Defining the antibody cross-reactome against the influenza virus surface glycoproteins
Identifieur interne : 000254 ( Pmc/Checkpoint ); précédent : 000253; suivant : 000255Defining the antibody cross-reactome against the influenza virus surface glycoproteins
Auteurs : Raffael Nachbagauer [États-Unis] ; Angela Choi [États-Unis] ; Ariana Hirsh [États-Unis] ; Irina Margine [États-Unis] ; Sayaka Iida [Japon] ; Aldo Barrera [Chili] ; Marcela Ferres [Chili] ; Randy A. Albrecht [États-Unis] ; Adolfo García-Sastre [États-Unis] ; Nicole M. Bouvier [États-Unis] ; Kimihito Ito [Japon] ; Rafael A. Medina [États-Unis, Chili] ; Peter Palese [États-Unis] ; Florian Krammer [États-Unis]Source :
- Nature immunology [ 1529-2908 ] ; 2017.
Abstract
Influenza virus infections induce antibodies against the viral surface glycoproteins hemagglutinin and neuraminidase, and these responses can be broadly protective. To test the breadth and magnitude of antibody responses, mice, guinea pigs and ferrets were sequentially infected with divergent H1N1 or H3N2 viruses. Antibody responses were measured by ELISA against an extensive panel of recombinant glycoproteins representing the viral diversity in nature. Guinea pigs developed high titers of broadly cross-reactive antibodies; mice and ferrets exhibited narrower humoral responses. Then, we compared antibody responses after H1N1 or H3N2 infections in humans and found markedly broad responses and cogent evidence for original antigenic sin. This work will inform universal influenza vaccine design and can guide pandemic preparedness efforts against emerging influenza viruses.
Url:
DOI: 10.1038/ni.3684
PubMed: 28192418
PubMed Central: 5360498
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Santiago, Chile</nlm:aff><country xml:lang="fr">Chili</country><wicri:regionArea>Millennium Institute on Immunology and Immunotherapy, Pontificia Universidad Católica de Chile, Santiago</wicri:regionArea><wicri:noRegion>Santiago</wicri:noRegion></affiliation></author><author><name sortKey="Palese, Peter" sort="Palese, Peter" uniqKey="Palese P" first="Peter" last="Palese">Peter Palese</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A6">Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country 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USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Choi, Angela" sort="Choi, Angela" uniqKey="Choi A" first="Angela" last="Choi">Angela Choi</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A2">Graduate School of Biological Sciences, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Graduate School of Biological Sciences, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Hirsh, Ariana" sort="Hirsh, Ariana" uniqKey="Hirsh A" first="Ariana" last="Hirsh">Ariana Hirsh</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Margine, Irina" sort="Margine, Irina" uniqKey="Margine I" first="Irina" last="Margine">Irina Margine</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Iida, Sayaka" sort="Iida, Sayaka" uniqKey="Iida S" first="Sayaka" last="Iida">Sayaka Iida</name><affiliation wicri:level="1"><nlm:aff id="A3">Division of Bioinformatics, Hokkaido University Research Center for Zoonosis Control, Kitaku, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Division of Bioinformatics, Hokkaido University Research Center for Zoonosis Control, Kitaku</wicri:regionArea><wicri:noRegion>Kitaku</wicri:noRegion></affiliation></author><author><name sortKey="Barrera, Aldo" sort="Barrera, Aldo" uniqKey="Barrera A" first="Aldo" last="Barrera">Aldo Barrera</name><affiliation wicri:level="1"><nlm:aff id="A4">Departamento de Infectología e Inmunología Pediátrica, School of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile</nlm:aff><country xml:lang="fr">Chili</country><wicri:regionArea>Departamento de Infectología e Inmunología Pediátrica, School of Medicine, Pontificia Universidad Católica de Chile, Santiago</wicri:regionArea><wicri:noRegion>Santiago</wicri:noRegion></affiliation></author><author><name sortKey="Ferres, Marcela" sort="Ferres, Marcela" uniqKey="Ferres M" first="Marcela" last="Ferres">Marcela