Changes in the hemagglutinin of H5N1 viruses during human infection – Influence on receptor binding☆
Identifieur interne : 000957 ( Ncbi/Merge ); précédent : 000956; suivant : 000958Changes in the hemagglutinin of H5N1 viruses during human infection – Influence on receptor binding☆
Auteurs : Martin Crusat [Viêt Nam, Pays-Bas] ; Junfeng Liu [Royaume-Uni] ; Angelina S. Palma [Royaume-Uni, Portugal] ; Robert A. Childs [Royaume-Uni] ; Yan Liu [Royaume-Uni] ; Stephen A. Wharton [Royaume-Uni] ; Yi Pu Lin [Royaume-Uni] ; Peter J. Coombs [Royaume-Uni] ; Stephen R. Martin [Royaume-Uni] ; Mikhail Matrosovich [Allemagne] ; Zi Chen [Royaume-Uni] ; David J. Stevens [Royaume-Uni] ; Vo Minh Hien [Viêt Nam] ; Tran Tan Thanh [Viêt Nam] ; Le Nguyen Truc Nhu [Viêt Nam] ; Lam Anh Nguyet [Viêt Nam] ; Do Quang Ha [Viêt Nam] ; H. Rogier Van Doorn [Viêt Nam] ; Tran Tinh Hien [Viêt Nam] ; Harald S. Conradt [Allemagne] ; Makoto Kiso [Japon] ; Steve J. Gamblin [Royaume-Uni] ; Wengang Chai [Royaume-Uni] ; John J. Skehel [Royaume-Uni] ; Alan J. Hay [Royaume-Uni] ; Jeremy Farrar [Viêt Nam, Singapour] ; Menno D. De Jong [Viêt Nam, Pays-Bas] ; Ten Feizi [Royaume-Uni]Source :
- Virology [ 0042-6822 ] ; 2013.
Abstract
As avian influenza A(H5N1) viruses continue to circulate in Asia and Africa, global concerns of an imminent pandemic persist. Recent experimental studies suggest that efficient transmission between humans of current H5N1 viruses only requires a few genetic changes. An essential step is alteration of the virus hemagglutinin from preferential binding to avian receptors for the recognition of human receptors present in the upper airway. We have identified receptor-binding changes which emerged during H5N1 infection of humans, due to single amino acid substitutions, Ala134Val and Ile151Phe, in the hemagglutinin. Detailed biological, receptor-binding, and structural analyses revealed reduced binding of the mutated viruses to avian-like receptors, but without commensurate increased binding to the human-like receptors investigated, possibly reflecting a receptor-binding phenotype intermediate in adaptation to more human-like characteristics. These observations emphasize that evolution in nature of avian H5N1 viruses to efficient binding of human receptors is a complex multistep process.
Url:
DOI: 10.1016/j.virol.2013.08.010
PubMed: 24050651
PubMed Central: 3820038
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<author><name sortKey="Chen, Zi" sort="Chen, Zi" uniqKey="Chen Z" first="Zi" last="Chen">Zi Chen</name>
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<author><name sortKey="Hien, Vo Minh" sort="Hien, Vo Minh" uniqKey="Hien V" first="Vo Minh" last="Hien">Vo Minh Hien</name>
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<author><name sortKey="Thanh, Tran Tan" sort="Thanh, Tran Tan" uniqKey="Thanh T" first="Tran Tan" last="Thanh">Tran Tan Thanh</name>
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<wicri:regionArea>Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City</wicri:regionArea>
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<author><name sortKey="Nhu, Le Nguyen Truc" sort="Nhu, Le Nguyen Truc" uniqKey="Nhu L" first="Le Nguyen Truc" last="Nhu">Le Nguyen Truc Nhu</name>
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<country xml:lang="fr">Viêt Nam</country>
<wicri:regionArea>Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City</wicri:regionArea>
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</author>
<author><name sortKey="Nguyet, Lam Anh" sort="Nguyet, Lam Anh" uniqKey="Nguyet L" first="Lam Anh" last="Nguyet">Lam Anh Nguyet</name>
<affiliation wicri:level="1"><nlm:aff id="aff0035">Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam</nlm:aff>
<country xml:lang="fr">Viêt Nam</country>
<wicri:regionArea>Hospital for Tropical Diseases, Ho Chi Minh City</wicri:regionArea>
<wicri:noRegion>Ho Chi Minh City</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Ha, Do Quang" sort="Ha, Do Quang" uniqKey="Ha D" first="Do Quang" last="Ha">Do Quang Ha</name>
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<country xml:lang="fr">Viêt Nam</country>
<wicri:regionArea>Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City</wicri:regionArea>
