The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance
Identifieur interne : 000B94 ( Pmc/Curation ); précédent : 000B93; suivant : 000B95The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance
Auteurs : Wenjuan Du [Pays-Bas] ; Hongbo Guo [Pays-Bas] ; Vera S. Nijman [Pays-Bas] ; Jennifer Doedt [Allemagne] ; Erhard Van Der Vries [Pays-Bas] ; Joline Van Der Lee [Pays-Bas] ; Zeshi Li [Pays-Bas] ; Geert-Jan Boons [Pays-Bas] ; Frank J. M. Van Kuppeveld [Pays-Bas] ; Erik De Vries [Pays-Bas] ; Mikhail Matrosovich [Allemagne] ; Cornelis A. M. De Haan [Pays-Bas]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2019.
Abstract
Influenza A virus (IAV) neuraminidase (NA) receptor-destroying activity and hemagglutinin (HA) receptor-binding affinity need to be balanced with the host receptor repertoire for optimal viral fitness. NAs of avian, but not human viruses, contain a functional 2nd sialic acid (SIA)-binding site (2SBS) adjacent to the catalytic site, which contributes to sialidase activity against multivalent substrates. The receptor-binding specificity and potentially crucial contribution of the 2SBS to the HA-NA balance of virus particles is, however, poorly characterized. Here, we elucidated the receptor-binding specificity of the 2SBS of N2 NA and established an important role for this site in the virion HA-NA-receptor balance. NAs of H2N2/1957 pandemic virus with or without a functional 2SBS and viruses containing this NA were analysed. Avian-like N2, with a restored 2SBS due to an amino acid substitution at position 367, was more active than human N2 on multivalent substrates containing α2,3-linked SIAs, corresponding with the pronounced binding-specificity of avian-like N2 for these receptors. When introduced into human viruses, avian-like N2 gave rise to altered plaque morphology and decreased replication compared to human N2. An opposite replication phenotype was observed when N2 was combined with avian-like HA. Specific bio-layer interferometry assays revealed a clear effect of the 2SBS on the dynamic interaction of virus particles with receptors. The absence or presence of a functional 2SBS affected virion-receptor binding and receptor cleavage required for particle movement on a receptor-coated surface and subsequent NA-dependent self-elution. The contribution of the 2SBS to virus-receptor interactions depended on the receptor-binding properties of HA and the identity of the receptors used. We conclude that the 2SBS is an important and underappreciated determinant of the HA-NA-receptor balance. The rapid loss of a functional 2SBS in pandemic viruses may have served to balance the novel host receptor-repertoire and altered receptor-binding properties of the corresponding HA protein.
Url:
DOI: 10.1371/journal.ppat.1007860
PubMed: 31181126
PubMed Central: 6586374
Links toward previous steps (curation, corpus...)
- to stream Pmc, to step Corpus: Pour aller vers cette notice dans l'étape Curation :000B94
Links to Exploration step
PMC:6586374Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The 2<sup>nd</sup> sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance</title><author><name sortKey="Du, Wenjuan" sort="Du, Wenjuan" uniqKey="Du W" first="Wenjuan" last="Du">Wenjuan Du</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Guo, Hongbo" sort="Guo, Hongbo" uniqKey="Guo H" first="Hongbo" last="Guo">Hongbo Guo</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Nijman, Vera S" sort="Nijman, Vera S" uniqKey="Nijman V" first="Vera S." last="Nijman">Vera S. Nijman</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Doedt, Jennifer" sort="Doedt, Jennifer" uniqKey="Doedt J" first="Jennifer" last="Doedt">Jennifer Doedt</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Institute of Virology, Philipps University, Marburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Virology, Philipps University, Marburg</wicri:regionArea></affiliation></author><author><name sortKey="Van Der Vries, Erhard" sort="Van Der Vries, Erhard" uniqKey="Van Der Vries E" first="Erhard" last="Van Der Vries">Erhard Van Der Vries</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Van Der Lee, Joline" sort="Van Der Lee, Joline" uniqKey="Van Der Lee J" first="Joline" last="Van Der Lee">Joline Van Der Lee</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Li, Zeshi" sort="Li, Zeshi" uniqKey="Li Z" first="Zeshi" last="Li">Zeshi Li</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht, the Netherlands</addr-line></nlm:aff><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Boons, Geert Jan" sort="Boons, Geert Jan" uniqKey="Boons G" first="Geert-Jan" last="Boons">Geert-Jan Boons</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht, the Netherlands</addr-line></nlm:aff><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Van Kuppeveld, Frank J M" sort="Van Kuppeveld, Frank J M" uniqKey="Van Kuppeveld F" first="Frank J. M." last="Van Kuppeveld">Frank J. M. Van Kuppeveld</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="De Vries, Erik" sort="De Vries, Erik" uniqKey="De Vries E" first="Erik" last="De Vries">Erik De Vries</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Matrosovich, Mikhail" sort="Matrosovich, Mikhail" uniqKey="Matrosovich M" first="Mikhail" last="Matrosovich">Mikhail Matrosovich</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Institute of Virology, Philipps University, Marburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Virology, Philipps University, Marburg</wicri:regionArea></affiliation></author><author><name sortKey="De Haan, Cornelis A M" sort="De Haan, Cornelis A M" uniqKey="De Haan C" first="Cornelis A. M." last="De Haan">Cornelis A. M. De Haan</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31181126</idno><idno type="pmc">6586374</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6586374</idno><idno type="RBID">PMC:6586374</idno><idno type="doi">10.1371/journal.ppat.1007860</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000B94</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000B94</idno><idno type="wicri:Area/Pmc/Curation">000B94</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000B94</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The 2<sup>nd</sup> sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance</title><author><name sortKey="Du, Wenjuan" sort="Du, Wenjuan" uniqKey="Du