Ferres</name><affiliation wicri:level="1"><nlm:aff id="A4">Departamento de Infectología e Inmunología Pediátrica, School of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile</nlm:aff><country xml:lang="fr">Chili</country><wicri:regionArea>Departamento de Infectología e Inmunología Pediátrica, School of Medicine, Pontificia Universidad Católica de Chile, Santiago</wicri:regionArea><wicri:noRegion>Santiago</wicri:noRegion></affiliation></author><author><name sortKey="Albrecht, Randy A" sort="Albrecht, Randy A" uniqKey="Albrecht R" first="Randy A." last="Albrecht">Randy A. Albrecht</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A5">Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="García-Sastre">Adolfo García-Sastre</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A5">Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A6">Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Bouvier, Nicole M" sort="Bouvier, Nicole M" uniqKey="Bouvier N" first="Nicole M." last="Bouvier">Nicole M. Bouvier</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A6">Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Ito, Kimihito" sort="Ito, Kimihito" uniqKey="Ito K" first="Kimihito" last="Ito">Kimihito Ito</name><affiliation wicri:level="1"><nlm:aff id="A3">Division of Bioinformatics, Hokkaido University Research Center for Zoonosis Control, Kitaku, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Division of Bioinformatics, Hokkaido University Research Center for Zoonosis Control, Kitaku</wicri:regionArea><wicri:noRegion>Kitaku</wicri:noRegion></affiliation></author><author><name sortKey="Medina, Rafael A" sort="Medina, Rafael A" uniqKey="Medina R" first="Rafael A." last="Medina">Rafael A. Medina</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="A4">Departamento de Infectología e Inmunología Pediátrica, School of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile</nlm:aff><country xml:lang="fr">Chili</country><wicri:regionArea>Departamento de Infectología e Inmunología Pediátrica, School of Medicine, Pontificia Universidad Católica de Chile, Santiago</wicri:regionArea><wicri:noRegion>Santiago</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A7">Millennium Institute on Immunology and Immunotherapy, Pontificia Universidad Católica de Chile, Santiago, Chile</nlm:aff><country xml:lang="fr">Chili</country><wicri:regionArea>Millennium Institute on Immunology and Immunotherapy, Pontificia Universidad Católica de Chile, Santiago</wicri:regionArea><wicri:noRegion>Santiago</wicri:noRegion></affiliation></author><author><name sortKey="Palese, Peter" sort="Palese, Peter" uniqKey="Palese P" first="Peter" last="Palese">Peter Palese</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="A6">Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Krammer, Florian" sort="Krammer, Florian" uniqKey="Krammer F" first="Florian" last="Krammer">Florian Krammer</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author></analytic><series><title level="j">Nature immunology</title><idno type="ISSN">1529-2908</idno><idno type="eISSN">1529-2916</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Summary</title><p id="P2">Influenza virus infections induce antibodies against the viral surface glycoproteins hemagglutinin and neuraminidase, and these responses can be broadly protective. To test the breadth and magnitude of antibody responses, mice, guinea pigs and ferrets were sequentially infected with divergent H1N1 or H3N2 viruses. Antibody responses were measured by ELISA against an extensive panel of recombinant glycoproteins representing the viral diversity in nature. Guinea pigs developed high titers of broadly cross-reactive antibodies; mice and ferrets exhibited narrower humoral responses. Then, we compared antibody responses after H1N1 or H3N2 infections in humans and found markedly broad responses and cogent evidence for original antigenic sin. This work will inform universal influenza vaccine design and can guide pandemic preparedness efforts against emerging influenza viruses.