<wicri:noRegion>Ho Chi Minh City</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Van Doorn, H Rogier" sort="Van Doorn, H Rogier" uniqKey="Van Doorn H" first="H. Rogier" last="Van Doorn">H. Rogier Van Doorn</name>
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<country xml:lang="fr">Viêt Nam</country>
<wicri:regionArea>Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City</wicri:regionArea>
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</affiliation>
</author>
<author><name sortKey="Hien, Tran Tinh" sort="Hien, Tran Tinh" uniqKey="Hien T" first="Tran Tinh" last="Hien">Tran Tinh Hien</name>
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<country xml:lang="fr">Viêt Nam</country>
<wicri:regionArea>Hospital for Tropical Diseases, Ho Chi Minh City</wicri:regionArea>
<wicri:noRegion>Ho Chi Minh City</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Conradt, Harald S" sort="Conradt, Harald S" uniqKey="Conradt H" first="Harald S." last="Conradt">Harald S. Conradt</name>
<affiliation wicri:level="3"><nlm:aff id="aff0040">GlycoThera GmbH, Hannover, Germany</nlm:aff>
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<wicri:regionArea>GlycoThera GmbH, Hannover</wicri:regionArea>
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</affiliation>
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<author><name sortKey="Kiso, Makoto" sort="Kiso, Makoto" uniqKey="Kiso M" first="Makoto" last="Kiso">Makoto Kiso</name>
<affiliation wicri:level="4"><nlm:aff id="aff0045">Department of Applied Bio-organic Chemistry, Gifu University, Japan</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Department of Applied Bio-organic Chemistry, Gifu University</wicri:regionArea>
<placeName><settlement type="city">Gifu (ville)</settlement>
<region type="province">Région du Chūbu</region>
<region type="prefecture">Préfecture de Gifu</region>
</placeName>
<orgName type="university">Université de Gifu</orgName>
</affiliation>
</author>
<author><name sortKey="Gamblin, Steve J" sort="Gamblin, Steve J" uniqKey="Gamblin S" first="Steve J." last="Gamblin">Steve J. Gamblin</name>
<affiliation wicri:level="3"><nlm:aff id="aff0015">MRC National Institute for Medical Research, London, United Kingdom</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>MRC National Institute for Medical Research, London</wicri:regionArea>
<placeName><settlement type="city">Londres</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Grand Londres</region>
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</affiliation>
</author>
<author><name sortKey="Chai, Wengang" sort="Chai, Wengang" uniqKey="Chai W" first="Wengang" last="Chai">Wengang Chai</name>
<affiliation wicri:level="1"><nlm:aff id="aff0020">The Glycosciences Laboratory, Department of Medicine, Imperial College London, United Kingdom</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>The Glycosciences Laboratory, Department of Medicine, Imperial College London</wicri:regionArea>
<wicri:noRegion>Imperial College London</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Skehel, John J" sort="Skehel, John J" uniqKey="Skehel J" first="John J." last="Skehel">John J. Skehel</name>
<affiliation wicri:level="3"><nlm:aff id="aff0015">MRC National Institute for Medical Research, London, United Kingdom</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>MRC National Institute for Medical Research, London</wicri:regionArea>
<placeName><settlement type="city">Londres</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Grand Londres</region>
</placeName>
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<author><name sortKey="Hay, Alan J" sort="Hay, Alan J" uniqKey="Hay A" first="Alan J." last="Hay">Alan J. Hay</name>
<affiliation wicri:level="3"><nlm:aff id="aff0015">MRC National Institute for Medical Research, London, United Kingdom</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>MRC National Institute for Medical Research, London</wicri:regionArea>
<placeName><settlement type="city">Londres</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Grand Londres</region>
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<author><name sortKey="Farrar, Jeremy" sort="Farrar, Jeremy" uniqKey="Farrar J" first="Jeremy" last="Farrar">Jeremy Farrar</name>
