The Influenza Virus Neuraminidase Protein Transmembrane and Head Domains Have Coevolved
Identifieur interne : 000659 ( Main/Exploration ); précédent : 000658; suivant : 000660The Influenza Virus Neuraminidase Protein Transmembrane and Head Domains Have Coevolved
Auteurs : Diogo V. Da Silva [Suède] ; Johan Nordholm [Suède] ; Dan Dou [Suède] ; Hao Wang [Suède] ; Jeremy S. Rossman [Royaume-Uni] ; Robert Daniels [Suède]Source :
- Journal of Virology [ 0022-538X ] ; 2014.
Abstract
Transmembrane domains (TMDs) from single-spanning membrane proteins are commonly viewed as membrane anchors for functional domains. Influenza virus neuraminidase (NA) exemplifies this concept, as it retains enzymatic function upon proteolytic release from the membrane. However, the subtype 1 NA TMDs have become increasingly more polar in human strains since 1918, which suggests that selection pressure exists on this domain. Here, we investigated the N1 TMD-head domain relationship by exchanging a prototypical “old” TMD (1933) with a “recent” (2009), more polar TMD and an engineered hydrophobic TMD. Each exchange altered the TMD association, decreased the NA folding efficiency, and significantly reduced viral budding and replication at 37°C compared to at 33°C, at which NA folds more efficiently. Passaging the chimera viruses at 37°C restored the NA folding efficiency, viral budding, and infectivity by selecting for NA TMD mutations that correspond with their polar or hydrophobic assembly properties. These results demonstrate that single-spanning membrane protein TMDs can influence distal domain folding, as well as membrane-related processes, and suggest the NA TMD in H1N1 viruses has become more polar to maintain compatibility with the evolving enzymatic head domain.
Url:
DOI: 10.1128/JVI.02005-14
PubMed: 25378494
PubMed Central: 4300628
Affiliations:
Links toward previous steps (curation, corpus...)
- to stream Pmc, to step Corpus: 000689
- to stream Pmc, to step Curation: 000689
- to stream Pmc, to step Checkpoint: 000446
- to stream Ncbi, to step Merge: 000A97
- to stream Ncbi, to step Curation: 000A97
- to stream Ncbi, to step Checkpoint: 000A97
- to stream Main, to step Merge: 000660
- to stream Main, to step Curation: 000659
Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The Influenza Virus Neuraminidase Protein Transmembrane and Head Domains Have Coevolved</title>
<author><name sortKey="Da Silva, Diogo V" sort="Da Silva, Diogo V" uniqKey="Da Silva D" first="Diogo V." last="Da Silva">Diogo V. Da Silva</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
<author><name sortKey="Nordholm, Johan" sort="Nordholm, Johan" uniqKey="Nordholm J" first="Johan" last="Nordholm">Johan Nordholm</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
<author><name sortKey="Dou, Dan" sort="Dou, Dan" uniqKey="Dou D" first="Dan" last="Dou">Dan Dou</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
<author><name sortKey="Wang, Hao" sort="Wang, Hao" uniqKey="Wang H" first="Hao" last="Wang">Hao Wang</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
<author><name sortKey="Rossman, Jeremy S" sort="Rossman, Jeremy S" uniqKey="Rossman J" first="Jeremy S." last="Rossman">Jeremy S. Rossman</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">School of Biosciences, University of Kent, Canterbury, United Kingdom</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>School of Biosciences, University of Kent, Canterbury</wicri:regionArea>
<wicri:noRegion>Canterbury</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Daniels, Robert" sort="Daniels, Robert" uniqKey="Daniels R" first="Robert" last="Daniels">Robert Daniels</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">25378494</idno>
<idno type="pmc">4300628</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4300628</idno>
<idno type="RBID">PMC:4300628</idno>
<idno type="doi">10.1128/JVI.02005-14</idno>
<date when="2014">2014</date>
<idno type="wicri:Area/Pmc/Corpus">000689</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000689</idno>
<idno type="wicri:Area/Pmc/Curation">000689</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000689</idno>
<idno type="wicri:Area/Pmc/Checkpoint">000446</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000446</idno>
<idno type="wicri:Area/Ncbi/Merge">000A97</idno>
<idno type="wicri:Area/Ncbi/Curation">000A97</idno>
<idno type="wicri:Area/Ncbi/Checkpoint">000A97</idno>
<idno type="wicri:doubleKey">0022-538X:2014:Da Silva D:the:influenza:virus</idno>
<idno type="wicri:Area/Main/Merge">000660</idno>
<idno type="wicri:Area/Main/Curation">000659</idno>
<idno type="wicri:Area/Main/Exploration">000659</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The Influenza Virus Neuraminidase Protein Transmembrane and Head Domains Have Coevolved</title>
<author><name sortKey="Da Silva, Diogo V" sort="Da Silva, Diogo V" uniqKey="Da Silva D" first="Diogo V." last="Da Silva">Diogo V. Da Silva</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
<author><name sortKey="Nordholm, Johan" sort="Nordholm, Johan" uniqKey="Nordholm J" first="Johan" last="Nordholm">Johan Nordholm</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
<author><name sortKey="Dou, Dan" sort="Dou, Dan" uniqKey="Dou D" first="Dan" last="Dou">Dan Dou</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
<author><name sortKey="Wang, Hao" sort="Wang, Hao" uniqKey="Wang H" first="Hao" last="Wang">Hao Wang</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