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Jayasundara, K" uniqKey="Jayasundara K">K Jayasundara</name></author><author><name sortKey="Soobiah, C" uniqKey="Soobiah C">C Soobiah</name></author><author><name sortKey="Thommes, E" uniqKey="Thommes E">E Thommes</name></author><author><name sortKey="Tricco, Ac" uniqKey="Tricco A">AC Tricco</name></author><author><name sortKey="Chit, A" uniqKey="Chit A">A Chit</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Krammer, F" uniqKey="Krammer F">F Krammer</name></author><author><name sortKey="Palese, P" uniqKey="Palese P">P Palese</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Horimoto, T" uniqKey="Horimoto T">T Horimoto</name></author><author><name sortKey="Kawaoka, Y" 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article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<pmc-dir>properties manuscript</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-journal-id">100941354</journal-id><journal-id journal-id-type="pubmed-jr-id">21750</journal-id><journal-id journal-id-type="nlm-ta">Nat Immunol</journal-id><journal-id journal-id-type="iso-abbrev">Nat. Immunol.</journal-id><journal-title-group><journal-title>Nature immunology</journal-title></journal-title-group><issn pub-type="ppub">1529-2908</issn><issn pub-type="epub">1529-2916</issn></journal-meta><article-meta><article-id pub-id-type="pmid">28192418</article-id><article-id pub-id-type="pmc">5360498</article-id><article-id pub-id-type="doi">10.1038/ni.3684</article-id><article-id pub-id-type="manuscript">NIHMS841825</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Defining the antibody cross-reactome against the influenza virus surface glycoproteins</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Nachbagauer</surname><given-names>Raffael</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><name><surname>Choi</surname><given-names>Angela</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref></contrib><contrib contrib-type="author"><name><surname>Hirsh</surname><given-names>Ariana</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><name><surname>Margine</surname><given-names>Irina</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><name><surname>Iida</surname><given-names>Sayaka</given-names></name><xref ref-type="aff" rid="A3">3</xref></contrib><contrib contrib-type="author"><name><surname>Barrera</surname><given-names>Aldo</given-names></name><xref ref-type="aff" rid="A4">4</xref></contrib><contrib contrib-type="author"><name><surname>Ferres</surname><given-names>Marcela</given-names></name><xref ref-type="aff" rid="A4">4</xref></contrib><contrib contrib-type="author"><name><surname>Albrecht</surname><given-names>Randy A.</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A5">5</xref></contrib><contrib contrib-type="author"><name><surname>García-Sastre</surname><given-names>Adolfo</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A5">5</xref><xref ref-type="aff" rid="A6">6</xref></contrib><contrib contrib-type="author"><name><surname>Bouvier</surname><given-names>Nicole M.</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A6">6</xref></contrib><contrib contrib-type="author"><name><surname>Ito</surname><given-names>Kimihito</given-names></name><xref ref-type="aff" rid="A3">3</xref></contrib><contrib contrib-type="author"><name><surname>Medina</surname><given-names>Rafael A.</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A4">4</xref><xref ref-type="aff" rid="A7">7</xref></contrib><contrib contrib-type="author"><name><surname>Palese</surname><given-names>Peter</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A6">6</xref></contrib><contrib contrib-type="author"><name><surname>Krammer</surname><given-names>Florian</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib></contrib-group><aff id="A1"><label>1</label>Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA</aff><aff id="A2"><label>2</label>Graduate School of Biological Sciences, Icahn School of Medicine at Mount Sinai, New York, New York, USA</aff><aff id="A3"><label>3</label>Division of Bioinformatics, Hokkaido University Research Center for Zoonosis Control, Kitaku, Japan</aff><aff id="A4"><label>4</label>Departamento de Infectología e Inmunología