<affiliation wicri:level="1"><nlm:aff id="aff0005">Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam</nlm:aff>
<country xml:lang="fr">Viêt Nam</country>
<wicri:regionArea>Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City</wicri:regionArea>
<wicri:noRegion>Ho Chi Minh City</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff0050">National University of Singapore, Singapore</nlm:aff>
<country xml:lang="fr">Singapour</country>
<wicri:regionArea>National University of Singapore</wicri:regionArea>
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</author>
<author><name sortKey="De Jong, Menno D" sort="De Jong, Menno D" uniqKey="De Jong M" first="Menno D." last="De Jong">Menno D. De Jong</name>
<affiliation wicri:level="1"><nlm:aff id="aff0005">Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam</nlm:aff>
<country xml:lang="fr">Viêt Nam</country>
<wicri:regionArea>Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City</wicri:regionArea>
<wicri:noRegion>Ho Chi Minh City</wicri:noRegion>
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<affiliation wicri:level="4"><nlm:aff id="aff0010">Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands</nlm:aff>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam</wicri:regionArea>
<placeName><settlement type="city">Amsterdam</settlement>
<region nuts="2" type="province">Hollande-Septentrionale</region>
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<orgName type="university">Université d'Amsterdam</orgName>
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<author><name sortKey="Feizi, Ten" sort="Feizi, Ten" uniqKey="Feizi T" first="Ten" last="Feizi">Ten Feizi</name>
<affiliation wicri:level="1"><nlm:aff id="aff0020">The Glycosciences Laboratory, Department of Medicine, Imperial College London, United Kingdom</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>The Glycosciences Laboratory, Department of Medicine, Imperial College London</wicri:regionArea>
<wicri:noRegion>Imperial College London</wicri:noRegion>
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<series><title level="j">Virology</title>
<idno type="ISSN">0042-6822</idno>
<idno type="eISSN">1096-0341</idno>
<imprint><date when="2013">2013</date>
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<front><div type="abstract" xml:lang="en"><p>As avian influenza A(H5N1) viruses continue to circulate in Asia and Africa, global concerns of an imminent pandemic persist. Recent experimental studies suggest that efficient transmission between humans of current H5N1 viruses only requires a few genetic changes. An essential step is alteration of the virus hemagglutinin from preferential binding to avian receptors for the recognition of human receptors present in the upper airway. We have identified receptor-binding changes which emerged during H5N1 infection of humans, due to single amino acid substitutions, Ala134Val and Ile151Phe, in the hemagglutinin. Detailed biological, receptor-binding, and structural analyses revealed reduced binding of the mutated viruses to avian-like receptors, but without commensurate increased binding to the human-like receptors investigated, possibly reflecting a receptor-binding phenotype intermediate in adaptation to more human-like characteristics. These observations emphasize that evolution in nature of avian H5N1 viruses to efficient binding of human receptors is a complex multistep process.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Virology</journal-id>
<journal-id journal-id-type="iso-abbrev">Virology</journal-id>
<journal-title-group><journal-title>Virology</journal-title>
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<issn pub-type="ppub">0042-6822</issn>
<issn pub-type="epub">1096-0341</issn>
<publisher><publisher-name>Academic Press</publisher-name>
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<article-id pub-id-type="pmc">3820038</article-id>
<article-id pub-id-type="publisher-id">S0042-6822(13)00481-9</article-id>
<article-id pub-id-type="doi">10.1016/j.virol.2013.08.010</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