W" first="Wenjuan" last="Du">Wenjuan Du</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Guo, Hongbo" sort="Guo, Hongbo" uniqKey="Guo H" first="Hongbo" last="Guo">Hongbo Guo</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Nijman, Vera S" sort="Nijman, Vera S" uniqKey="Nijman V" first="Vera S." last="Nijman">Vera S. Nijman</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Doedt, Jennifer" sort="Doedt, Jennifer" uniqKey="Doedt J" first="Jennifer" last="Doedt">Jennifer Doedt</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Institute of Virology, Philipps University, Marburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Virology, Philipps University, Marburg</wicri:regionArea></affiliation></author><author><name sortKey="Van Der Vries, Erhard" sort="Van Der Vries, Erhard" uniqKey="Van Der Vries E" first="Erhard" last="Van Der Vries">Erhard Van Der Vries</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Van Der Lee, Joline" sort="Van Der Lee, Joline" uniqKey="Van Der Lee J" first="Joline" last="Van Der Lee">Joline Van Der Lee</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Li, Zeshi" sort="Li, Zeshi" uniqKey="Li Z" first="Zeshi" last="Li">Zeshi Li</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht, the Netherlands</addr-line></nlm:aff><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Boons, Geert Jan" sort="Boons, Geert Jan" uniqKey="Boons G" first="Geert-Jan" last="Boons">Geert-Jan Boons</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht, the Netherlands</addr-line></nlm:aff><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Van Kuppeveld, Frank J M" sort="Van Kuppeveld, Frank J M" uniqKey="Van Kuppeveld F" first="Frank J. M." last="Van Kuppeveld">Frank J. M. Van Kuppeveld</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="De Vries, Erik" sort="De Vries, Erik" uniqKey="De Vries E" first="Erik" last="De Vries">Erik De Vries</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Matrosovich, Mikhail" sort="Matrosovich, Mikhail" uniqKey="Matrosovich M" first="Mikhail" last="Matrosovich">Mikhail Matrosovich</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Institute of Virology, Philipps University, Marburg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Virology, Philipps University, Marburg</wicri:regionArea></affiliation></author><author><name sortKey="De Haan, Cornelis A M" sort="De Haan, Cornelis A M" uniqKey="De Haan C" first="Cornelis A. M." last="De Haan">Cornelis A. M. De Haan</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS Pathogens</title><idno type="ISSN">1553-7366</idno><idno type="eISSN">1553-7374</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Influenza A virus (IAV) neuraminidase (NA) receptor-destroying activity and hemagglutinin (HA) receptor-binding affinity need to be balanced with the host receptor repertoire for optimal viral fitness. NAs of avian, but not human viruses, contain a functional 2<sup>nd</sup> sialic acid (SIA)-binding site (2SBS) adjacent to the catalytic site, which contributes to sialidase activity against multivalent substrates. The receptor-binding specificity and potentially crucial contribution of the 2SBS to the HA-NA balance of virus particles is, however, poorly characterized. Here, we elucidated the receptor-binding specificity of the 2SBS of N2 NA and established an important role for this site in the virion HA-NA-receptor balance. NAs of H2N2/1957 pandemic virus with or without a functional 2SBS and viruses containing this NA were analysed. Avian-like N2, with a restored 2SBS due to an amino acid substitution at position 367, was more active than human N2 on multivalent substrates containing α2,3-linked SIAs, corresponding with the pronounced binding-specificity of avian-like N2 for these receptors. When introduced into human viruses, avian-like N2 gave rise to altered plaque morphology and decreased replication compared to human N2. An opposite replication phenotype was observed when N2 was combined with avian-like HA. Specific bio-layer interferometry assays revealed a clear effect of the 2SBS on the dynamic interaction of virus particles with receptors. The absence or presence of a functional 2SBS affected virion-receptor binding and receptor cleavage required for particle movement on a receptor-coated surface and subsequent NA-dependent self-elution. The contribution of the 2SBS to virus-receptor interactions depended on the receptor-binding properties of HA and the identity of the receptors used. We conclude that the 2SBS is an important and underappreciated determinant of the HA-NA-receptor balance. The rapid loss of a functional 2SBS in pandemic viruses may have served to balance the novel host receptor-repertoire and altered receptor-binding properties of the corresponding HA protein.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Gambaryan, As" uniqKey="Gambaryan A">AS Gambaryan</name></author><author><name sortKey="Matrosovich, Mn" uniqKey="Matrosovich M">MN Matrosovich</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Byrd Leotis, L" uniqKey="Byrd Leotis L">L Byrd-Leotis</name></author><author><name sortKey="Cummings, Rd" uniqKey="Cummings R">RD Cummings</name></author><author><name sortKey="Steinhauer, Da" uniqKey="Steinhauer D">DA Steinhauer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gaymard, A" uniqKey="Gaymard A">A Gaymard</name></author><author><name sortKey="Le Briand, N" uniqKey="Le Briand N">N Le Briand</name></author><author><name sortKey="Frobert, E" uniqKey="Frobert E">E Frobert</name></author><author><name sortKey="Lina, B" uniqKey="Lina B">B Lina</name></author><author><name sortKey="Escuret, V" uniqKey="Escuret V">V Escuret</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yen, Hl" uniqKey="Yen H">HL Yen</name></author><author><name sortKey="Liang, Ch" uniqKey="Liang C">CH Liang</name></author><author><name sortKey="Wu, Cy" uniqKey="Wu C">CY Wu</name></author><author><name sortKey="Forrest, Hl" uniqKey="Forrest H">HL Forrest</name></author><author><name sortKey="Ferguson, A" uniqKey="Ferguson A">A Ferguson</name></author><author><name sortKey="Choy, Kt" uniqKey="Choy K">KT Choy</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Xu, R" uniqKey="Xu R">R Xu</name></author><author><name sortKey="Zhu, X" uniqKey="Zhu X">X Zhu</name></author><author><name sortKey="Mcbride, R" uniqKey="Mcbride R">R