The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance.
Identifieur interne : 000007 ( PubMed/Checkpoint ); précédent : 000006; suivant : 000008The 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 [ 1553-7374 ] ; 2019.
Descripteurs français
- KwdFr :
- Acide N-acétyl-neuraminique (génétique), Acide N-acétyl-neuraminique (métabolisme), Animaux, Cellules Vero, Cellules rénales canines Madin-Darby, Chiens, Humains, Protéines virales (), Protéines virales (génétique), Protéines virales (métabolisme), Récepteurs viraux (), Récepteurs viraux (génétique), Récepteurs viraux (métabolisme), Sialidase (), Sialidase (génétique), Sialidase (métabolisme), Sites de fixation, Sous-type H2N2 du virus de la grippe A (), Sous-type H2N2 du virus de la grippe A (génétique), Sous-type H2N2 du virus de la grippe A (métabolisme), Sous-type H3N2 du virus de la grippe A (), Sous-type H3N2 du virus de la grippe A (génétique), Sous-type H3N2 du virus de la grippe A (métabolisme), Virion (), Virion (génétique), Virion (métabolisme).
- MESH :
- génétique : Acide N-acétyl-neuraminique, Protéines virales, Récepteurs viraux, Sialidase, Sous-type H2N2 du virus de la grippe A, Sous-type H3N2 du virus de la grippe A, Virion.
- métabolisme : Acide N-acétyl-neuraminique, Protéines virales, Récepteurs viraux, Sialidase, Sous-type H2N2 du virus de la grippe A, Sous-type H3N2 du virus de la grippe A, Virion.
- Animaux, Cellules Vero, Cellules rénales canines Madin-Darby, Chiens, Humains, Protéines virales, Récepteurs viraux, Sialidase, Sites de fixation, Sous-type H2N2 du virus de la grippe A, Sous-type H3N2 du virus de la grippe A, Virion.
English descriptors
- KwdEn :
- Animals, Binding Sites, Chlorocebus aethiops, Dogs, Humans, Influenza A Virus, H2N2 Subtype (chemistry), Influenza A Virus, H2N2 Subtype (genetics), Influenza A Virus, H2N2 Subtype (metabolism), Influenza A Virus, H3N2 Subtype (chemistry), Influenza A Virus, H3N2 Subtype (genetics), Influenza A Virus, H3N2 Subtype (metabolism), Madin Darby Canine Kidney Cells, N-Acetylneuraminic Acid (genetics), N-Acetylneuraminic Acid (metabolism), Neuraminidase (chemistry), Neuraminidase (genetics), Neuraminidase (metabolism), Receptors, Virus (chemistry), Receptors, Virus (genetics), Receptors, Virus (metabolism), Vero Cells, Viral Proteins (chemistry), Viral Proteins (genetics), Viral Proteins (metabolism), Virion (chemistry), Virion (genetics), Virion (metabolism).
- MESH :
- chemical , chemistry : Neuraminidase, Receptors, Virus, Viral Proteins.
- chemical , genetics : N-Acetylneuraminic Acid, Neuraminidase, Receptors, Virus, Viral Proteins.
- chemistry : Influenza A Virus, H2N2 Subtype, Influenza A Virus, H3N2 Subtype, Virion.
- genetics : Influenza A Virus, H2N2 Subtype, Influenza A Virus, H3N2 Subtype, Virion.
- metabolism : Influenza A Virus, H2N2 Subtype, Influenza A Virus, H3N2 Subtype, N-Acetylneuraminic Acid, Neuraminidase, Receptors, Virus, Viral Proteins, Virion.
- Animals, Binding Sites, Chlorocebus aethiops, Dogs, Humans, Madin Darby Canine Kidney Cells, Vero Cells.
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.