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<given-names>Harald S.</given-names>
</name>
<xref rid="aff0040" ref-type="aff">h</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kiso</surname>
<given-names>Makoto</given-names>
</name>
<xref rid="aff0045" ref-type="aff">i</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gamblin</surname>
<given-names>Steve J.</given-names>
</name>
<xref rid="aff0015" ref-type="aff">c</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chai</surname>
<given-names>Wengang</given-names>
</name>
<xref rid="aff0020" ref-type="aff">d</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Skehel</surname>
<given-names>John J.</given-names>
</name>
<xref rid="aff0015" ref-type="aff">c</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hay</surname>
<given-names>Alan J.</given-names>
</name>
<xref rid="aff0015" ref-type="aff">c</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Farrar</surname>
<given-names>Jeremy</given-names>
</name>
<xref rid="aff0005" ref-type="aff">a</xref>
<xref rid="aff0050" ref-type="aff">j</xref>
</contrib>
<contrib contrib-type="author"><name><surname>de Jong</surname>
<given-names>Menno D.</given-names>
</name>
<email>dejongmd@gmail.com</email>
<xref rid="aff0005" ref-type="aff">a</xref>
<xref rid="aff0010" ref-type="aff">b</xref>
<xref rid="cor1" ref-type="corresp">⁎</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Feizi</surname>
<given-names>Ten</given-names>
</name>
<email>t.feizi@imperial.ac.uk</email>
<xref rid="aff0020" ref-type="aff">d</xref>
<xref rid="cor2" ref-type="corresp">⁎⁎</xref>
</contrib>
</contrib-group>
<aff id="aff0005"><label>a</label>
Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam</aff>
<aff id="aff0010"><label>b</label>
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands</aff>
<aff id="aff0015"><label>c</label>
MRC National Institute for Medical Research, London, United Kingdom</aff>
<aff id="aff0020"><label>d</label>
The Glycosciences Laboratory, Department of Medicine, Imperial College London, United Kingdom</aff>
<aff id="aff0025"><label>e</label>
REQUIMTE/CQFB, Faculty of Science and Technology, New University of Lisbon, Caparica, Portugal</aff>
<aff id="aff0030"><label>f</label>
Institute of Virology, Philipps University, Marburg, Germany</aff>
<aff id="aff0035"><label>g</label>
Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam</aff>
<aff id="aff0040"><label>h</label>
GlycoThera GmbH, Hannover, Germany</aff>
<aff id="aff0045"><label>i</label>
Department of Applied Bio-organic Chemistry, Gifu University, Japan</aff>
<aff id="aff0050"><label>j</label>
National University of Singapore, Singapore</aff>
<author-notes><corresp id="cor1"><label>⁎</label>
Corresponding author at: Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands <email>dejongmd@gmail.com</email>
</corresp>
<corresp id="cor2"><label>⁎⁎</label>
Corresponding author. Tel.: +44 (0)20-7594 7207. <email>t.feizi@imperial.ac.uk</email>
</corresp>
<fn id="fn1"><label>1</label>
<p>Present address: Research Unit in Pediatric Vaccines, Galician Genetics Group, Hospital Clínico Universitario de Santiago de Compostela, Spain.</p>
</fn>
<fn id="fn2"><label>2</label>
<p>These authors contributed equally.</p>
</fn>
<fn id="fn3"><label>3</label>
<p>Present address: MOA Key Laboratory of Plant Pathology, China Agricultural University, No. 2 Yuanmingyuan Xilu, Beijing, PR China.</p>
</fn>
<fn id="fn4"><label>4</label>
<p>Present address: MRC Technology, 1–3 Burtonhole Lane, London NW7 1AD, United Kingdom.</p>
</fn>
<fn id="fn5"><label>5</label>
<p>Present address: Xiang Ya Second Affiliated Hospital, Central South University, PR China.</p>
</fn>
</author-notes>
<pub-date pub-type="pmc-release"><day>1</day>
<month>12</month>
<year>2013</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>12</month>
<year>2013</year>
</pub-date>
<volume>447</volume>
<issue>1-2</issue>
<fpage>326</fpage>
<lpage>337</lpage>
<history><date date-type="received"><day>21</day>
<month>6</month>
<year>2013</year>
</date>
<date date-type="rev-recd"><day>6</day>
<month>8</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>12</day>
<month>8</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>© 2013 The Authros</copyright-statement>
