort="Smolonogina, Tatiana" uniqKey="Smolonogina T" first="Tatiana" last="Smolonogina">Tatiana Smolonogina</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Department, Federal State Budgetary Scientific Institution “Institute of Experimental Medicine”, Saint Petersburg, Russian Federation</addr-line></nlm:aff><country xml:lang="fr">Russie</country><wicri:regionArea>Virology Department, Federal State Budgetary Scientific Institution “Institute of 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Silver Spring, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Biotechnology Research and Review II, Center for Drug Evaluation and Research, U.S. Food and Drug Administration, Silver Spring, Maryland</wicri:regionArea></affiliation></author><author><name sortKey="Lugovtsev, Vladimir" sort="Lugovtsev, Vladimir" uniqKey="Lugovtsev V" first="Vladimir" last="Lugovtsev">Vladimir Lugovtsev</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Division of Viral Products, Center for Biologics Evaluation and Research, Food and Drug Administration, Silver Spring, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Viral Products, Center for Biologics Evaluation and Research, Food and Drug Administration, Silver Spring, Maryland</wicri:regionArea></affiliation></author><author><name sortKey="Samsonova, Anastasia" sort="Samsonova, Anastasia" uniqKey="Samsonova A" first="Anastasia" last="Samsonova">Anastasia Samsonova</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Division of Viral Products, Center for Biologics Evaluation and Research, Food and Drug Administration, Silver Spring, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Viral Products, Center for Biologics Evaluation and Research, Food and Drug Administration, Silver Spring, Maryland</wicri:regionArea></affiliation></author><author><name sortKey="Go, Aleksey" sort="Go, Aleksey" uniqKey="Go A" first="Aleksey" last="Go">Aleksey Go</name><affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Clinical and Diagnostic Center, Research Institute of Influenza, Saint Petersburg, Russian Federation</addr-line></nlm:aff><country xml:lang="fr">Russie</country><wicri:regionArea>Clinical and Diagnostic Center, Research Institute of Influenza, Saint Petersburg</wicri:regionArea></affiliation></author><author><name sortKey="Lerner, Anna" sort="Lerner, Anna" uniqKey="Lerner A" first="Anna" last="Lerner">Anna Lerner</name><affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>Medical Research Center, Federal State Budgetary Scientific Institution “Institute of Experimental Medicine”, Saint Petersburg, Russian Federation</addr-line></nlm:aff><country xml:lang="fr">Russie</country><wicri:regionArea>Medical Research Center, Federal State Budgetary Scientific Institution “Institute of Experimental Medicine”, Saint Petersburg</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The main objective of the study was to evaluate neuraminidase inhibiting (NI) antibodies against A/H1N1pdm09 influenza viruses in the community as a whole and after infection. We evaluated NI serum antibodies against A/California/07/09(H1N1)pdm and A/South Africa/3626/2013(H1N1)pdm in 134 blood donors of different ages using enzyme-linked lectin assay and in 15 paired sera from convalescents with laboratory confirmed influenza. The neuraminidase (NA) proteins of both A/H1N1pdm09 viruses had minimal genetic divergence, but demonstrated different enzymatic and antigenic properties. 5.2% of individuals had NI antibody titers ≥1:20 against A/South Africa/3626/2013(H1N1)pdm compared to 53% of those who were positive to A/California/07/2009(H1N1)pdm NA. 2% of individuals had detectable NI titers against A/South Africa/3626/13(H1N1)pdm and 47.3% were positive to A/California/07/2009(H1N1)pdm NA among participants negative to hemagglutinin (HA) of A/H1N1pdm09 but positive to seasonal A/H1N1. The lowest NI antibody levels to both A/H1N1pdm09 viruses were detected in individuals born between 1956 and 1968. Our data suggest that NI antibodies against A/South Africa/3626/13 (H1N1)pdm found in the blood donors could have resulted from direct infection with a new antigenic A/H1N1pdm09 variant rather than from cross-reaction as a result of contact with previously circulating seasonal A/H1N1 variants. The immune responses against HA and NA were formed simultaneously right after natural infection with A/H1N1pdm09. NI antibodies correlated with virus-neutralizing antibodies when acquired shortly after influenza infection. A group of middle-aged patients with the lowest level of anti-NA antibodies against A/California/07/2009 (H1N1)pdm was identified, indicating the highest-priority vaccination against A/H1N1pdm09 viruses.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Komissarov, A" uniqKey="Komissarov A">A Komissarov</name></author><author><name sortKey="Fadeev, A" uniqKey="Fadeev A">A Fadeev</name></author><author><name sortKey="Sergeeva, M" uniqKey="Sergeeva M">M Sergeeva</name></author><author><name sortKey="Petrov, S" uniqKey="Petrov S">S Petrov</name></author><author><name sortKey="Sintsova, K" uniqKey="Sintsova K">K Sintsova</name></author><author><name sortKey="Egorova, A" uniqKey="Egorova A">A Egorova</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Monto, A" uniqKey="Monto A">A Monto</name></author><author><name sortKey="Kendal, A" uniqKey="Kendal A">A 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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><subject>H1N1</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>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><subject>H1N1</subject></subj-group></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><subject>H1N1</subject></subj-group></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><subject>H1N1</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>Pulmonology</subject><subj-group><subject>Respiratory Infections</subject></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>Biological Databases</subject><subj-group><subject>Sequence Databases</subject></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 