Pediátrica, School of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile</aff><aff id="A5"><label>5</label>Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, New York, USA</aff><aff id="A6"><label>6</label>Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA</aff><aff id="A7"><label>7</label>Millennium Institute on Immunology and Immunotherapy, Pontificia Universidad Católica de Chile, Santiago, Chile</aff><author-notes><corresp id="FN1">Correspondence should be addressed to F.K. (<email>florian.krammer@mssm.edu</email>)</corresp></author-notes><pub-date pub-type="nihms-submitted"><day>12</day><month>1</month><year>2017</year></pub-date><pub-date pub-type="epub"><day>13</day><month>2</month><year>2017</year></pub-date><pub-date pub-type="ppub"><month>4</month><year>2017</year></pub-date><pub-date pub-type="pmc-release"><day>13</day><month>8</month><year>2017</year></pub-date><volume>18</volume><issue>4</issue><fpage>464</fpage><lpage>473</lpage><pmc-comment>elocation-id from pubmed: 10.1038/ni.3684</pmc-comment>
<permissions><license><license-p>Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:
<uri xlink:type="simple" xlink:href="http://www.nature.com/authors/editorial_policies/license.html#terms">http://www.nature.com/authors/editorial_policies/license.html#terms</uri></license-p></license></permissions><abstract><title>Summary</title><p id="P2">Influenza virus infections induce antibodies against the viral surface glycoproteins hemagglutinin and neuraminidase, and these responses can be broadly protective. To test the breadth and magnitude of antibody responses, mice, guinea pigs and ferrets were sequentially infected with divergent H1N1 or H3N2 viruses. Antibody responses were measured by ELISA against an extensive panel of recombinant glycoproteins representing the viral diversity in nature. Guinea pigs developed high titers of broadly cross-reactive antibodies; mice and ferrets exhibited narrower humoral responses. Then, we compared antibody responses after H1N1 or H3N2 infections in humans and found markedly broad responses and cogent evidence for original antigenic sin. This work will inform universal influenza vaccine design and can guide pandemic preparedness efforts against emerging influenza viruses.</p></abstract></article-meta></front><floats-group><fig id="F1" orientation="portrait" position="float"><label>Figure 1</label><caption><title>Cross-reactive HA antibody responses in the mouse model measured by ELISA</title><p>Serum IgG antibodies against all subtypes of HA were measured by ELISA. Pooled sera of 10 mice per group were measured in technical duplicates and the geometric mean value was used for graphical representation. A heat map overlay on top of a phylogenetic tree was used to illustrate the antibody titers induced by repeated influenza virus infection. The scale bar represents 4% amino acid difference. <bold>A)</bold> HA titers after a single H1N1 (NC99) infection in mice. <bold>B)</bold> HA titers after two consecutive H1N1 (NC99+NL09) infections in mice. <bold>C)</bold> HA titers after a single H3N2 (Phil82) infection in mice. <bold>D)</bold> HA titers after two consecutive H3N2 (Phil82+Vic11) infections in mice.</p></caption><graphic xlink:href="nihms841825f1"></graphic></fig><fig id="F2" orientation="portrait" position="float"><label>Figure 2</label><caption><title>Cross-reactive NA antibody responses in the mouse model measured by ELISA</title><p>Serum IgG antibodies against NA were measured by ELISA. Pooled sera of 10 mice per group were measured in technical duplicates and the geometric mean value was used for graphical representation. A heat map overlay on top of a phylogenetic tree was used to illustrate the antibody titers induced by repeated influenza virus infection. The scale bar represents 8% amino acid difference. <bold>A)</bold> NA titers after a single H1N1 (NC99) infection in mice. <bold>B)</bold> NA titers after two consecutive H1N1 (NC99+NL09) infections in mice. <bold>C)</bold> NA titers after a single H3N2 (Phil82) infection in mice. <bold>D)</bold> NA titers after two consecutive H3N2 (Phil82+Vic11) infections in mice.