McBride</name></author><author><name sortKey="Nycholat, Cm" uniqKey="Nycholat C">CM Nycholat</name></author><author><name sortKey="Yu, W" uniqKey="Yu W">W Yu</name></author><author><name sortKey="Paulson, Jc" uniqKey="Paulson J">JC Paulson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Baigent, Sj" uniqKey="Baigent S">SJ Baigent</name></author><author><name sortKey="Mccauley, Jw" uniqKey="Mccauley J">JW McCauley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cohen, M" uniqKey="Cohen M">M Cohen</name></author><author><name sortKey="Zhang, X Q" uniqKey="Zhang X">X-Q Zhang</name></author><author><name sortKey="Senaati, Hp" uniqKey="Senaati H">HP Senaati</name></author><author><name sortKey="Chen, H W" uniqKey="Chen H">H-W Chen</name></author><author><name sortKey="Varki, Nm" uniqKey="Varki N">NM Varki</name></author><author><name sortKey="Schooley, Rt" uniqKey="Schooley R">RT Schooley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ito, T" uniqKey="Ito T">T Ito</name></author><author><name sortKey="Kawaoka, Y" uniqKey="Kawaoka Y">Y Kawaoka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Russell, Rj" uniqKey="Russell R">RJ Russell</name></author><author><name sortKey="Stevens, Dj" uniqKey="Stevens D">DJ Stevens</name></author><author><name sortKey="Haire, Lf" uniqKey="Haire L">LF Haire</name></author><author><name sortKey="Gamblin, Sj" uniqKey="Gamblin S">SJ Gamblin</name></author><author><name sortKey="Skehel, Jj" uniqKey="Skehel J">JJ Skehel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Connor, Rj" uniqKey="Connor R">RJ Connor</name></author><author><name sortKey="Kawaoka, Y" uniqKey="Kawaoka Y">Y Kawaoka</name></author><author><name sortKey="Webster, Rg" uniqKey="Webster R">RG Webster</name></author><author><name sortKey="Paulson, Jc" uniqKey="Paulson J">JC Paulson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Matrosovich, M" uniqKey="Matrosovich M">M Matrosovich</name></author><author><name sortKey="Tuzikov, A" uniqKey="Tuzikov A">A Tuzikov</name></author><author><name sortKey="Bovin, N" uniqKey="Bovin N">N Bovin</name></author><author><name sortKey="Gambaryan, A" uniqKey="Gambaryan A">A Gambaryan</name></author><author><name sortKey="Klimov, A" uniqKey="Klimov A">A Klimov</name></author><author><name sortKey="Castrucci, Mr" uniqKey="Castrucci M">MR Castrucci</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stevens, J" uniqKey="Stevens J">J Stevens</name></author><author><name sortKey="Blixt, O" uniqKey="Blixt O">O Blixt</name></author><author><name sortKey="Glaser, L" uniqKey="Glaser L">L Glaser</name></author><author><name sortKey="Taubenberger, Jk" uniqKey="Taubenberger J">JK Taubenberger</name></author><author><name sortKey="Palese, P" uniqKey="Palese P">P Palese</name></author><author><name sortKey="Paulson, Jc" uniqKey="Paulson J">JC Paulson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wasik, Br" uniqKey="Wasik B">BR Wasik</name></author><author><name sortKey="Barnard, Kn" uniqKey="Barnard K">KN Barnard</name></author><author><name sortKey="Parrish, Cr" uniqKey="Parrish C">CR Parrish</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Peng, W" uniqKey="Peng W">W Peng</name></author><author><name sortKey="De Vries, Rp" uniqKey="De Vries R">RP de Vries</name></author><author><name sortKey="Grant, Oc" uniqKey="Grant O">OC Grant</name></author><author><name sortKey="Thompson, Aj" uniqKey="Thompson A">AJ Thompson</name></author><author><name sortKey="Mcbride, R" uniqKey="Mcbride R">R McBride</name></author><author><name sortKey="Tsogtbaatar, B" uniqKey="Tsogtbaatar B">B Tsogtbaatar</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="De Vries, Rp" uniqKey="De Vries R">RP de Vries</name></author><author><name sortKey="De Vries, E" uniqKey="De Vries E">E de Vries</name></author><author><name sortKey="Moore, Ks" uniqKey="Moore K">KS Moore</name></author><author><name sortKey="Rigter, A" uniqKey="Rigter A">A Rigter</name></author><author><name sortKey="Rottier, Pj" uniqKey="Rottier P">PJ Rottier</name></author><author><name sortKey="De Haan, Ca" uniqKey="De Haan C">CA de Haan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Guo, H" uniqKey="Guo H">H Guo</name></author><author><name sortKey="De Vries, E" uniqKey="De Vries E">E de Vries</name></author><author><name sortKey="Mcbride, R" uniqKey="Mcbride R">R McBride</name></author><author><name sortKey="Dekkers, J" uniqKey="Dekkers J">J Dekkers</name></author><author><name sortKey="Peng, W" uniqKey="Peng W">W Peng</name></author><author><name sortKey="Bouwman, Km" uniqKey="Bouwman K">KM Bouwman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gambaryan, A" uniqKey="Gambaryan A">A Gambaryan</name></author><author><name sortKey="Yamnikova, S" uniqKey="Yamnikova S">S Yamnikova</name></author><author><name sortKey="Lvov, D" uniqKey="Lvov D">D Lvov</name></author><author><name sortKey="Tuzikov, A" uniqKey="Tuzikov A">A Tuzikov</name></author><author><name sortKey="Chinarev, A" uniqKey="Chinarev A">A Chinarev</name></author><author><name sortKey="Pazynina, G" uniqKey="Pazynina G">G Pazynina</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tumpey, Tm" uniqKey="Tumpey T">TM Tumpey</name></author><author><name sortKey="Maines, Tr" uniqKey="Maines T">TR Maines</name></author><author><name sortKey="Van Hoeven, N" uniqKey="Van Hoeven N">N Van Hoeven</name></author><author><name sortKey="Glaser, L" uniqKey="Glaser L">L Glaser</name></author><author><name sortKey="Sol Rzano, A" uniqKey="Sol Rzano A">A Solórzano</name></author><author><name sortKey="Pappas, C" uniqKey="Pappas C">C Pappas</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Saito, T" uniqKey="Saito T">T Saito</name></author><author><name sortKey="Taylor, G" uniqKey="Taylor G">G Taylor</name></author><author><name sortKey="Webster, Rg" uniqKey="Webster R">RG Webster</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dai, M" uniqKey="Dai M">M Dai</name></author><author><name sortKey="Guo, H" uniqKey="Guo H">H Guo</name></author><author><name sortKey="Dortmans, Jc" uniqKey="Dortmans J">JC Dortmans</name></author><author><name sortKey="Dekkers, J" uniqKey="Dekkers J">J Dekkers</name></author><author><name sortKey="Nordholm, J" uniqKey="Nordholm J">J Nordholm</name></author><author><name sortKey="Daniels, R" uniqKey="Daniels R">R Daniels</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shtyrya, Ya" uniqKey="Shtyrya Y">YA