Databases</subject></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Anti-neuraminidase antibodies against pandemic A/H1N1 influenza viruses in healthy and influenza-infected individuals</article-title><alt-title alt-title-type="running-head">Anti-neuraminidase antibodies against pandemic A/H1N1 influenza in healthy and influenza-infected individuals</alt-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-9794-3520</contrib-id><name><surname>Desheva</surname><given-names>Yulia</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Supervision</role><role content-type="http://credit.casrai.org/">Writing – original draft</role><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="corresp" rid="cor001">*</xref></contrib><contrib contrib-type="author"><name><surname>Sychev</surname><given-names>Ivan</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Validation</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Smolonogina</surname><given-names>Tatiana</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Rekstin</surname><given-names>Andrey</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ilyushina</surname><given-names>Natalia</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lugovtsev</surname><given-names>Vladimir</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Samsonova</surname><given-names>Anastasia</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Go</surname><given-names>Aleksey</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lerner</surname><given-names>Anna</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><xref ref-type="aff" rid="aff006"><sup>6</sup></xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Virology Department, Federal State Budgetary Scientific Institution “Institute of Experimental Medicine”, Saint Petersburg, Russian Federation</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Department of Fundamental Problems of Medicine and Medical Technologies, Saint Petersburg State University, Saint Petersburg, Russian Federation</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Division of Biotechnology Research and Review II, Center for Drug Evaluation and Research, U.S. Food and Drug Administration, Silver Spring, Maryland, United States of America</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Division of Viral Products, Center for Biologics Evaluation and Research, Food and Drug Administration, Silver Spring, Maryland, United States of America</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Clinical and Diagnostic Center, Research Institute of Influenza, Saint Petersburg, Russian Federation</addr-line></aff><aff id="aff006"><label>6</label><addr-line>Medical Research Center, Federal State Budgetary Scientific Institution “Institute of Experimental Medicine”, Saint Petersburg, Russian Federation</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Krammer</surname><given-names>Florian</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Icahn School of Medicine at Mount Sinai, UNITED STATES</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>desheva@mail.ru</email></corresp></author-notes><pub-date pub-type="epub"><day>9</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>e0196771</elocation-id><history><date date-type="received"><day>5</day><month>11</month><year>2017</year></date><date date-type="accepted"><day>19</day><month>4</month><year>2018</year></date></history><permissions><license xlink:href="https://creativecommons.org/publicdomain/zero/1.0/"><license-p>This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/publicdomain/zero/1.0/">Creative Commons CC0</ext-link> public domain dedication.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0196771.pdf"></self-uri><abstract><p>The main objective of the study was to evaluate neuraminidase inhibiting (NI) antibodies against A/H1N1pdm09 influenza viruses in the community as a whole and after infection. We evaluated NI serum antibodies against A/California/07/09(H1N1)pdm and A/South Africa/3626/2013(H1N1)pdm in 134 blood donors of different ages using enzyme-linked lectin assay and in 15 paired sera from convalescents with laboratory confirmed influenza. The neuraminidase (NA) proteins of both A/H1N1pdm09 viruses had minimal genetic divergence, but demonstrated different enzymatic and antigenic properties. 5.2% of individuals had NI antibody titers ≥1:20 against A/South Africa/3626/2013(H1N1)pdm compared to 53% of those who were positive to A/California/07/2009(H1N1)pdm NA. 2% of individuals had detectable NI titers against A/South Africa/3626/13(H1N1)pdm and 47.3% were positive to A/California/07/2009(H1N1)pdm NA among participants negative to hemagglutinin (HA) of A/H1N1pdm09 but positive to seasonal A/H1N1. The lowest NI antibody levels to both A/H1N1pdm09 viruses were detected in individuals born between 1956 and 1968. Our data suggest that NI antibodies against A/South Africa/3626/13 (H1N1)pdm found in the blood donors could have resulted from direct infection with a new antigenic A/H1N1pdm09 variant rather than from cross-reaction as a result of contact with previously circulating seasonal A/H1N1 variants. The immune responses against HA and NA were formed simultaneously right after natural infection with A/H1N1pdm09. NI antibodies correlated with virus-neutralizing antibodies when acquired shortly after influenza infection. A group of middle-aged patients with the lowest level of anti-NA antibodies against A/California/07/2009 (H1N1)pdm was identified, indicating the highest-priority vaccination against A/H1N1pdm09 viruses.</p></abstract><funding-group><funding-statement>The authors received no specific funding for this work.</funding-statement></funding-group><counts><fig-count count="5"></fig-count><table-count count="2"></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 relevant data are within the paper and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper and its Supporting Information files.</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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