</p></caption><graphic xlink:href="nihms841825f2"></graphic></fig><fig id="F3" orientation="portrait" position="float"><label>Figure 3</label><caption><title>Cross-reactive antibody titers post infection negatively correlate with phylogenetic distance</title><p>To illustrate a correlation of antibody titers with phylogenetic distance, antibody titers measured by ELISA after sequential influenza virus infection were plotted on the <italic>y</italic>-axis and the percent amino acid difference to the HA of the strain used for the second infection was plotted on the <italic>x</italic>-axis. Each point represents the geometric mean titer measured against a single HA (dark blue dot for H1 HAs, light blue dot for other group 1 HAs, dark red triangle for H3 HAs, light red triangle for other group 2 HAs). A non-linear fit (plateau followed by one phase decay) was performed to illustrate the differences in the breadth of the antibody response in all animals. Points for HAs with titers lower than 10<sup>3</sup> are plotted at 10<sup>3</sup>. The geometric mean titer against all non-H1 group 1 HAs is plotted as a light blue line. The geometric mean titer against all non-H3 group 2 HAs is plotted as a light red line. <bold>A)</bold> Mouse group 1 HA titers after two consecutive H1N1 (NC99+NL09) infections. ELISAs were performed on pooled sera of 10 mice and geometric mean titers of technical duplicates are shown. <bold>B)</bold> Guinea pig group 1 HA titers after two consecutive H1N1 (NC99+NL09) infections. ELISAs were performed on individual sera of 3 guinea pigs and geometric mean titers are shown. <bold>C)</bold> Ferret group 1 HA titers after two consecutive H1N1 (NC99+NL09) infections. ELISAs were performed on individual sera of 2 ferrets and geometric mean titers are shown. <bold>D)</bold> Mouse group 2 HA titers after two consecutive H3N2 (Phil82+Vic11) infections. ELISAs were performed on pooled sera of 10 mice and geometric mean titers of technical duplicates are shown. <bold>E)</bold> Guinea pig group 2 HA titers after two consecutive H3N2 (Phil82+Vic11) infections. ELISAs were performed on individual sera of 2 guinea pigs and geometric mean titers are shown. <bold>F</bold> Ferret group 2 HA titers after two consecutive H3N2 (Phil82+Vic11) infections. ELISAs were performed on individual sera of 2 ferrets and geometric mean titers are shown.</p></caption><graphic xlink:href="nihms841825f3"></graphic></fig><fig id="F4" orientation="portrait" position="float"><label>Figure 4</label><caption><title>Human antibody responses post pH1N1 infection are broader than post H3N2 infection</title><p><bold>A)</bold> Geometric mean fold-induction of individual antibody responses (n=9) post pH1N1 infection was plotted as a heat-map on a phylogenetic tree of HA. The scale bar represents 4% amino acid difference. <bold>B)</bold> The geometric mean fold-induction and 95% confidence intervals post pH1N1 infection of 9 individuals was plotted in a bar graph and sorted from highest to lowest induction. Group 1 HAs are shown as blue bars, group 2 HAs are shown as red bars and influenza B HA is shown in green. <bold>C)</bold> Three dimensional surfaces of the pre- and post-pH1N1 infection antibody titers were generated by plotting the relative distances of HAs to each other based on amino acid differences. Both <italic>x</italic>-and <italic>y</italic>-axes show amino acid differences and geometric mean titers (n=9) are plotted on the <italic>z</italic>-axis. The post-infection surfaces were plotted in color (blue for group 1 HAs, red for group 2 HAs) and the corresponding pre-infection surfaces are plotted in gray. <bold>D)</bold> Geometric mean fold-induction of individual antibody responses (n=10) post H3N2 infection was plotted as a heat-map on a phylogenetic tree of HA. The scale bar represents 8% amino acid difference. <bold>E)</bold> The geometric mean fold-induction and 95% confidence intervals post H3N2 infection of 10 individuals was plotted in a bar graph and sorted from highest to lowest induction. Group 1 HAs are shown as blue bars, group 2 HAs are shown as red bars and influenza B HA is shown in green. <bold>F)</bold> Three dimensional surfaces of the pre- and post-H3N2 infection antibody titers were generated by plotting the relative distances of HAs to each other based on amino acid differences. Both <italic>x</italic>-and <italic>y</italic>-axes show amino acid differences and geometric mean titers (n=10) are plotted on the <italic>z</italic>-axis. The post-infection surfaces were plotted in color (blue for group 1 HAs, red for group 2 HAs) and the corresponding pre-infection surfaces are plotted in gray.