Shotgun glycomics of pig lung identifies natural endogenous receptors for influenza viruses
Identifieur interne : 000760 ( Pmc/Corpus ); précédent : 000759; suivant : 000761Shotgun glycomics of pig lung identifies natural endogenous receptors for influenza viruses
Auteurs : Lauren Byrd-Leotis ; Renpeng Liu ; Konrad C. Bradley ; Yi Lasanajak ; Sandra F. Cummings ; Xuezheng Song ; Jamie Heimburg-Molinaro ; Summer E. Galloway ; Marie R. Culhane ; David F. Smith ; David A. Steinhauer ; Richard D. CummingsSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2014.
Abstract
Studies using novel “shotgun glycan microarray” technology identify, for the first time to our knowledge, the endogenous receptors for influenza viruses from a natural host, the pig. Libraries of total N-glycans from pig lung were probed for binding properties using a panel of influenza viruses isolated from humans, birds, and swine. Natural glycan receptors were identified for all viruses examined, and although some displayed the rather broad α2,3 or α2,6 sialic acid linkage specificity conventionally associated with avian or human viruses, other strains were highly specific, revealing a complexity that has not been demonstrated previously. Because pigs are often implicated as intermediate hosts for pandemic viruses, these results and the approaches described will transform our understanding of influenza host range, transmission, and pathogenicity.
Url:
DOI: 10.1073/pnas.1323162111
PubMed: 24843157
PubMed Central: 4050609
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Cummings</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Song, Xuezheng" sort="Song, Xuezheng" uniqKey="Song X" first="Xuezheng" last="Song">Xuezheng Song</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Heimburg Molinaro, Jamie" sort="Heimburg Molinaro, Jamie" uniqKey="Heimburg Molinaro J" first="Jamie" last="Heimburg-Molinaro">Jamie Heimburg-Molinaro</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Galloway, Summer E" sort="Galloway, Summer E" uniqKey="Galloway S" first="Summer E." last="Galloway">Summer E. Galloway</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Culhane, Marie R" sort="Culhane, Marie R" uniqKey="Culhane M" first="Marie R." last="Culhane">Marie R. Culhane</name><affiliation><nlm:aff id="aff4">Minnesota Veterinary Diagnostic Laboratory,<institution>University of Minnesota</institution>, St. Paul,<addr-line>MN</addr-line> 55108</nlm:aff></affiliation></author><author><name sortKey="Smith, David F" sort="Smith, David F" uniqKey="Smith D" first="David F." last="Smith">David F. Smith</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Steinhauer, David A" sort="Steinhauer, David A" uniqKey="Steinhauer D" first="David A." last="Steinhauer">David A. Steinhauer</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Cummings, Richard D" sort="Cummings, Richard D" uniqKey="Cummings R" first="Richard D." last="Cummings">Richard D. Cummings</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24843157</idno><idno type="pmc">4050609</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4050609</idno><idno type="RBID">PMC:4050609</idno><idno type="doi">10.1073/pnas.1323162111</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000760</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000760</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Shotgun glycomics of pig lung identifies natural endogenous receptors for influenza viruses</title><author><name sortKey="Byrd Leotis, Lauren" sort="Byrd Leotis, Lauren" uniqKey="Byrd Leotis L" first="Lauren" last="Byrd-Leotis">Lauren Byrd-Leotis</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Liu, Renpeng" sort="Liu, Renpeng" uniqKey="Liu R" first="Renpeng" last="Liu">Renpeng Liu</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Bradley, Konrad C" sort="Bradley, Konrad C" uniqKey="Bradley K" first="Konrad C." last="Bradley">Konrad C. Bradley</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Lasanajak, Yi" sort="Lasanajak, Yi" uniqKey="Lasanajak Y" first="Yi" last="Lasanajak">Yi Lasanajak</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Cummings, Sandra F" sort="Cummings, Sandra F" uniqKey="Cummings S" first="Sandra F." last="Cummings">Sandra F. Cummings</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Song, Xuezheng" sort="Song, Xuezheng" uniqKey="Song X" first="Xuezheng" last="Song">Xuezheng Song</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Heimburg Molinaro, Jamie" sort="Heimburg Molinaro, Jamie" uniqKey="Heimburg Molinaro J" first="Jamie" last="Heimburg-Molinaro">Jamie Heimburg-Molinaro</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Galloway, Summer