DOI: 10.1371/journal.ppat.1007860
PubMed: 31181126
Affiliations:
- Allemagne, Pays-Bas
- District de Giessen, Hesse (Land), Utrecht (province)
- Marbourg, Utrecht
- Université d'Utrecht
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pubmed:31181126Le document en format XML
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<sourceDesc><biblStruct><analytic><title xml:lang="en">The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance.</title>
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<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>
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<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>
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<country xml:lang="fr">Pays-Bas</country>
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<author><name sortKey="Li, Zeshi" sort="Li, Zeshi" uniqKey="Li Z" first="Zeshi" last="Li">Zeshi Li</name>
<affiliation wicri:level="4"><nlm:affiliation>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht, the Netherlands.</nlm:affiliation>
<country xml:lang="fr" wicri:curation="lc">Pays-Bas</country>
<wicri:regionArea>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht</wicri:regionArea>
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</placeName>
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<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="4"><nlm:affiliation>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht, the Netherlands.</nlm:affiliation>
<country xml:lang="fr" wicri:curation="lc">Pays-Bas</country>
<wicri:regionArea>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht</wicri:regionArea>
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<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="4"><nlm:affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</nlm:affiliation>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea>
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<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="4"><nlm:affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</nlm:affiliation>
<country xml:lang="fr">Pays-Bas</country>
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<author><name sortKey="Matrosovich, Mikhail" sort="Matrosovich, Mikhail" uniqKey="Matrosovich M" first="Mikhail" last="Matrosovich">Mikhail Matrosovich</name>
<affiliation wicri:level="3"><nlm:affiliation>Institute of Virology, Philipps University, Marburg, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute of Virology, Philipps University, Marburg</wicri:regionArea>
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<region type="district" nuts="2">District de Giessen</region>
<settlement type="city">Marbourg</settlement>
</placeName>
</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="4"><nlm:affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</nlm:affiliation>
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<series><title level="j">PLoS pathogens</title>
<idno type="eISSN">1553-7374</idno>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term>
<term>Binding Sites</term>
<term>Chlorocebus aethiops</term>
<term>Dogs</term>
<term>Humans</term>
<term>Influenza A Virus, H2N2 Subtype (chemistry)</term>
<term>Influenza A Virus, H2N2 Subtype (genetics)</term>
<term>Influenza A Virus, H2N2 Subtype (metabolism)</term>
<term>Influenza A Virus, H3N2 Subtype (chemistry)</term>
<term>Influenza A Virus, H3N2 Subtype (genetics)</term>
<term>Influenza A Virus, H3N2 Subtype (metabolism)</term>
<term>Madin Darby Canine Kidney Cells</term>
<term>N-Acetylneuraminic Acid (genetics)</term>
<term>N-Acetylneuraminic Acid (metabolism)</term>
<term>Neuraminidase (chemistry)</term>
<term>Neuraminidase (genetics)</term>
<term>Neuraminidase (metabolism)</term>
<term>Receptors, Virus (chemistry)</term>
<term>Receptors, Virus (genetics)</term>
<term>Receptors, Virus (metabolism)</term>
<term>Vero Cells</term>
<term>Viral Proteins (chemistry)</term>
<term>Viral Proteins (genetics)</term>
<term>Viral Proteins (metabolism)</term>
<term>Virion (chemistry)</term>
<term>Virion (genetics)</term>
<term>Virion (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Acide N-acétyl-neuraminique (génétique)</term>
<term>Acide N-acétyl-neuraminique (métabolisme)</term>
<term>Animaux</term>
<term>Cellules Vero</term>
<term>Cellules rénales canines Madin-Darby</term>
<term>Chiens</term>
<term>Humains</term>
<term>Protéines virales ()</term>