<author><name sortKey="Rossman, Jeremy S" sort="Rossman, Jeremy S" uniqKey="Rossman J" first="Jeremy S." last="Rossman">Jeremy S. Rossman</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">School of Biosciences, University of Kent, Canterbury, United Kingdom</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>School of Biosciences, University of Kent, Canterbury</wicri:regionArea>
<wicri:noRegion>Canterbury</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Daniels, Robert" sort="Daniels, Robert" uniqKey="Daniels R" first="Robert" last="Daniels">Robert Daniels</name>
<affiliation wicri:level="4"><nlm:aff id="aff1">Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Center for Biomembrane Research, Department of Biochemistry and Biophysics, Stockholm University, Stockholm</wicri:regionArea>
<placeName><settlement type="city">Stockholm</settlement>
<region nuts="2">Svealand</region>
</placeName>
<orgName type="university">Université de Stockholm</orgName>
</affiliation>
</author>
</analytic>
<series><title level="j">Journal of Virology</title>
<idno type="ISSN">0022-538X</idno>
<idno type="eISSN">1098-5514</idno>
<imprint><date when="2014">2014</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>Transmembrane domains (TMDs) from single-spanning membrane proteins are commonly viewed as membrane anchors for functional domains. Influenza virus neuraminidase (NA) exemplifies this concept, as it retains enzymatic function upon proteolytic release from the membrane. However, the subtype 1 NA TMDs have become increasingly more polar in human strains since 1918, which suggests that selection pressure exists on this domain. Here, we investigated the N1 TMD-head domain relationship by exchanging a prototypical “old” TMD (1933) with a “recent” (2009), more polar TMD and an engineered hydrophobic TMD. Each exchange altered the TMD association, decreased the NA folding efficiency, and significantly reduced viral budding and replication at 37°C compared to at 33°C, at which NA folds more efficiently. Passaging the chimera viruses at 37°C restored the NA folding efficiency, viral budding, and infectivity by selecting for NA TMD mutations that correspond with their polar or hydrophobic assembly properties. These results demonstrate that single-spanning membrane protein TMDs can influence distal domain folding, as well as membrane-related processes, and suggest the NA TMD in H1N1 viruses has become more polar to maintain compatibility with the evolving enzymatic head domain.</p>
<p><bold>IMPORTANCE</bold>
The neuraminidase (NA) protein from influenza A viruses (IAVs) functions to promote viral release and is one of the major surface antigens. The receptor-destroying activity in NA resides in the distal head domain that is linked to the viral membrane by an N-terminal hydrophobic transmembrane domain (TMD). Over the last century, the subtype 1 NA TMDs (N1) in human H1N1 viruses have become increasingly more polar, and the head domains have changed to alter their antigenicity. Here, we provide the first evidence that an “old” N1 head domain from 1933 is incompatible with a “recent” (2009), more polar N1 TMD sequence and that, during viral replication, the head domain drives the selection of TMD mutations. These mutations modify the intrinsic TMD assembly to restore the head domain folding compatibility and the resultant budding deficiency. This likely explains why the N1 TMDs have become more polar and suggests the N1 TMD and head domain have coevolved.</p>
</div>
</front>
</TEI>
<affiliations><list><country><li>Royaume-Uni</li>
<li>Suède</li>
</country>
<region><li>Svealand</li>
</region>
<settlement><li>Stockholm</li>
</settlement>
<orgName><li>Université de Stockholm</li>
</orgName>
</list>
<tree><country name="Suède"><region name="Svealand"><name sortKey="Da Silva, Diogo V" sort="Da Silva, Diogo V" uniqKey="Da Silva D" first="Diogo V." last="Da Silva">Diogo V. Da Silva</name>
</region>
<name sortKey="Daniels, Robert" sort="Daniels, Robert" uniqKey="Daniels R" first="Robert" last="Daniels">Robert Daniels</name>
<name sortKey="Dou, Dan" sort="Dou, Dan" uniqKey="Dou D" first="Dan" last="Dou">Dan Dou</name>
<name sortKey="Nordholm, Johan" sort="Nordholm, Johan" uniqKey="Nordholm J" first="Johan" last="Nordholm">Johan Nordholm</name>
<name sortKey="Wang, Hao" sort="Wang, Hao" uniqKey="Wang H" first="Hao" last="Wang">Hao Wang</name>
</country>
<country name="Royaume-Uni"><noRegion><name sortKey="Rossman, Jeremy S" sort="Rossman, Jeremy S" uniqKey="Rossman J" first="Jeremy S." last="Rossman">Jeremy S. Rossman</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
Pour manipuler ce document sous Unix (Dilib)
EXPLOR_STEP=$WICRI_ROOT/Sante/explor/H2N2V1/Data/Main/Exploration
HfdSelect -h $EXPLOR_STEP/biblio.hfd -nk 000659 | SxmlIndent | more
Ou
HfdSelect -h $EXPLOR_AREA/Data/Main/Exploration/biblio.hfd -nk 000659 | SxmlIndent | more
Pour mettre un lien sur cette page dans le réseau Wicri
{{Explor lien |wiki= Sante |area= H2N2V1 |flux= Main |étape= Exploration |type= RBID |clé= PMC:4300628 |texte= The Influenza Virus Neuraminidase Protein Transmembrane and Head Domains Have Coevolved }}
Pour générer des pages wiki
HfdIndexSelect -h $EXPLOR_AREA/Data/Main/Exploration/RBID.i -Sk "pubmed:25378494" \ | HfdSelect -Kh $EXPLOR_AREA/Data/Main/Exploration/biblio.hfd \ | NlmPubMed2Wicri -a H2N2V1
This area was generated with Dilib version V0.6.33. |