Shtyrya</name></author><author><name sortKey="Mochalova, Lv" uniqKey="Mochalova L">LV Mochalova</name></author><author><name sortKey="Bovin, Nv" uniqKey="Bovin N">NV Bovin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Air, Gm" uniqKey="Air G">GM Air</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Russell, Rj" uniqKey="Russell R">RJ Russell</name></author><author><name sortKey="Haire, Lf" uniqKey="Haire L">LF Haire</name></author><author><name sortKey="Stevens, Dj" uniqKey="Stevens D">DJ Stevens</name></author><author><name sortKey="Collins, Pj" uniqKey="Collins P">PJ Collins</name></author><author><name sortKey="Lin, Yp" uniqKey="Lin Y">YP Lin</name></author><author><name sortKey="Blackburn, Gm" uniqKey="Blackburn G">GM Blackburn</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Baum, Lg" uniqKey="Baum L">LG Baum</name></author><author><name sortKey="Paulson, Jc" uniqKey="Paulson J">JC Paulson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, Y" uniqKey="Li Y">Y Li</name></author><author><name sortKey="Cao, H" uniqKey="Cao H">H Cao</name></author><author><name sortKey="Dao, N" uniqKey="Dao N">N Dao</name></author><author><name sortKey="Luo, Z" uniqKey="Luo Z">Z Luo</name></author><author><name sortKey="Yu, H" uniqKey="Yu H">H Yu</name></author><author><name sortKey="Chen, Y" uniqKey="Chen Y">Y Chen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Du, W" uniqKey="Du W">W Du</name></author><author><name sortKey="Dai, M" uniqKey="Dai M">M Dai</name></author><author><name sortKey="Li, Z" uniqKey="Li Z">Z Li</name></author><author><name sortKey="Boons, Gj" uniqKey="Boons G">GJ Boons</name></author><author><name sortKey="Peeters, B" uniqKey="Peeters B">B Peeters</name></author><author><name sortKey="Van Kuppeveld, Fjm" uniqKey="Van Kuppeveld F">FJM van Kuppeveld</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kobasa, D" uniqKey="Kobasa D">D Kobasa</name></author><author><name sortKey="Kodihalli, S" uniqKey="Kodihalli S">S Kodihalli</name></author><author><name sortKey="Luo, M" uniqKey="Luo M">M Luo</name></author><author><name sortKey="Castrucci, Mr" uniqKey="Castrucci M">MR Castrucci</name></author><author><name sortKey="Donatelli, I" uniqKey="Donatelli I">I Donatelli</name></author><author><name sortKey="Suzuki, Y" uniqKey="Suzuki Y">Y Suzuki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Uhlendorff, J" uniqKey="Uhlendorff J">J Uhlendorff</name></author><author><name sortKey="Matrosovich, T" uniqKey="Matrosovich T">T Matrosovich</name></author><author><name sortKey="Klenk, Hd" uniqKey="Klenk H">HD Klenk</name></author><author><name sortKey="Matrosovich, M" uniqKey="Matrosovich M">M Matrosovich</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Varghese, Jn" uniqKey="Varghese J">JN Varghese</name></author><author><name sortKey="Colman, Pm" uniqKey="Colman P">PM Colman</name></author><author><name sortKey="Van Donkelaar, A" uniqKey="Van Donkelaar A">A van Donkelaar</name></author><author><name sortKey="Blick, Tj" uniqKey="Blick T">TJ Blick</name></author><author><name sortKey="Sahasrabudhe, A" uniqKey="Sahasrabudhe A">A Sahasrabudhe</name></author><author><name sortKey="Mckimm Breschkin, Jl" uniqKey="Mckimm Breschkin J">JL McKimm-Breschkin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sun, X" uniqKey="Sun X">X Sun</name></author><author><name sortKey="Li, Q" uniqKey="Li Q">Q Li</name></author><author><name sortKey="Wu, Y" uniqKey="Wu Y">Y Wu</name></author><author><name sortKey="Wang, M" uniqKey="Wang M">M Wang</name></author><author><name sortKey="Liu, Y" uniqKey="Liu Y">Y Liu</name></author><author><name sortKey="Qi, J" uniqKey="Qi J">J Qi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lai, Jc" uniqKey="Lai J">JC Lai</name></author><author><name sortKey="Garcia, Jm" uniqKey="Garcia J">JM Garcia</name></author><author><name sortKey="Dyason, Jc" uniqKey="Dyason J">JC Dyason</name></author><author><name sortKey="Bohm, R" uniqKey="Bohm R">R Bohm</name></author><author><name sortKey="Madge, Pd" uniqKey="Madge P">PD Madge</name></author><author><name sortKey="Rose, Fj" uniqKey="Rose F">FJ Rose</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nuss, Jm" uniqKey="Nuss J">JM Nuss</name></author><author><name sortKey="Air, Gm" uniqKey="Air G">GM Air</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dai, M" uniqKey="Dai M">M Dai</name></author><author><name sortKey="Mcbride, R" uniqKey="Mcbride R">R McBride</name></author><author><name sortKey="Dortmans, Jc" uniqKey="Dortmans J">JC Dortmans</name></author><author><name sortKey="Peng, W" uniqKey="Peng W">W Peng</name></author><author><name sortKey="Bakkers, Mj" uniqKey="Bakkers M">MJ Bakkers</name></author><author><name sortKey="De Groot, Rj" uniqKey="De Groot R">RJ de Groot</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kobasa, D" uniqKey="Kobasa D">D Kobasa</name></author><author><name sortKey="Rodgers, Me" uniqKey="Rodgers M">ME Rodgers</name></author><author><name sortKey="Wells, K" uniqKey="Wells K">K Wells</name></author><author><name sortKey="Kawaoka, Y" uniqKey="Kawaoka Y">Y Kawaoka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hausmann, J" uniqKey="Hausmann J">J Hausmann</name></author><author><name sortKey="Kretzschmar, E" uniqKey="Kretzschmar E">E Kretzschmar</name></author><author><name sortKey="Garten, W" uniqKey="Garten W">W Garten</name></author><author><name sortKey="Klenk, Hd" uniqKey="Klenk H">HD Klenk</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Matrosovich, Mn" uniqKey="Matrosovich M">MN Matrosovich</name></author><author><name sortKey="Krauss, S" uniqKey="Krauss S">S Krauss</name></author><author><name sortKey="Webster, Rg" uniqKey="Webster R">RG Webster</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Guo, H" uniqKey="Guo H">H Guo</name></author><author><name sortKey="Rabouw, H" uniqKey="Rabouw H">H Rabouw</name></author><author><name sortKey="Slomp, A" uniqKey="Slomp A">A Slomp</name></author><author><name sortKey="Dai, M" uniqKey="Dai M">M Dai</name></author><author><name sortKey="Van Der Vegt, F" uniqKey="Van Der Vegt F">F van der Vegt</name></author><author><name sortKey="Van Lent, Jwm" uniqKey="Van Lent J">JWM van Lent</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sauter, Nk" uniqKey="Sauter N">NK Sauter</name></author><author><name sortKey="Bednarski, Md" uniqKey="Bednarski M">MD Bednarski</name></author><author><name