<copyright-year>2013</copyright-year>
<license xlink:href="https://creativecommons.org/licenses/by/3.0/"><license-p>Open Access under <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/3.0/">CC BY 3.0</ext-link>
license</license-p>
</license>
</permissions>
<abstract><p>As avian influenza A(H5N1) viruses continue to circulate in Asia and Africa, global concerns of an imminent pandemic persist. Recent experimental studies suggest that efficient transmission between humans of current H5N1 viruses only requires a few genetic changes. An essential step is alteration of the virus hemagglutinin from preferential binding to avian receptors for the recognition of human receptors present in the upper airway. We have identified receptor-binding changes which emerged during H5N1 infection of humans, due to single amino acid substitutions, Ala134Val and Ile151Phe, in the hemagglutinin. Detailed biological, receptor-binding, and structural analyses revealed reduced binding of the mutated viruses to avian-like receptors, but without commensurate increased binding to the human-like receptors investigated, possibly reflecting a receptor-binding phenotype intermediate in adaptation to more human-like characteristics. These observations emphasize that evolution in nature of avian H5N1 viruses to efficient binding of human receptors is a complex multistep process.</p>
</abstract>
<abstract abstract-type="author-highlights"><title>Highlights</title>
<p><list list-type="simple"><list-item id="u0005"><label>•</label>
<p>Changes in receptor binding of HA during H5N1 human infection were identified.</p>
</list-item>
<list-item id="u0010"><label>•</label>
<p>Single A134V and L151F substitutions caused reduced affinity for avian receptors.</p>
</list-item>
<list-item id="u0015"><label>•</label>
<p>Glycan array analyses were used to identify changes in receptor binding specificity.</p>
</list-item>
<list-item id="u0020"><label>•</label>
<p>Structural basis for altered receptor binding was examined by X-ray crystallography.</p>
</list-item>
</list>
</p>
</abstract>
<kwd-group><title>Keywords</title>
<kwd>H5N1 influenza infection</kwd>
<kwd>Pyrosequencing</kwd>
<kwd>Hemagglutinin</kwd>
<kwd>Receptor specificity</kwd>
<kwd>Hemagglutination assays</kwd>
<kwd>Receptor binding</kwd>
<kwd>Carbohydrate microarray</kwd>
<kwd>Biolayer interferometry</kwd>
<kwd>Synthetic sialylglycopolymers</kwd>
<kwd>Hemagglutinin X-ray crystal structure</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="f0005"><label>Fig. 1</label>
<caption><p>Binding of biotinylated sialylglycopolymers 3SLN-PAA (30 kDa) and 6SLN-PAA (1 MDa) to viruses adsorbed in 96-well microplates. H5N1 viruses rVN1194 (circles), rVN1194(Ala134Val) (diamonds), rVNCL105(Ala134Val) (filled diamonds), rVN1194(Glu186Asp) (triangles), rVNCL01(Glu186Asp) (filled triangles). Control human H3N2 virus R1 (asterisks). The data show averaged values of two replicates and are representative of two independent experiments performed on different days.</p>
</caption>
<graphic xlink:href="gr1"></graphic>
</fig>
<fig id="f0010"><label>Fig. 2</label>
<caption><p>Virus binding analysis by biolayer interferometry. H5 viruses rVN1194 (circles), rVN1194(Glu186Asp) (triangles) and rVN1194(Ala134Val) (diamonds) were analyzed for binding to immobilized biotinylated 30 kDA sialylglycopolymers 3SLN-PAA and 6SLN-PAA.</p>
</caption>
<graphic xlink:href="gr2"></graphic>
</fig>
<fig id="f0015"><label>Fig. 3</label>
<caption><p>Carbohydrate microarray analyses of wild type and mutant H5N1 viruses and X31(H3N2) as control. Numerical scores for the binding signals are shown as means of duplicate spots at 5 fmol/spot (with error bars) and are representative of at least three independent experiments. The insets show enlarged the <italic>Y</italic>
-axis scales for the 134 mutant viruses, which gave very low binding signals. The microarrays consisted of lipid-linked oligosaccharide probes, printed on nitrocellulose-coated glass slides. These are listed in <xref rid="s0145" ref-type="fn">Supplementary Table S2</xref>
and arranged according to sialic acid linkage and oligosaccharide backbone sequence. The various types of sialic acid linkage are indicated by the colored panels as defined at the bottom of the figure.</p>