</p></caption><graphic xlink:href="nihms841825f4"></graphic></fig><fig id="F5" orientation="portrait" position="float"><label>Figure 5</label><caption><title>Titers in the general human population show distinct age related patterns</title><p><bold>A)</bold> Schematic of selection of age groups that were tested. To investigate the effect of pre-exposure to different viruses, three distinct age groups were selected depending on the influenza viruses that most likely circulated during the childhood of the individuals. The oldest age group (49–64 year olds, ‘experienced’) was born when either a drifted version of the 1918 H1N1 virus or the H2N2 pandemic virus circulated. All individuals in this group should therefore have had exposure to H2N2 viruses. The slightly younger age group (33–44 year olds, ‘middle-aged’) was born after H2N2 went extinct and was replaced by the group 2 H3N2 virus and has therefore not been previously exposed to H2N2. 18–20 year olds (‘young’ cohort) were used as a young control group with only a limited exposure to group 1 and group 2 influenza A virus strains. <bold>B–D)</bold> To illustrate the differences of antibody profiles in the different age groups, three dimensional antigenic landscapes were plotted. All HAs are shown in their relative difference to each other based on amino acid sequences on the <italic>x</italic>- and <italic>y</italic>-axes. The geometric mean titers were plotted on the <italic>z</italic>-axis. <bold>B)</bold> Geometric mean titers of 18–20 year old individuals (n=30). <bold>C)</bold> Geometric mean titers of 33–44 year old individuals (n=30). <bold>D)</bold> Geometric mean titers of 49–64 year old individuals (n=30).</p></caption><graphic xlink:href="nihms841825f5"></graphic></fig><fig id="F6" orientation="portrait" position="float"><label>Figure 6</label><caption><title><italic>In vitro</italic> and <italic>in vivo</italic> protective effect of sera from the general human population</title><p>To test if antibody titers measured by ELISA also translate to measurable neutralizing responses <italic>in vitro</italic> and protective responses <italic>in vivo</italic>, re-assortant viruses that contain the same PR8 backbone and an irrelevant neuraminidase were generated for H1, H3, H4, H4, H7 and H9. <bold>A)</bold> Individual microneutralization titers against group 1 viruses (H1, H5, H9) are shown for sera from 18–20 year olds (blue dots, n=30), 33–44 year olds (red squares, n=30) and 49–64 year olds (teal triangles, n=30). A bar that represents the geometric mean titer is shown for each group. The gray line indicates the limit of detection for the assay. For each virus, groups were compared with an ordinary one-way ANOVA, followed by a Tukey’s multiple comparisons test. Statistical significance is indicated as follows: ** = p ≤ 0.01, *** = p ≤ 0.001, **** = p ≤ 0.0001. <bold>B)</bold> Proportion of individuals with a neutralization titer of 1:40 or higher against group 1 viruses (H1, H5, H9) for each age group (n=30 per group). <bold>C)</bold> Individual microneutralization titers against group 2 viruses (H3, H4, H7) are shown for sera from 18–20 year olds (blue dots, n=30), 33–44 year olds (red squares, n=30) and 49–64 year olds (teal triangles, n=30). A bar that represents the geometric mean titer is shown for each group. The gray line indicates the limit of detection for the assay. For each virus, groups were compared with an ordinary one-way ANOVA, followed by a Tukey’s multiple comparisons test. Statistical significance is indicated as follows: ** = p ≤ 0.01, *** = p ≤ 0.001, **** = p ≤ 