<term>Protéines virales (génétique)</term>
<term>Protéines virales (métabolisme)</term>
<term>Récepteurs viraux ()</term>
<term>Récepteurs viraux (génétique)</term>
<term>Récepteurs viraux (métabolisme)</term>
<term>Sialidase ()</term>
<term>Sialidase (génétique)</term>
<term>Sialidase (métabolisme)</term>
<term>Sites de fixation</term>
<term>Sous-type H2N2 du virus de la grippe A ()</term>
<term>Sous-type H2N2 du virus de la grippe A (génétique)</term>
<term>Sous-type H2N2 du virus de la grippe A (métabolisme)</term>
<term>Sous-type H3N2 du virus de la grippe A ()</term>
<term>Sous-type H3N2 du virus de la grippe A (génétique)</term>
<term>Sous-type H3N2 du virus de la grippe A (métabolisme)</term>
<term>Virion ()</term>
<term>Virion (génétique)</term>
<term>Virion (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Neuraminidase</term>
<term>Receptors, Virus</term>
<term>Viral Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>N-Acetylneuraminic Acid</term>
<term>Neuraminidase</term>
<term>Receptors, Virus</term>
<term>Viral Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="chemistry" xml:lang="en"><term>Influenza A Virus, H2N2 Subtype</term>
<term>Influenza A Virus, H3N2 Subtype</term>
<term>Virion</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Influenza A Virus, H2N2 Subtype</term>
<term>Influenza A Virus, H3N2 Subtype</term>
<term>Virion</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Acide N-acétyl-neuraminique</term>
<term>Protéines virales</term>
<term>Récepteurs viraux</term>
<term>Sialidase</term>
<term>Sous-type H2N2 du virus de la grippe A</term>
<term>Sous-type H3N2 du virus de la grippe A</term>
<term>Virion</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Influenza A Virus, H2N2 Subtype</term>
<term>Influenza A Virus, H3N2 Subtype</term>
<term>N-Acetylneuraminic Acid</term>
<term>Neuraminidase</term>
<term>Receptors, Virus</term>
<term>Viral Proteins</term>
<term>Virion</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Acide N-acétyl-neuraminique</term>
<term>Protéines virales</term>
<term>Récepteurs viraux</term>
<term>Sialidase</term>
<term>Sous-type H2N2 du virus de la grippe A</term>
<term>Sous-type H3N2 du virus de la grippe A</term>
<term>Virion</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Animals</term>
<term>Binding Sites</term>
<term>Chlorocebus aethiops</term>
<term>Dogs</term>
<term>Humans</term>
<term>Madin Darby Canine Kidney Cells</term>
<term>Vero Cells</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Animaux</term>
<term>Cellules Vero</term>
<term>Cellules rénales canines Madin-Darby</term>
<term>Chiens</term>
<term>Humains</term>
<term>Protéines virales</term>
<term>Récepteurs viraux</term>
<term>Sialidase</term>
<term>Sites de fixation</term>
<term>Sous-type H2N2 du virus de la grippe A</term>
<term>Sous-type H3N2 du virus de la grippe A</term>
<term>Virion</term>
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<front><div type="abstract" xml:lang="en">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.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31181126</PMID>
<DateCompleted><Year>2019</Year>
<Month>12</Month>
<Day>02</Day>
</DateCompleted>
<DateRevised><Year>2020</Year>
<Month>03</Month>
<Day>09</Day>
</DateRevised>
<Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1553-7374</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>15</Volume>
<Issue>6</Issue>
<PubDate><Year>2019</Year>
<Month>06</Month>
</PubDate>
</JournalIssue>
<Title>PLoS pathogens</Title>
<ISOAbbreviation>PLoS Pathog.</ISOAbbreviation>
</Journal>
<ArticleTitle>The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance.</ArticleTitle>
<Pagination><MedlinePgn>e1007860</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.ppat.1007860</ELocationID>
<Abstract><AbstractText>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.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Du</LastName>
<ForeName>Wenjuan</ForeName>
<Initials>W</Initials>
<AffiliationInfo><Affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Guo</LastName>
<ForeName>Hongbo</ForeName>
<Initials>H</Initials>
<AffiliationInfo><Affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Nijman</LastName>
<ForeName>Vera S</ForeName>
<Initials>VS</Initials>
<AffiliationInfo><Affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Doedt</LastName>
<ForeName>Jennifer</ForeName>
<Initials>J</Initials>