</caption>
<graphic xlink:href="gr3"></graphic>
</fig>
<fig id="f0020"><label>Fig. 4</label>
<caption><p>Crystal structures of wild type and mutant H5 hemagglutinins complexed with avian and human receptor analogs (LSTa and LSTc, respectively). (A) Superposition of complexes of LSTa with rVN1194 HA (gray) and with rVN1194(Glu186Asp) HA (green). (B) Superposition of complexes of LSTc with rVN1194 HA (gray) and with rVN1194(Glu186Asp) HA (green). Only density for the Sia-1 of the receptor analog was detected. (C) Superposition of complexes of LSTa with rVN1194 HA (gray) and with rVN1194(Ala134Val) HA (yellow). The increase in width of the hydrophobic channel between the 130 and 220 loops in the mutant that results in an increase in the distance between Gln222 and Ser132 is shown. (D) Superposition of complexes of LSTc with rVN1194 HA (gray) and with rVN1194(Ala134Val) HA (yellow). Only density for the Sia-1 of the receptor analog was detected. E, Superposition of the complex of rVN1194 HA with LSTc (gray) and rVN1194(Ile151Phe) HA (blue). Although no sialic acid was detected in the Ile151Phe crystals soaked in LSTc the proximity of Phe 151 to where the sialic acid would be located is shown.</p>
</caption>
<graphic xlink:href="gr4"></graphic>
</fig>
<table-wrap id="t0005" position="float"><label>Table 1</label>
<caption><p>Hemagglutination titers of MDCK cell- and egg-cultured Influenza A viruses.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th><bold>Virus</bold>
</th>
<th><bold>Subtype</bold>
</th>
<th><bold>Origin</bold>
</th>
<th colspan="2"><bold>MDCK GMT</bold>
<xref rid="tbl1fna" ref-type="table-fn">a</xref>
<hr></hr>
</th>
<th colspan="2"><bold>ω5 GMT</bold>
<xref rid="tbl1fna" ref-type="table-fn">a</xref>
<hr></hr>
</th>
</tr>
<tr><th></th>
<th></th>
<th></th>
<th><bold>Horse</bold>
</th>
<th><bold>Guinea pig</bold>
</th>
<th><bold>Horse</bold>
</th>
<th><bold>Guinea pig</bold>
</th>
</tr>
</thead>
<tbody><tr><td align="char">A/VN/HTD33/04</td>
<td>H1N1</td>
<td>Human</td>
<td align="char">0</td>
<td align="char">75</td>
<td>0</td>
<td>24</td>
</tr>
<tr><td align="char">A/VN/HTD34/04</td>
<td>H1N1</td>
<td>Human</td>
<td align="char">0</td>
<td align="char">192</td>
<td>0</td>
<td>32</td>
</tr>
<tr><td align="char">A/VN/HTD566/04</td>
<td>H3N2</td>
<td>Human</td>
<td align="char">0</td>
<td align="char">53</td>
<td>0</td>
<td>4</td>
</tr>
<tr><td align="char">A/VN/HTD567/04</td>
<td>H3N2</td>
<td>Human</td>
<td align="char">0</td>
<td align="char">21</td>
<td>0</td>
<td>8</td>
</tr>
<tr><td align="char">A/Ck/VLC13/06</td>
<td>H5N1</td>
<td>Chicken</td>
<td align="char">267</td>
<td align="char">144</td>
<td>12</td>
<td>32</td>
</tr>
<tr><td align="char">A/Ck/VLC15/06</td>
<td>H5N1</td>
<td>Chicken</td>
<td align="char">491</td>
<td align="char">416</td>
<td>64</td>
<td>24</td>
</tr>
<tr><td align="char">A/Dk/LAD404/06</td>
<td>H4N6</td>
<td>Duck</td>
<td align="char">341</td>
<td align="char">352</td>
<td>48</td>
<td>128</td>
</tr>
<tr><td align="char">A/Dk/DTD516/06</td>
<td>H6N1</td>
<td>Duck</td>
<td align="char">224</td>
<td align="char">160</td>
<td>32</td>
<td>32</td>
</tr>
<tr><td align="char">A/VN/CL1/04</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">0</td>
<td align="char">100</td>
<td>512</td>
<td>192</td>
</tr>
<tr><td align="char">A/VN/CL2/04</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">52</td>
<td align="char">72</td>
<td>64</td>
<td>48</td>
</tr>
<tr><td align="char">A/VNCL26/04</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">64</td>
<td align="char">192</td>
<td>256</td>
<td>192</td>
</tr>
<tr><td align="char">A/VN/CL36/04</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">64</td>
<td align="char">68</td>
<td>64</td>
<td>64</td>
</tr>
<tr><td align="char">A/VN/PEV016/04</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">32</td>
<td align="char">44</td>
<td>128</td>
<td>96</td>
</tr>
<tr><td align="char">A/VN/CL100/05</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">112</td>
<td align="char">352</td>
<td>192</td>
<td>384</td>
</tr>
<tr><td colspan="7">
</td>
</tr>
