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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">N-Linked Glycosylation of the Hemagglutinin Protein Influences Virulence and Antigenicity of the 1918 Pandemic and Seasonal H1N1 Influenza A Viruses</title>
<author><name sortKey="Sun, Xiangjie" sort="Sun, Xiangjie" uniqKey="Sun X" first="Xiangjie" last="Sun">Xiangjie Sun</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Jayaraman, Akila" sort="Jayaraman, Akila" uniqKey="Jayaraman A" first="Akila" last="Jayaraman">Akila Jayaraman</name>
<affiliation><nlm:aff id="aff3"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Maniprasad, Pavithra" sort="Maniprasad, Pavithra" uniqKey="Maniprasad P" first="Pavithra" last="Maniprasad">Pavithra Maniprasad</name>
<affiliation><nlm:aff id="aff3"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Raman, Rahul" sort="Raman, Rahul" uniqKey="Raman R" first="Rahul" last="Raman">Rahul Raman</name>
<affiliation><nlm:aff id="aff3"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Houser, Katherine V" sort="Houser, Katherine V" uniqKey="Houser K" first="Katherine V." last="Houser">Katherine V. Houser</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Pappas, Claudia" sort="Pappas, Claudia" uniqKey="Pappas C" first="Claudia" last="Pappas">Claudia Pappas</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zeng, Hui" sort="Zeng, Hui" uniqKey="Zeng H" first="Hui" last="Zeng">Hui Zeng</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Sasisekharan, Ram" sort="Sasisekharan, Ram" uniqKey="Sasisekharan R" first="Ram" last="Sasisekharan">Ram Sasisekharan</name>
<affiliation><nlm:aff id="aff3"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Katz, Jacqueline M" sort="Katz, Jacqueline M" uniqKey="Katz J" first="Jacqueline M." last="Katz">Jacqueline M. Katz</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Tumpey, Terrence M" sort="Tumpey, Terrence M" uniqKey="Tumpey T" first="Terrence M." last="Tumpey">Terrence M. Tumpey</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">23740978</idno>
<idno type="pmc">3719814</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3719814</idno>
<idno type="RBID">PMC:3719814</idno>
<idno type="doi">10.1128/JVI.00593-13</idno>
<date when="2013">2013</date>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">N-Linked Glycosylation of the Hemagglutinin Protein Influences Virulence and Antigenicity of the 1918 Pandemic and Seasonal H1N1 Influenza A Viruses</title>
<author><name sortKey="Sun, Xiangjie" sort="Sun, Xiangjie" uniqKey="Sun X" first="Xiangjie" last="Sun">Xiangjie Sun</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Jayaraman, Akila" sort="Jayaraman, Akila" uniqKey="Jayaraman A" first="Akila" last="Jayaraman">Akila Jayaraman</name>
<affiliation><nlm:aff id="aff3"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Maniprasad, Pavithra" sort="Maniprasad, Pavithra" uniqKey="Maniprasad P" first="Pavithra" last="Maniprasad">Pavithra Maniprasad</name>
<affiliation><nlm:aff id="aff3"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Raman, Rahul" sort="Raman, Rahul" uniqKey="Raman R" first="Rahul" last="Raman">Rahul Raman</name>
<affiliation><nlm:aff id="aff3"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Houser, Katherine V" sort="Houser, Katherine V" uniqKey="Houser K" first="Katherine V." last="Houser">Katherine V. Houser</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Pappas, Claudia" sort="Pappas, Claudia" uniqKey="Pappas C" first="Claudia" last="Pappas">Claudia Pappas</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zeng, Hui" sort="Zeng, Hui" uniqKey="Zeng H" first="Hui" last="Zeng">Hui Zeng</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Sasisekharan, Ram" sort="Sasisekharan, Ram" uniqKey="Sasisekharan R" first="Ram" last="Sasisekharan">Ram Sasisekharan</name>
<affiliation><nlm:aff id="aff3"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Katz, Jacqueline M" sort="Katz, Jacqueline M" uniqKey="Katz J" first="Jacqueline M." last="Katz">Jacqueline M. Katz</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Tumpey, Terrence M" sort="Tumpey, Terrence M" uniqKey="Tumpey T" first="Terrence M." last="Tumpey">Terrence M. Tumpey</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Journal of Virology</title>
<idno type="ISSN">0022-538X</idno>
<idno type="eISSN">1098-5514</idno>
<imprint><date when="2013">2013</date>
</imprint>
</series>
</biblStruct>
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<front><div type="abstract" xml:lang="en"><p>The hemagglutinin (HA) protein is a major virulence determinant for the 1918 pandemic influenza virus; however, it encodes no known virulence-associated determinants. In comparison to seasonal influenza viruses of lesser virulence, the 1918 H1N1 virus has fewer glycosylation sequons on the HA globular head region. Using site-directed mutagenesis, we found that a 1918 HA recombinant virus, of high virulence, could be significantly attenuated in mice by adding two additional glycosylation sites (asparagine [Asn] 71 and Asn 286) on the side of the HA head. The 1918 HA recombinant virus was further attenuated by introducing two additional glycosylation sites on the top of the HA head at Asn 142 and Asn 172. In a reciprocal experimental approach, deletion of HA glycosylation sites (Asn 142 and Asn 177, but not Asn 71 and Asn 104) from a seasonal influenza H1N1 virus, A/Solomon Islands/2006 (SI/06), led to increased virulence in mice. The addition of glycosylation sites to 1918 HA and removal of glycosylation sites from SI/06 HA imposed constraints on the theoretical structure surrounding the glycan receptor binding sites, which in turn led to distinct glycan receptor binding properties. The modification of glycosylation sites for the 1918 and SI/06 viruses also caused changes in viral antigenicity based on cross-reactive hemagglutinin inhibition antibody titers with antisera from mice infected with wild-type or glycan mutant viruses. These results demonstrate that glycosylation patterns of the 1918 and seasonal H1N1 viruses directly contribute to differences in virulence and are partially responsible for their distinct antigenicity.</p>