<AffiliationInfo><Affiliation>Institute of Virology, Philipps University, Marburg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>van der Vries</LastName>
<ForeName>Erhard</ForeName>
<Initials>E</Initials>
<Identifier Source="ORCID">0000-0001-8528-2585</Identifier>
<AffiliationInfo><Affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>van der Lee</LastName>
<ForeName>Joline</ForeName>
<Initials>J</Initials>
<AffiliationInfo><Affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Li</LastName>
<ForeName>Zeshi</ForeName>
<Initials>Z</Initials>
<Identifier Source="ORCID">0000-0002-8358-3162</Identifier>
<AffiliationInfo><Affiliation>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht, the Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Boons</LastName>
<ForeName>Geert-Jan</ForeName>
<Initials>GJ</Initials>
<Identifier Source="ORCID">0000-0003-3111-5954</Identifier>
<AffiliationInfo><Affiliation>Department of Chemical Biology and Drug Discovery, Utrecht University, Utrecht, the Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>van Kuppeveld</LastName>
<ForeName>Frank J M</ForeName>
<Initials>FJM</Initials>
<AffiliationInfo><Affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>de Vries</LastName>
<ForeName>Erik</ForeName>
<Initials>E</Initials>
<AffiliationInfo><Affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Matrosovich</LastName>
<ForeName>Mikhail</ForeName>
<Initials>M</Initials>
<Identifier Source="ORCID">0000-0003-1618-2083</Identifier>
<AffiliationInfo><Affiliation>Institute of Virology, Philipps University, Marburg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>de Haan</LastName>
<ForeName>Cornelis A M</ForeName>
<Initials>CAM</Initials>
<Identifier Source="ORCID">0000-0002-4459-9874</Identifier>
<AffiliationInfo><Affiliation>Virology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2019</Year>
<Month>06</Month>
<Day>10</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>PLoS Pathog</MedlineTA>
<NlmUniqueID>101238921</NlmUniqueID>
<ISSNLinking>1553-7366</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011991">Receptors, Virus</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D014764">Viral Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>EC 3.2.1.18</RegistryNumber>
<NameOfSubstance UI="C487630">NA protein, influenza A virus</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>EC 3.2.1.18</RegistryNumber>
<NameOfSubstance UI="D009439">Neuraminidase</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>GZP2782OP0</RegistryNumber>
<NameOfSubstance UI="D019158">N-Acetylneuraminic Acid</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D001665" MajorTopicYN="N">Binding Sites</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002522" MajorTopicYN="N">Chlorocebus aethiops</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D004285" MajorTopicYN="N">Dogs</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D053121" MajorTopicYN="Y">Influenza A Virus, H2N2 Subtype</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D053122" MajorTopicYN="Y">Influenza A Virus, H3N2 Subtype</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D061985" MajorTopicYN="N">Madin Darby Canine Kidney Cells</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D019158" MajorTopicYN="N">N-Acetylneuraminic Acid</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D009439" MajorTopicYN="Y">Neuraminidase</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D011991" MajorTopicYN="Y">Receptors, Virus</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014709" MajorTopicYN="N">Vero Cells</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014764" MajorTopicYN="Y">Viral Proteins</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014771" MajorTopicYN="Y">Virion</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<CoiStatement>The authors have declared that no competing interests exist.</CoiStatement>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year>
<Month>01</Month>
<Day>03</Day>
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<PubMedPubDate PubStatus="accepted"><Year>2019</Year>
<Month>05</Month>
<Day>22</Day>
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<PubMedPubDate PubStatus="revised"><Year>2019</Year>
<Month>06</Month>
<Day>20</Day>
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<Month>6</Month>
<Day>11</Day>
<Hour>6</Hour>
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<Month>12</Month>
<Day>4</Day>
<Hour>6</Hour>
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