<tr><td align="char">A/VN/CL105/05</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">0</td>
<td align="char">120</td>
<td>128</td>
<td>320</td>
</tr>
<tr><td align="char">A/VN/CL107/05</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">112</td>
<td align="char">464</td>
<td>NA<xref rid="tbl1fnb" ref-type="table-fn">b</xref>
</td>
<td>NA<xref rid="tbl1fnb" ref-type="table-fn">b</xref>
</td>
</tr>
<tr><td align="char">A/VN/CL115/05</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">112</td>
<td align="char">200</td>
<td>8</td>
<td>20</td>
</tr>
<tr><td align="char">A/VN/CL119/05</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">80</td>
<td align="char">136</td>
<td>384</td>
<td>384</td>
</tr>
<tr><td align="char">A/VN/CL2009C/05</td>
<td>H5N1</td>
<td>Human</td>
<td align="char">27</td>
<td align="char">405</td>
<td>128</td>
<td>96</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>ω5: five serial passages in the allantois of embryonated hen eggs.</p>
</fn>
</table-wrap-foot>
<table-wrap-foot><fn id="tbl1fna"><label>a</label>
<p>Geometric mean titers of triplicates.</p>
</fn>
</table-wrap-foot>
<table-wrap-foot><fn id="tbl1fnb"><label>b</label>
<p>Not analyzed due to technical difficulties.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="t0010" position="float"><label>Table 2</label>
<caption><p>Amino acid residues in MDCK cell- and egg-cultured viruses and viruses in clinical specimens.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th><bold>Virus isolates and clinical samples (day since onset of illness)</bold>
</th>
<th><bold>HA position</bold>
</th>
<th colspan="2"><bold>Amino acid (%)</bold>
<xref rid="tbl2fna" ref-type="table-fn">a</xref>
<hr></hr>
</th>
</tr>
<tr><th><bold>Wild-type</bold>
<xref rid="tbl2fnb" ref-type="table-fn">b</xref>
</th>
<th><bold>Mutant</bold>
</th>
</tr>
</thead>
<tbody><tr><td>A/VN/CL1/04</td>
<td align="char">186</td>
<td>Glu (5)</td>
<td>Asp (95)</td>
</tr>
<tr><td>A/VN/CL1/04 ω5</td>
<td align="char">186</td>
<td>Glu (97)</td>
<td>Asp (3)</td>
</tr>
<tr><td>CL1 Throat swab (d8)<xref rid="tbl2fnc" ref-type="table-fn">c</xref>
</td>
<td align="char">186</td>
<td>Glu (100)</td>
<td>Asp (0)</td>
</tr>
<tr><td>CL1 Nose swab (d10)</td>
<td align="char">186</td>
<td>Glu (100)</td>
<td>Asp (0)</td>
</tr>
<tr><td colspan="4">
</td>
</tr>
<tr><td>A/VN/CL2009C/05</td>
<td align="char">151</td>
<td>Ile (3)</td>
<td>Phe (95), Leu (2)</td>
</tr>
<tr><td>A/VN/CL2009C/05 ω5</td>
<td align="char">151</td>
<td>Ile (0)</td>
<td>Phe (2), Leu (98)</td>
</tr>
<tr><td>CL2009 Throat swab (d7)</td>
<td align="char">151</td>
<td>Ile (35)</td>
<td>Phe (65)</td>
</tr>
<tr><td>CL2009 Nose swab (d8)</td>
<td align="char">151</td>
<td>Ile (0)</td>
<td>Phe (100)</td>
</tr>
<tr><td>CL2009 Throat swab (d8)<xref rid="tbl2fnc" ref-type="table-fn">c</xref>
</td>
<td align="char">151</td>
<td>Ile (0)</td>
<td>Phe (100)</td>
</tr>
<tr><td colspan="4">
</td>
</tr>
<tr><td>A/VN/CL105/05</td>
<td align="char">134</td>
<td>Ala (48)</td>
<td>Val (52)</td>
</tr>
<tr><td>A/VN/CL105/05 ω5</td>
<td align="char">134</td>
<td>Ala (96)</td>
<td>Val (4)</td>
</tr>
<tr><td>CL105 Throat swab (d4)<xref rid="tbl2fnc" ref-type="table-fn">c</xref>
</td>
<td align="char">134</td>
<td>Ala (26)</td>
<td>Val (74)</td>
</tr>
<tr><td>CL105 Tracheal aspirate (d4)</td>
<td align="char">134</td>
<td>Ala (27)</td>
<td>Val (73)</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>ω5: five serial passages in the allantois of embryonated chicken eggs.</p>
</fn>
</table-wrap-foot>
<table-wrap-foot><fn id="tbl2fna"><label>a</label>
<p>Proportions of subpopulations were determined by pyrosequencing of the regions of interest.</p>
</fn>
</table-wrap-foot>
<table-wrap-foot><fn id="tbl2fnb"><label>b</label>
<p>Wild-type refers to the avian virus consensus sequence.</p>
</fn>
</table-wrap-foot>
<table-wrap-foot><fn id="tbl2fnc"><label>c</label>
<p>Source of the MDCK cell isolate.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="t0015" position="float"><label>Table 3</label>
<caption><p>Amino acid differences and hemagglutination patterns with guinea pig and horse red blood cells of recombinant H5N1 viruses<xref rid="tbl3fna" ref-type="table-fn">a</xref>