sortKey="Wurzburg, Ba" uniqKey="Wurzburg B">BA Wurzburg</name></author><author><name sortKey="Hanson, Je" uniqKey="Hanson J">JE Hanson</name></author><author><name sortKey="Whitesides, Gm" uniqKey="Whitesides G">GM Whitesides</name></author><author><name sortKey="Skehel, Jj" uniqKey="Skehel J">JJ Skehel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Takemoto, Dk" uniqKey="Takemoto D">DK Takemoto</name></author><author><name sortKey="Skehel, Jj" uniqKey="Skehel J">JJ Skehel</name></author><author><name sortKey="Wiley, Dc" uniqKey="Wiley D">DC Wiley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wu, Am" uniqKey="Wu A">AM Wu</name></author><author><name sortKey="Wu, Jh" uniqKey="Wu J">JH Wu</name></author><author><name sortKey="Tsai, Ms" uniqKey="Tsai M">MS Tsai</name></author><author><name sortKey="Yang, Z" uniqKey="Yang Z">Z Yang</name></author><author><name sortKey="Sharon, N" uniqKey="Sharon N">N Sharon</name></author><author><name sortKey="Herp, A" uniqKey="Herp A">A Herp</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sharma, V" uniqKey="Sharma V">V Sharma</name></author><author><name sortKey="Srinivas, Vr" uniqKey="Srinivas V">VR Srinivas</name></author><author><name sortKey="Adhikari, P" uniqKey="Adhikari P">P Adhikari</name></author><author><name sortKey="Vijayan, M" uniqKey="Vijayan M">M Vijayan</name></author><author><name sortKey="Surolia, A" uniqKey="Surolia A">A Surolia</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Geisler, C" uniqKey="Geisler C">C Geisler</name></author><author><name sortKey="Jarvis, Dl" uniqKey="Jarvis D">DL Jarvis</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shibuya, N" uniqKey="Shibuya N">N Shibuya</name></author><author><name sortKey="Goldstein, Ij" uniqKey="Goldstein I">IJ Goldstein</name></author><author><name sortKey="Broekaert, Wf" uniqKey="Broekaert W">WF Broekaert</name></author><author><name sortKey="Nsimba Lubaki, M" uniqKey="Nsimba Lubaki M">M Nsimba-Lubaki</name></author><author><name sortKey="Peeters, B" uniqKey="Peeters B">B Peeters</name></author><author><name sortKey="Peumans, Wj" uniqKey="Peumans W">WJ Peumans</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Baenziger, Ju" uniqKey="Baenziger J">JU Baenziger</name></author><author><name sortKey="Fiete, D" uniqKey="Fiete D">D Fiete</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Spik, G" uniqKey="Spik G">G Spik</name></author><author><name sortKey="Bayard, B" uniqKey="Bayard B">B Bayard</name></author><author><name sortKey="Fournet, B" uniqKey="Fournet B">B Fournet</name></author><author><name sortKey="Strecker, G" uniqKey="Strecker G">G Strecker</name></author><author><name sortKey="Bouquelet, S" uniqKey="Bouquelet S">S Bouquelet</name></author><author><name sortKey="Montreuil, J" uniqKey="Montreuil J">J Montreuil</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Von Bonsdorff, L" uniqKey="Von Bonsdorff L">L von Bonsdorff</name></author><author><name sortKey="Tolo, H" uniqKey="Tolo H">H Tölö</name></author><author><name sortKey="Lindeberg, E" uniqKey="Lindeberg E">E Lindeberg</name></author><author><name sortKey="Nyman, T" uniqKey="Nyman T">T Nyman</name></author><author><name sortKey="Harju, A" uniqKey="Harju A">A Harju</name></author><author><name sortKey="Parkkinen, J" uniqKey="Parkkinen J">J Parkkinen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lai, Jc" uniqKey="Lai J">JC Lai</name></author><author><name sortKey="Chan, Ww" uniqKey="Chan W">WW Chan</name></author><author><name sortKey="Kien, F" uniqKey="Kien F">F Kien</name></author><author><name sortKey="Nicholls, Jm" uniqKey="Nicholls J">JM Nicholls</name></author><author><name sortKey="Peiris, Js" uniqKey="Peiris J">JS Peiris</name></author><author><name sortKey="Garcia, Jm" uniqKey="Garcia J">JM Garcia</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Del Piccolo, N" uniqKey="Del Piccolo N">N Del Piccolo</name></author><author><name sortKey="Placone, J" uniqKey="Placone J">J Placone</name></author><author><name sortKey="He, L" uniqKey="He L">L He</name></author><author><name sortKey="Agudelo, Sc" uniqKey="Agudelo S">SC Agudelo</name></author><author><name sortKey="Hristova, K" uniqKey="Hristova K">K Hristova</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hatakeyama, S" uniqKey="Hatakeyama S">S Hatakeyama</name></author><author><name sortKey="Sakai Tagawa, Y" uniqKey="Sakai Tagawa Y">Y Sakai-Tagawa</name></author><author><name sortKey="Kiso, M" uniqKey="Kiso M">M Kiso</name></author><author><name sortKey="Goto, H" uniqKey="Goto H">H Goto</name></author><author><name sortKey="Kawakami, C" uniqKey="Kawakami C">C Kawakami</name></author><author><name sortKey="Mitamura, K" uniqKey="Mitamura K">K Mitamura</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Govorkova, Ea" uniqKey="Govorkova E">EA Govorkova</name></author><author><name sortKey="Murti, G" uniqKey="Murti G">G Murti</name></author><author><name sortKey="Meignier, B" uniqKey="Meignier B">B Meignier</name></author><author><name sortKey="De Taisne, C" uniqKey="De Taisne C">C de Taisne</name></author><author><name sortKey="Webster, Rg" uniqKey="Webster R">RG Webster</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Carlsson, Sr" uniqKey="Carlsson S">SR Carlsson</name></author><author><name sortKey="Lycksell, Po" uniqKey="Lycksell P">PO Lycksell</name></author><author><name sortKey="Fukuda, M" uniqKey="Fukuda M">M Fukuda</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Carlsson, Sr" uniqKey="Carlsson S">SR Carlsson</name></author><author><name sortKey="Roth, J" uniqKey="Roth J">J Roth</name></author><author><name sortKey="Piller, F" uniqKey="Piller F">F Piller</name></author><author><name sortKey="Fukuda, M" uniqKey="Fukuda M">M Fukuda</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yoshima, H" uniqKey="Yoshima H">H Yoshima</name></author><author><name sortKey="Furthmayr, H" uniqKey="Furthmayr H">H Furthmayr</name></author><author><name sortKey="Kobata, A" uniqKey="Kobata A">A Kobata</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zdebska, E" uniqKey="Zdebska E">E Zdebska</name></author><author><name sortKey="Koscielak, J" uniqKey="Koscielak J">J Koscielak</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Van Poucke, S" uniqKey="Van Poucke S">S Van Poucke</name></author><author><name sortKey="Doedt, J" uniqKey="Doedt J">J Doedt</name></author><author><name