E" sort="Galloway, Summer E" uniqKey="Galloway S" first="Summer E." last="Galloway">Summer E. Galloway</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Culhane, Marie R" sort="Culhane, Marie R" uniqKey="Culhane M" first="Marie R." last="Culhane">Marie R. Culhane</name><affiliation><nlm:aff id="aff4">Minnesota Veterinary Diagnostic Laboratory,<institution>University of Minnesota</institution>, St. Paul,<addr-line>MN</addr-line> 55108</nlm:aff></affiliation></author><author><name sortKey="Smith, David F" sort="Smith, David F" uniqKey="Smith D" first="David F." last="Smith">David F. Smith</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author><author><name sortKey="Steinhauer, David A" sort="Steinhauer, David A" uniqKey="Steinhauer D" first="David A." last="Steinhauer">David A. Steinhauer</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Cummings, Richard D" sort="Cummings, Richard D" uniqKey="Cummings R" first="Richard D." last="Cummings">Richard D. Cummings</name><affiliation><nlm:aff wicri:cut=" and" id="aff2">Biochemistry</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff3">The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322</nlm:aff></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Studies using novel “shotgun glycan microarray” technology identify, for the first time to our knowledge, the endogenous receptors for influenza viruses from a natural host, the pig. Libraries of total N-glycans from pig lung were probed for binding properties using a panel of influenza viruses isolated from humans, birds, and swine. Natural glycan receptors were identified for all viruses examined, and although some displayed the rather broad α2,3 or α2,6 sialic acid linkage specificity conventionally associated with avian or human viruses, other strains were highly specific, revealing a complexity that has not been demonstrated previously. Because pigs are often implicated as intermediate hosts for pandemic viruses, these results and the approaches described will transform our understanding of influenza host range, transmission, and pathogenicity.</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">Proc Natl Acad Sci U S A</journal-id><journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id><journal-id journal-id-type="hwp">pnas</journal-id><journal-id journal-id-type="pmc">pnas</journal-id><journal-id journal-id-type="publisher-id">PNAS</journal-id><journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title></journal-title-group><issn pub-type="ppub">0027-8424</issn><issn pub-type="epub">1091-6490</issn><publisher><publisher-name>National Academy of Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24843157</article-id><article-id pub-id-type="pmc">4050609</article-id><article-id pub-id-type="publisher-id">201323162</article-id><article-id pub-id-type="doi">10.1073/pnas.1323162111</article-id><article-categories><subj-group subj-group-type="heading"><subject>PNAS Plus</subject></subj-group><subj-group subj-group-type="heading"><subject>Biological Sciences</subject><subj-group><subject>Biochemistry</subject></subj-group></subj-group><series-title>PNAS Plus</series-title></article-categories><title-group><article-title>Shotgun glycomics of pig lung identifies natural endogenous receptors for influenza viruses</article-title><alt-title alt-title-type="short">Influenza binding to pig lung shotgun glycan array</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Byrd-Leotis</surname><given-names>Lauren</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Liu</surname><given-names>Renpeng</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bradley</surname><given-names>Konrad C.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lasanajak</surname><given-names>Yi</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Cummings</surname><given-names>Sandra F.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Song</surname><given-names>Xuezheng</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Heimburg-Molinaro</surname><given-names>Jamie</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Galloway</surname><given-names>Summer E.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Culhane</surname><given-names>Marie R.</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><contrib contrib-type="author"><name><surname>Smith</surname><given-names>David F.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Steinhauer</surname><given-names>David A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="corresp" rid="cor1"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Cummings</surname><given-names>Richard D.