0.0001. <bold>D)</bold> Proportion of individuals with a neutralization titer of 1:40 or higher against group 2 viruses (H3, H4, H7) for each age group (n=30 per group) <bold>E–F)</bold> Serum transfer studies in mice (n=5 per group per virus) were performed with pooled serum from each age group (n=30 per group) with subsequent challenge with viruses containing H3, H4 or H7 HAs. Mice that received immunoglobulin depleted serum served as a control. To measure the level of protection, lungs were extracted on day 3 and day 6 post-challenge and virus titers measured by plaque assay. A bar that represents the geometric mean titer is shown for each group. The gray line indicates the limit of detection for the assay. For each virus, groups were compared to the immunoglobulin depleted group with an ordinary one-way ANOVA, followed by a Dunnet’s multiple comparisons test. Statistical significance is indicated as follows: ** = p ≤ 0.01, *** = p ≤ 0.001, **** = p ≤ 0.0001.</p></caption><graphic xlink:href="nihms841825f6"></graphic></fig></floats-group></pmc><affiliations><list><country><li>Chili</li><li>Japon</li><li>États-Unis</li></country><region><li>État de New York</li></region></list><tree><country name="États-Unis"><region name="État de New York"><name sortKey="Nachbagauer, Raffael" sort="Nachbagauer, Raffael" uniqKey="Nachbagauer R" first="Raffael" last="Nachbagauer">Raffael Nachbagauer</name></region><name sortKey="Albrecht, Randy A" sort="Albrecht, Randy A" uniqKey="Albrecht R" first="Randy A." last="Albrecht">Randy A. Albrecht</name><name sortKey="Albrecht, Randy A" sort="Albrecht, Randy A" uniqKey="Albrecht R" first="Randy A." last="Albrecht">Randy A. Albrecht</name><name sortKey="Bouvier, Nicole M" sort="Bouvier, Nicole M" uniqKey="Bouvier N" first="Nicole M." last="Bouvier">Nicole M. Bouvier</name><name sortKey="Bouvier, Nicole M" sort="Bouvier, Nicole M" uniqKey="Bouvier N" first="Nicole M." last="Bouvier">Nicole M. Bouvier</name><name sortKey="Choi, Angela" sort="Choi, Angela" uniqKey="Choi A" first="Angela" last="Choi">Angela Choi</name><name sortKey="Choi, Angela" sort="Choi, Angela" uniqKey="Choi A" first="Angela" last="Choi">Angela Choi</name><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="García-Sastre">Adolfo García-Sastre</name><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="García-Sastre">Adolfo García-Sastre</name><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="García-Sastre">Adolfo García-Sastre</name><name sortKey="Hirsh, Ariana" sort="Hirsh, Ariana" uniqKey="Hirsh A" first="Ariana" last="Hirsh">Ariana Hirsh</name><name sortKey="Krammer, Florian" sort="Krammer, Florian" uniqKey="Krammer F" first="Florian" last="Krammer">Florian Krammer</name><name sortKey="Margine, Irina" sort="Margine, Irina" uniqKey="Margine I" first="Irina" last="Margine">Irina Margine</name><name sortKey="Medina, Rafael A" sort="Medina, Rafael A" uniqKey="Medina R" first="Rafael A." last="Medina">Rafael A. Medina</name><name sortKey="Palese, Peter" sort="Palese, Peter" uniqKey="Palese P" first="Peter" last="Palese">Peter Palese</name><name sortKey="Palese, Peter" sort="Palese, Peter" uniqKey="Palese P" first="Peter" last="Palese">Peter Palese</name></country><country name="Japon"><noRegion><name sortKey="Iida, Sayaka" sort="Iida, Sayaka" uniqKey="Iida S" first="Sayaka" last="Iida">Sayaka Iida</name></noRegion><name sortKey="Ito, Kimihito" sort="Ito, Kimihito" uniqKey="Ito K" first="Kimihito" last="Ito">Kimihito Ito</name></country><country name="Chili"><noRegion><name sortKey="Barrera, Aldo" sort="Barrera, Aldo" uniqKey="Barrera A" first="Aldo" last="Barrera">Aldo Barrera</name></noRegion><name sortKey="Ferres, Marcela" sort="Ferres, Marcela" uniqKey="Ferres M" first="Marcela" last="Ferres">Marcela Ferres</name><name sortKey="Medina, Rafael A" sort="Medina, Rafael A" uniqKey="Medina R" first="Rafael A." last="Medina">Rafael A. Medina</name><name sortKey="Medina, Rafael A" sort="Medina, Rafael A" uniqKey="Medina R" first="Rafael A." last="Medina">Rafael A. Medina</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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