sortKey="Baumann, J" uniqKey="Baumann J">J Baumann</name></author><author><name sortKey="Qiu, Y" uniqKey="Qiu Y">Y Qiu</name></author><author><name sortKey="Matrosovich, T" uniqKey="Matrosovich T">T Matrosovich</name></author><author><name sortKey="Klenk, Hd" uniqKey="Klenk H">HD Klenk</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Matrosovich, M" uniqKey="Matrosovich M">M Matrosovich</name></author><author><name sortKey="Matrosovich, T" uniqKey="Matrosovich T">T Matrosovich</name></author><author><name sortKey="Uhlendorff, J" uniqKey="Uhlendorff J">J Uhlendorff</name></author><author><name sortKey="Garten, W" uniqKey="Garten W">W Garten</name></author><author><name sortKey="Klenk, Hd" uniqKey="Klenk H">HD Klenk</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Laver, Wg" uniqKey="Laver W">WG Laver</name></author><author><name sortKey="Colman, Pm" uniqKey="Colman P">PM Colman</name></author><author><name sortKey="Webster, Rg" uniqKey="Webster R">RG Webster</name></author><author><name sortKey="Hinshaw, Vs" uniqKey="Hinshaw V">VS Hinshaw</name></author><author><name sortKey="Air, Gm" uniqKey="Air G">GM Air</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Benton, Dj" uniqKey="Benton D">DJ Benton</name></author><author><name sortKey="Wharton, Sa" uniqKey="Wharton S">SA Wharton</name></author><author><name sortKey="Martin, Sr" uniqKey="Martin S">SR Martin</name></author><author><name sortKey="Mccauley, Jw" uniqKey="Mccauley J">JW McCauley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lin, Yp" uniqKey="Lin Y">YP Lin</name></author><author><name sortKey="Gregory, V" uniqKey="Gregory V">V Gregory</name></author><author><name sortKey="Collins, P" uniqKey="Collins P">P Collins</name></author><author><name sortKey="Kloess, J" uniqKey="Kloess J">J Kloess</name></author><author><name sortKey="Wharton, S" uniqKey="Wharton S">S Wharton</name></author><author><name sortKey="Cattle, N" uniqKey="Cattle N">N Cattle</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mogling, R" uniqKey="Mogling R">R Mogling</name></author><author><name sortKey="Richard, Mj" uniqKey="Richard M">MJ Richard</name></author><author><name sortKey="Vliet, Sv" uniqKey="Vliet S">SV Vliet</name></author><author><name sortKey="Beek, Rv" uniqKey="Beek R">RV Beek</name></author><author><name sortKey="Schrauwen, Eja" uniqKey="Schrauwen E">EJA Schrauwen</name></author><author><name sortKey="Spronken, Mi" uniqKey="Spronken M">MI Spronken</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lai, Jcc" uniqKey="Lai J">JCC Lai</name></author><author><name sortKey="Karunarathna, H" uniqKey="Karunarathna H">H Karunarathna</name></author><author><name sortKey="Wong, Hh" uniqKey="Wong H">HH Wong</name></author><author><name sortKey="Peiris, Jsm" uniqKey="Peiris J">JSM Peiris</name></author><author><name sortKey="Nicholls, Jm" uniqKey="Nicholls J">JM Nicholls</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Webster, Rg" uniqKey="Webster R">RG Webster</name></author><author><name sortKey="Air, Gm" uniqKey="Air G">GM Air</name></author><author><name sortKey="Metzger, Dw" uniqKey="Metzger D">DW Metzger</name></author><author><name sortKey="Colman, Pm" uniqKey="Colman P">PM Colman</name></author><author><name sortKey="Varghese, Jn" uniqKey="Varghese J">JN Varghese</name></author><author><name sortKey="Baker, At" uniqKey="Baker A">AT Baker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bakkers, Mj" uniqKey="Bakkers M">MJ Bakkers</name></author><author><name sortKey="Lang, Y" uniqKey="Lang Y">Y Lang</name></author><author><name sortKey="Feitsma, Lj" uniqKey="Feitsma L">LJ Feitsma</name></author><author><name sortKey="Hulswit, Rj" uniqKey="Hulswit R">RJ Hulswit</name></author><author><name sortKey="De Poot, Sa" uniqKey="De Poot S">SA de Poot</name></author><author><name sortKey="Van Vliet, Al" uniqKey="Van Vliet A">AL van Vliet</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cornelissen, La" uniqKey="Cornelissen L">LA Cornelissen</name></author><author><name sortKey="De Vries, Rp" uniqKey="De Vries R">RP de Vries</name></author><author><name sortKey="De Boer Luijtze, Ea" uniqKey="De Boer Luijtze E">EA de Boer-Luijtze</name></author><author><name sortKey="Rigter, A" uniqKey="Rigter A">A Rigter</name></author><author><name sortKey="Rottier, Pj" uniqKey="Rottier P">PJ Rottier</name></author><author><name sortKey="De Haan, Ca" uniqKey="De Haan C">CA de Haan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Predonzani, A" uniqKey="Predonzani A">A Predonzani</name></author><author><name sortKey="Arnoldi, F" uniqKey="Arnoldi F">F Arnoldi</name></author><author><name sortKey="Lopez Requena, A" uniqKey="Lopez Requena A">A Lopez-Requena</name></author><author><name sortKey="Burrone, Or" uniqKey="Burrone O">OR Burrone</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="James, Kt" uniqKey="James K">KT James</name></author><author><name sortKey="Cooney, B" uniqKey="Cooney B">B Cooney</name></author><author><name sortKey="Agopsowicz, K" uniqKey="Agopsowicz K">K Agopsowicz</name></author><author><name sortKey="Trevors, Ma" uniqKey="Trevors M">MA Trevors</name></author><author><name sortKey="Mohamed, A" uniqKey="Mohamed A">A Mohamed</name></author><author><name sortKey="Stoltz, D" uniqKey="Stoltz D">D Stoltz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Potier, M" uniqKey="Potier M">M Potier</name></author><author><name sortKey="Mameli, L" uniqKey="Mameli L">L Mameli</name></author><author><name sortKey="Belisle, M" uniqKey="Belisle M">M Bélisle</name></author><author><name sortKey="Dallaire, L" uniqKey="Dallaire L">L Dallaire</name></author><author><name sortKey="Melancon, Sb" uniqKey="Melancon S">SB Melançon</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Matrosovich, M" uniqKey="Matrosovich M">M Matrosovich</name></author><author><name sortKey="Matrosovich, T" uniqKey="Matrosovich T">T Matrosovich</name></author><author><name sortKey="Garten, W" uniqKey="Garten W">W Garten</name></author><author><name sortKey="Klenk, Hd" uniqKey="Klenk H">HD Klenk</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Vavricka, Cj" uniqKey="Vavricka C">CJ Vavricka</name></author><author><name sortKey="Liu, Y" uniqKey="Liu Y">Y Liu</name></author><author><name sortKey="Kiyota, H" uniqKey="Kiyota H">H Kiyota</name></author><author><name sortKey="Sriwilaijaroen, N" uniqKey="Sriwilaijaroen N">N Sriwilaijaroen</name></author><author><name