The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance.
Identifieur interne : 000008 ( PubMed/Corpus ); précédent : 000007; suivant : 000009The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance.
Auteurs : Wenjuan Du ; Hongbo Guo ; Vera S. Nijman ; Jennifer Doedt ; Erhard Van Der Vries ; Joline Van Der Lee ; Zeshi Li ; Geert-Jan Boons ; Frank J M. Van Kuppeveld ; Erik De Vries ; Mikhail Matrosovich ; Cornelis A M. De HaanSource :
- PLoS pathogens [ 1553-7374 ] ; 2019.
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
Links to Exploration step
pubmed:31181126Le document en format XML
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<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>
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<term>Neuraminidase (genetics)</term>
<term>Neuraminidase (metabolism)</term>
<term>Receptors, Virus (chemistry)</term>
<term>Receptors, Virus (genetics)</term>
<term>Receptors, Virus (metabolism)</term>
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<keywords scheme="MESH" qualifier="chemistry" xml:lang="en"><term>Influenza A Virus, H2N2 Subtype</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>
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<ArticleTitle>The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance.</ArticleTitle>
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<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>
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<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Du</LastName>
<ForeName>Wenjuan</ForeName>
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</AffiliationInfo>
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</AffiliationInfo>
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<ForeName>Erik</ForeName>
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</AffiliationInfo>
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<ForeName>Mikhail</ForeName>
<Initials>M</Initials>
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<AffiliationInfo><Affiliation>Institute of Virology, Philipps University, Marburg, Germany.</Affiliation>
</AffiliationInfo>
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<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>
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<Month>06</Month>
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