.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th><bold>Viruses</bold>
</th>
<th colspan="6"><bold>HA residue number</bold>
<hr></hr>
</th>
<th colspan="2"><bold>Hemagglutination titer</bold>
<xref rid="tbl3fnb" ref-type="table-fn">b</xref>
<hr></hr>
</th>
</tr>
<tr><th>83</th>
<th>94</th>
<th>134</th>
<th>175</th>
<th>186</th>
<th>188</th>
<th>Guinea pig</th>
<th>Horse</th>
</tr>
</thead>
<tbody><tr><td>NIBRG14 (rVN1194)</td>
<td>Ala</td>
<td>Asp</td>
<td><bold>Ala</bold>
</td>
<td>Leu</td>
<td><bold>Glu</bold>
</td>
<td>Thr</td>
<td>256</td>
<td align="left">128</td>
</tr>
<tr><td colspan="9">
</td>
</tr>
<tr><td>rVNCL105 (Ala134Val)</td>
<td>Val</td>
<td>Val</td>
<td><bold>Val</bold>
</td>
<td>Ile</td>
<td></td>
<td>Ile</td>
<td>256</td>
<td align="left">4</td>
</tr>
<tr><td>rVN1194 (Ala134Val)</td>
<td></td>
<td></td>
<td><bold>Val</bold>
</td>
<td></td>
<td></td>
<td></td>
<td>1024</td>
<td align="left"><4</td>
</tr>
<tr><td>rVNCL01 (Glu186Asp)</td>
<td></td>
<td></td>
<td></td>
<td>Met</td>
<td><bold>Asp</bold>
</td>
<td></td>
<td>1024</td>
<td align="left"><4</td>
</tr>
<tr><td>rVN1194 (Glu186Asp)</td>
<td></td>
<td></td>
<td></td>
<td></td>
<td><bold>Asp</bold>
</td>
<td></td>
<td>512</td>
<td align="left"><4</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="tbl3fna"><label>a</label>
<p>The residue designation is according to H5 numbering. Differences from the sequence of VN1194 are shown. Amino acids in positions that were altered on egg passage are highlighted in bold.</p>
</fn>
</table-wrap-foot>
<table-wrap-foot><fn id="tbl3fnb"><label>b</label>
<p>Using the virus-containing allantoic fluid before purification of the viruses for the microarray analyses.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="t0020" position="float"><label>Table 4</label>
<caption><p>Virus binding to 24 oligosaccharide probes that are well matched with respect to backbone sequences, substituents and aglycones in the carbohydrate microarrays.</p>
</caption>
<table frame="hsides" rules="groups"><tbody><tr><td><inline-graphic xlink:href="fx1.gif"></inline-graphic>
</td>
</tr>
</tbody>
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</table-wrap>
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<li>Japon</li>
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<li>Singapour</li>
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<li>Basse-Saxe</li>
<li>District de Giessen</li>
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<li>Préfecture de Gifu</li>
<li>Région du Chūbu</li>
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<li>Gifu (ville)</li>
<li>Hanovre</li>
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<orgName><li>Université d'Amsterdam</li>
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<name sortKey="Coombs, Peter J" sort="Coombs, Peter J" uniqKey="Coombs P" first="Peter J." last="Coombs">Peter J. Coombs</name>
<name sortKey="Feizi, Ten" sort="Feizi, Ten" uniqKey="Feizi T" first="Ten" last="Feizi">Ten Feizi</name>
<name sortKey="Gamblin, Steve J" sort="Gamblin, Steve J" uniqKey="Gamblin S" first="Steve J." last="Gamblin">Steve J. Gamblin</name>
<name sortKey="Hay, Alan J" sort="Hay, Alan J" uniqKey="Hay A" first="Alan J." last="Hay">Alan J. Hay</name>
<name sortKey="Lin, Yi Pu" sort="Lin, Yi Pu" uniqKey="Lin Y" first="Yi Pu" last="Lin">Yi Pu Lin</name>
<name sortKey="Liu, Yan" sort="Liu, Yan" uniqKey="Liu Y" first="Yan" last="Liu">Yan Liu</name>
<name sortKey="Martin, Stephen R" sort="Martin, Stephen R" uniqKey="Martin S" first="Stephen R." last="Martin">Stephen R. Martin</name>
<name sortKey="Palma, Angelina S" sort="Palma, Angelina S" uniqKey="Palma A" first="Angelina S." last="Palma">Angelina S. Palma</name>
<name sortKey="Skehel, John J" sort="Skehel, John J" uniqKey="Skehel J" first="John J." last="Skehel">John J. Skehel</name>
<name sortKey="Stevens, David J" sort="Stevens, David J" uniqKey="Stevens D" first="David J." last="Stevens">David J. Stevens</name>
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<country name="Japon"><region name="Région du Chūbu"><name sortKey="Kiso, Makoto" sort="Kiso, Makoto" uniqKey="Kiso M" first="Makoto" last="Kiso">Makoto Kiso</name>
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