sortKey="Qi, J" uniqKey="Qi J">J Qi</name></author><author><name sortKey="Tanaka, K" uniqKey="Tanaka K">K Tanaka</name></author><author><name sortKey="Wu, Y" uniqKey="Wu Y">Y Wu</name></author><author><name sortKey="Li, Q" uniqKey="Li Q">Q Li</name></author><author><name sortKey="Li, Y" uniqKey="Li Y">Y Li</name></author><author><name sortKey="Yan, J" uniqKey="Yan J">J Yan</name></author><author><name sortKey="Suzuki, Y" uniqKey="Suzuki Y">Y Suzuki</name></author><author><name sortKey="Gao, Gf" uniqKey="Gao G">GF Gao</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Xu, J" uniqKey="Xu J">J Xu</name></author><author><name sortKey="Davis, Ct" uniqKey="Davis C">CT Davis</name></author><author><name sortKey="Christman, Mc" uniqKey="Christman M">MC Christman</name></author><author><name sortKey="Rivailler, P" uniqKey="Rivailler P">P Rivailler</name></author><author><name sortKey="Zhong, H" uniqKey="Zhong H">H Zhong</name></author><author><name sortKey="Donis, Ro" uniqKey="Donis R">RO Donis</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id><journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plospath</journal-id><journal-title-group><journal-title>PLoS Pathogens</journal-title></journal-title-group><issn pub-type="ppub">1553-7366</issn><issn pub-type="epub">1553-7374</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31181126</article-id><article-id pub-id-type="pmc">6586374</article-id><article-id pub-id-type="doi">10.1371/journal.ppat.1007860</article-id><article-id pub-id-type="publisher-id">PPATHOGENS-D-18-02468</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Eukaryota</subject><subj-group><subject>Animals</subject><subj-group><subject>Vertebrates</subject><subj-group><subject>Amniotes</subject><subj-group><subject>Birds</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Chemical Characterization</subject><subj-group><subject>Binding Analysis</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Lectins</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Virology</subject><subj-group><subject>Viral Structure</subject><subj-group><subject>Virions</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Virology</subject><subj-group><subject>Viral Replication</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Recombinant Proteins</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Chemical Characterization</subject><subj-group><subject>Binding Analysis</subject><subj-group><subject>Receptor Binding Assays</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>The 2<sup>nd</sup> sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance</article-title><alt-title alt-title-type="running-head">Role for 2<sup>nd</sup> SIA-binding site of IAV NA in HA-NA-receptor balance</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Du</surname><given-names>Wenjuan</given-names></name><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Visualization</role><role content-type="http://credit.casrai.org/">Writing – original draft</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Guo</surname><given-names>Hongbo</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Nijman</surname><given-names>Vera S.</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Doedt</surname><given-names>Jennifer</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="author-notes" rid="currentaff001"><sup>¤</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-8528-2585</contrib-id><name><surname>van der Vries</surname><given-names>Erhard</given-names></name><role content-type="http://credit.casrai.org/">Resources</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>van der Lee</surname><given-names>Joline</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-8358-3162</contrib-id><name><surname>Li</surname><given-names>Zeshi</given-names></name><role content-type="http://credit.casrai.org/">Resources</role><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-3111-5954</contrib-id><name><surname>Boons</surname><given-names>Geert-Jan</given-names></name><role content-type="http://credit.casrai.org/">Resources</role><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>van Kuppeveld</surname><given-names>Frank J. M.</given-names></name><role content-type="http://credit.casrai.org/">Resources</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>de Vries</surname><given-names>Erik</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-1618-2083</contrib-id><name><surname>Matrosovich</surname><given-names>Mikhail</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-4459-9874</contrib-id><name><surname>de Haan</surname><given-names>Cornelis A. M.</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Funding acquisition</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Writing – original draft</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Institute of Virology, Philipps University, Marburg, Germany</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht, the Netherlands</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Krammer</surname><given-names>Florian</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Icahn School of Medicine at Mount Sinai, UNITED STATES</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="current-aff" id="currentaff001"><label>¤</label><p>Current address: Sividon Diagnostics GmbH, Cologne, Germany.</p></fn><corresp id="cor001">* E-mail: <email>m.matrosovich@gmail.com</email> (MM); <email>c.a.m.dehaan@uu.nl</email> (CAMdH)</corresp></author-notes><pub-date pub-type="epub"><day>10</day><month>6</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>6</month><year>2019</year></pub-date><volume>15</volume><issue>6</issue><elocation-id>e1007860</elocation-id><history><date date-type="received"><day>3</day><month>1</month><year>2019</year></date><date date-type="accepted"><day>22</day><month>5</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 Du et al</copyright-statement><copyright-year>2019</copyright-year><copyright-holder>Du et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="ppat.1007860.pdf"></self-uri><abstract><p>Influenza A virus (IAV) neuraminidase (NA) receptor-destroying activity and hemagglutinin (HA) receptor-binding affinity need to be balanced with the host receptor repertoire for optimal viral fitness. NAs of avian, but not human viruses, contain a functional 2<sup>nd</sup> sialic acid (SIA)-binding site (2SBS) adjacent to the catalytic site, which contributes to sialidase activity against multivalent substrates. The receptor-binding specificity and potentially crucial contribution of the 2SBS to the HA-NA balance of virus particles is, however, poorly characterized. Here, we elucidated the receptor-binding specificity of the 2SBS of N2 NA and established an important role for this site in the virion HA-NA-receptor balance. NAs of H2N2/1957 pandemic virus with or without a functional 2SBS and viruses containing this NA were analysed. Avian-like N2, with a restored 2SBS due to an amino acid substitution at position 367, was more active than human N2 on multivalent substrates containing α2,3-linked SIAs, corresponding with the pronounced binding-specificity of avian-like N2 for these receptors. When introduced into human viruses, avian-like N2 gave rise to altered plaque morphology and decreased replication compared to human N2. An opposite replication phenotype was observed when N2 was combined with avian-like HA. Specific bio-layer interferometry assays revealed a clear effect of the 2SBS on the dynamic interaction of virus particles with receptors. The absence or presence of a functional 2SBS affected virion-receptor binding and receptor cleavage required for particle movement on a receptor-coated surface and subsequent NA-dependent self-elution. The contribution of the 2SBS to virus-receptor interactions depended on the receptor-binding properties of HA and the identity of the receptors used. We conclude that the 2SBS is an important and underappreciated determinant of the HA-NA-receptor balance. The rapid loss of a functional 2SBS in pandemic viruses may have served to balance the novel host receptor-repertoire and altered receptor-binding properties of the corresponding HA protein.</p></abstract><abstract abstract-type="summary"><title>Author summary</title><p>Influenza A viruses infect birds and mammals. They contain receptor-binding (HA) and receptor-destroying (NA) proteins, which are crucial determinants of host tropism and pathogenesis. It is generally accepted that the functional properties of HA and NA need to be well balanced to enable virion penetration of the receptor-rich mucus layer, binding to host cells, and release of newly assembled particles. This HA-NA-receptor balance is, however, poorly characterized resulting in part from a lack of suitable assays to measure this balance. In addition, NA is much less studied than HA. NA contains, besides its receptor-cleavage site, a 2<sup>nd</sup> receptor-binding site, which is functional in avian, but not in human viruses. We now show that this 2<sup>nd</sup> receptor-binding site prefers binding to avian-type receptors and promotes cleavage of substrates carrying this receptor. Furthermore, by using novel assays, we established an important role for this site in the HA-NA-receptor balance of virus particles as it contributes to receptor binding and cleavage by virions, the latter of which is required for virion movement and self-elution from receptors. The results may provide an explanation for the rapid loss of a functional 2<sup>nd</sup> receptor-binding site in human pandemic viruses.</p></abstract><funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100001659</institution-id><institution>Deutsche Forschungsgemeinschaft</institution></institution-wrap></funding-source><award-id>SFB 1021, project B02</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-1618-2083</contrib-id><name><surname>Matrosovich</surname><given-names>Mikhail</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution>Chinese Scholarship Council</institution></funding-source><award-id>201603250057</award-id><principal-award-recipient><name><surname>Du</surname><given-names>Wenjuan</given-names></name></principal-award-recipient></award-group><award-group id="award003"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100009578</institution-id><institution>Mizutani Foundation for Glycoscience</institution></institution-wrap></funding-source><award-id>180094</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-4459-9874</contrib-id><name><surname>de Haan</surname><given-names>Cornelis A. M.</given-names></name></principal-award-recipient></award-group><award-group id="award004"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100001663</institution-id><institution>Volkswagen Foundation</institution></institution-wrap></funding-source><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-8528-2585</contrib-id><name><surname>van der Vries</surname><given-names>Erhard</given-names></name></principal-award-recipient></award-group><funding-statement>W.D. was supported by a personal grant from the Chinese Scholarship Council (file number 201603250057). M.M. was supported by the German Research Foundation (DFG) (SFB 1021, project B02). E.v.d.V. was supported by a grant of the Volkswagen Foundation. C.A.M.d.H. was supported by the Mizutani Foundation for Glycoscience. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><fig-count count="6"></fig-count><table-count count="0"></table-count><page-count count="24"></page-count></counts><custom-meta-group><custom-meta><meta-name>PLOS Publication Stage</meta-name><meta-value>vor-update-to-uncorrected-proof</meta-value></custom-meta><custom-meta><meta-name>Publication Update</meta-name><meta-value>2019-06-20</meta-value></custom-meta><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the manuscript and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the manuscript and its Supporting Information files.</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
EXPLOR_STEP=$WICRI_ROOT/Sante/explor/H2N2V1/Data/Pmc/Curation
HfdSelect -h $EXPLOR_STEP/biblio.hfd -nk 000B94 | SxmlIndent | more
Ou
HfdSelect -h $EXPLOR_AREA/Data/Pmc/Curation/biblio.hfd -nk 000B94 | SxmlIndent | more
Pour mettre un lien sur cette page dans le réseau Wicri
{{Explor lien
|wiki= Sante
|area= H2N2V1
|flux= Pmc
|étape= Curation
|type= RBID
|clé= PMC:6586374
|texte= The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance
}}
Pour générer des pages wiki
HfdIndexSelect -h $EXPLOR_AREA/Data/Pmc/Curation/RBID.i -Sk "pubmed:31181126" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Pmc/Curation/biblio.hfd \
| NlmPubMed2Wicri -a H2N2V1
| This area was generated with Dilib version V0.6.33. |  |