</div>
</front>
</TEI>
<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">23740978</article-id>
<article-id pub-id-type="pmc">3719814</article-id>
<article-id pub-id-type="publisher-id">00593-13</article-id>
<article-id pub-id-type="doi">10.1128/JVI.00593-13</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Pathogenesis and Immunity</subject>
</subj-group>
</article-categories>
<title-group><article-title>N-Linked Glycosylation of the Hemagglutinin Protein Influences Virulence and Antigenicity of the 1918 Pandemic and Seasonal H1N1 Influenza A Viruses</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Sun</surname>
<given-names>Xiangjie</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jayaraman</surname>
<given-names>Akila</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Maniprasad</surname>
<given-names>Pavithra</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Raman</surname>
<given-names>Rahul</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Houser</surname>
<given-names>Katherine V.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pappas</surname>
<given-names>Claudia</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zeng</surname>
<given-names>Hui</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sasisekharan</surname>
<given-names>Ram</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Katz</surname>
<given-names>Jacqueline M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Tumpey</surname>
<given-names>Terrence M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<aff id="aff1">Immunology and Pathogenesis Branch, Influenza Division, National Center for Immunology and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA<label>a</label>
</aff>
<aff id="aff2">Graduate Program in Immunology and Molecular Pathogenesis of the Graduate Division of Biological and Biomedical Sciences, Emory University, Atlanta, Georgia, USA<label>b</label>
</aff>
<aff id="aff3">Harvard-MIT Division of Health Sciences and Technology, Singapore-MIT Alliance for Research and Technology, Department of Biological Engineering, Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA<label>c</label>
</aff>
</contrib-group>
<author-notes><corresp id="cor1">Address correspondence to Terrence M. Tumpey, <email>tft9@cdc.gov</email>
.</corresp>
</author-notes>
<pub-date pub-type="ppub"><month>8</month>
<year>2013</year>
</pub-date>
<volume>87</volume>
<issue>15</issue>
<fpage>8756</fpage>
<lpage>8766</lpage>
<history><date date-type="received"><day>4</day>
<month>3</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>26</day>
<month>5</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2013, American Society for Microbiology. All Rights Reserved.</copyright-statement>
<copyright-year>2013</copyright-year>
<copyright-holder>American Society for Microbiology</copyright-holder>
</permissions>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="zjv01513008756.pdf"></self-uri>
<abstract><p>The hemagglutinin (HA) protein is a major virulence determinant for the 1918 pandemic influenza virus; however, it encodes no known virulence-associated determinants. In comparison to seasonal influenza viruses of lesser virulence, the 1918 H1N1 virus has fewer glycosylation sequons on the HA globular head region. Using site-directed mutagenesis, we found that a 1918 HA recombinant virus, of high virulence, could be significantly attenuated in mice by adding two additional glycosylation sites (asparagine [Asn] 71 and Asn 286) on the side of the HA head. The 1918 HA recombinant virus was further attenuated by introducing two additional glycosylation sites on the top of the HA head at Asn 142 and Asn 172. In a reciprocal experimental approach, deletion of HA glycosylation sites (Asn 142 and Asn 177, but not Asn 71 and Asn 104) from a seasonal influenza H1N1 virus, A/Solomon Islands/2006 (SI/06), led to increased virulence in mice. The addition of glycosylation sites to 1918 HA and removal of glycosylation sites from SI/06 HA imposed constraints on the theoretical structure surrounding the glycan receptor binding sites, which in turn led to distinct glycan receptor binding properties. The modification of glycosylation sites for the 1918 and SI/06 viruses also caused changes in viral antigenicity based on cross-reactive hemagglutinin inhibition antibody titers with antisera from mice infected with wild-type or glycan mutant viruses. These results demonstrate that glycosylation patterns of the 1918 and seasonal H1N1 viruses directly contribute to differences in virulence and are partially responsible for their distinct antigenicity.</p>
</abstract>
</article-meta>
</front>
</pmc>
</record>
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