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref><xref ref-type="corresp" rid="cor1"><sup>4</sup></xref></contrib><aff id="aff1">Departments of<sup>a</sup>Microbiology and Immunology and</aff><aff id="aff2"><sup>b</sup>Biochemistry and</aff><aff id="aff3"><sup>c</sup>The Glycomics Center,<institution>Emory University School of Medicine</institution>, Atlanta,<addr-line>GA</addr-line> 30322; and</aff><aff id="aff4"><sup>d</sup>Minnesota Veterinary Diagnostic Laboratory,<institution>University of Minnesota</institution>, St. Paul,<addr-line>MN</addr-line> 55108</aff></contrib-group><author-notes><corresp id="cor1"><sup>4</sup>To whom correspondence may be addressed. E-mail: <email>dsteinh@emory.edu</email> or <email>rdcummi@emory.edu</email>.</corresp><fn fn-type="edited-by"><p>Edited by Peter Palese, Icahn School of Medicine at Mount Sinai, New York, NY, and approved April 22, 2014 (received for review December 19, 2013)</p></fn><fn fn-type="con"><p>Author contributions: L.B.-L., R.L., D.F.S., D.A.S., and R.D.C. designed research; L.B.-L., R.L., K.C.B., Y.L., S.F.C., X.S., and S.E.G. performed research; M.R.C. contributed new reagents/analytic tools; L.B.-L., X.S., J.H.-M., D.F.S., D.A.S., and R.D.C. analyzed data; and L.B.-L., R.L., J.H.-M., D.F.S., D.A.S., and R.D.C. wrote the paper.</p></fn><fn fn-type="equal" id="fn1"><p><sup>1</sup>L.B.-L. and R.L. contributed equally to this work.</p></fn><fn fn-type="present-address" id="fn2"><p><sup>2</sup>Present address: New England Biolabs, Ipswitch, MA 01938.</p></fn><fn fn-type="present-address" id="fn3"><p><sup>3</sup>Present address: Imperial College London, London SW7 2AZ, United Kingdom.</p></fn><fn fn-type="conflict"><p>The authors declare no conflict of interest.</p></fn></author-notes><pub-date pub-type="ppub"><day>3</day><month>6</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>19</day><month>5</month><year>2014</year></pub-date><volume>111</volume><issue>22</issue><fpage>E2241</fpage><lpage>E2250</lpage><self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201323162.pdf"></self-uri><abstract abstract-type="executive-summary"><title>Significance</title><p>Studies using novel “shotgun glycan microarray” technology identify, for the first time to our knowledge, the endogenous receptors for influenza viruses from a natural host, the pig. Libraries of total N-glycans from pig lung were probed for binding properties using a panel of influenza viruses isolated from humans, birds, and swine. Natural glycan receptors were identified for all viruses examined, and although some displayed the rather broad α2,3 or α2,6 sialic acid linkage specificity conventionally associated with avian or human viruses, other strains were highly specific, revealing a complexity that has not been demonstrated previously. Because pigs are often implicated as intermediate hosts for pandemic viruses, these results and the approaches described will transform our understanding of influenza host range, transmission, and pathogenicity.</p></abstract><abstract><p>Influenza viruses bind to host cell surface glycans containing terminal sialic acids, but as studies on influenza binding become more sophisticated, it is becoming evident that although sialic acid may be necessary, it is not sufficient for productive binding. To better define endogenous glycans that serve as viral receptors, we have explored glycan recognition in the pig lung, because influenza is broadly disseminated in swine, and swine have been postulated as an intermediary host for the emergence of pandemic strains. For these studies, we used the technology of “shotgun glycomics” to identify natural receptor glycans. The total released <italic>N</italic>- and <italic>O</italic>-glycans from pig lung glycoproteins and glycolipid-derived glycans were fluorescently tagged and separated by multidimensional HPLC, and individual glycans were covalently printed to generate pig lung shotgun glycan microarrays. All viruses tested interacted with one or more sialylated <italic>N</italic>-glycans but not <italic>O</italic>-glycans or glycolipid-derived glycans, and each virus demonstrated novel and unexpected differences in endogenous <italic>N</italic>-glycan recognition. The results illustrate the repertoire of specific, endogenous <italic>N</italic>-glycans of pig lung glycoproteins for virus recognition and offer a new direction for studying endogenous glycan functions in viral pathogenesis.</p></abstract><kwd-group><kwd>receptor binding</kwd><kwd>hemagglutinin</kwd><kwd>virus attachment</kwd></kwd-group><counts><page-count count="10"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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