Membrane alterations induced by nonstructural proteins of human norovirus.
Identifieur interne : 000346 ( PubMed/Curation ); précédent : 000345; suivant : 000347Membrane alterations induced by nonstructural proteins of human norovirus.
Auteurs : Sylvie Y. Doerflinger [Allemagne] ; Mirko Cortese [Allemagne] ; Inés Romero-Brey [Allemagne] ; Zach Menne [Allemagne] ; Thibault Tubiana [France] ; Christian Schenk [Allemagne] ; Peter A. White [Australie] ; Ralf Bartenschlager [Allemagne] ; Stéphane Bressanelli [France] ; Grant S. Hansman [Allemagne] ; Volker Lohmann [Allemagne]Source :
- PLoS pathogens [ 1553-7374 ] ; 2017.
Abstract
Human noroviruses (huNoV) are the most frequent cause of non-bacterial acute gastroenteritis worldwide, particularly genogroup II genotype 4 (GII.4) variants. The viral nonstructural (NS) proteins encoded by the ORF1 polyprotein induce vesical clusters harboring the viral replication sites. Little is known so far about the ultrastructure of these replication organelles or the contribution of individual NS proteins to their biogenesis. We compared the ultrastructural changes induced by expression of norovirus ORF1 polyproteins with those induced upon infection with murine norovirus (MNV). Characteristic membrane alterations induced by ORF1 expression resembled those found in MNV infected cells, consisting of vesicle accumulations likely built from the endoplasmic reticulum (ER) which included single membrane vesicles (SMVs), double membrane vesicles (DMVs) and multi membrane vesicles (MMVs). In-depth analysis using electron tomography suggested that MMVs originate through the enwrapping of SMVs with tubular structures similar to mechanisms reported for picornaviruses. Expression of GII.4 NS1-2, NS3 and NS4 fused to GFP revealed distinct membrane alterations when analyzed by correlative light and electron microscopy. Expression of NS1-2 induced proliferation of smooth ER membranes forming long tubular structures that were affected by mutations in the active center of the putative NS1-2 hydrolase domain. NS3 was associated with ER membranes around lipid droplets (LDs) and induced the formation of convoluted membranes, which were even more pronounced in case of NS4. Interestingly, NS4 was the only GII.4 protein capable of inducing SMV and DMV formation when expressed individually. Our work provides the first ultrastructural analysis of norovirus GII.4 induced vesicle clusters and suggests that their morphology and biogenesis is most similar to picornaviruses. We further identified NS4 as a key factor in the formation of membrane alterations of huNoV and provide models of the putative membrane topologies of NS1-2, NS3 and NS4 to guide future studies.
DOI: 10.1371/journal.ppat.1006705
PubMed: 29077760
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White</name><affiliation wicri:level="1"><nlm:affiliation>School of Biotechnology and Biomolecular Sciences, Faculty of Science, University of New South Wales, Sydney, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biotechnology and Biomolecular Sciences, Faculty of Science, University of New South Wales, Sydney</wicri:regionArea></affiliation></author><author><name sortKey="Bartenschlager, Ralf" sort="Bartenschlager, Ralf" uniqKey="Bartenschlager R" first="Ralf" last="Bartenschlager">Ralf Bartenschlager</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg</wicri:regionArea></affiliation></author><author><name sortKey="Bressanelli, Stephane" sort="Bressanelli, Stephane" uniqKey="Bressanelli S" first="Stéphane" last="Bressanelli">Stéphane Bressanelli</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ Paris Sud, Université Paris-Saclay, Gif sur Yvette cedex, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ Paris Sud, Université Paris-Saclay, Gif sur Yvette cedex</wicri:regionArea></affiliation></author><author><name sortKey="Hansman, Grant S" sort="Hansman, Grant S" uniqKey="Hansman G" first="Grant S" last="Hansman">Grant S. Hansman</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, Virology, Heidelberg University, Heidelberg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Infectious Diseases, Virology, Heidelberg University, Heidelberg</wicri:regionArea></affiliation></author><author><name sortKey="Lohmann, Volker" sort="Lohmann, Volker" uniqKey="Lohmann V" first="Volker" last="Lohmann">Volker Lohmann</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS pathogens</title><idno type="eISSN">1553-7374</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Human noroviruses (huNoV) are the most frequent cause of non-bacterial acute gastroenteritis worldwide, particularly genogroup II genotype 4 (GII.4) variants. The viral nonstructural (NS) proteins encoded by the ORF1 polyprotein induce vesical clusters harboring the viral replication sites. Little is known so far about the ultrastructure of these replication organelles or the contribution of individual NS proteins to their biogenesis. We compared the ultrastructural changes induced by expression of norovirus ORF1 polyproteins with those induced upon infection with murine norovirus (MNV). Characteristic membrane alterations induced by ORF1 expression resembled those found in MNV infected cells, consisting of vesicle accumulations likely built from the endoplasmic reticulum (ER) which included single membrane vesicles (SMVs), double membrane vesicles (DMVs) and multi membrane vesicles (MMVs). In-depth analysis using electron tomography suggested that MMVs originate through the enwrapping of SMVs with tubular structures similar to mechanisms reported for picornaviruses. Expression of GII.4 NS1-2, NS3 and NS4 fused to GFP revealed distinct membrane alterations when analyzed by correlative light and electron microscopy. Expression of NS1-2 induced proliferation of smooth ER membranes forming long tubular structures that were affected by mutations in the active center of the putative NS1-2 hydrolase domain. NS3 was associated with ER membranes around lipid droplets (LDs) and induced the formation of convoluted membranes, which were even more pronounced in case of NS4. Interestingly, NS4 was the only GII.4 protein capable of inducing SMV and DMV formation when expressed individually. Our work provides the first ultrastructural analysis of norovirus GII.4 induced vesicle clusters and suggests that their morphology and biogenesis is most similar to picornaviruses. We further identified NS4 as a key factor in the formation of membrane alterations of huNoV and provide models of the putative membrane topologies of NS1-2, NS3 and NS4 to guide future studies.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">29077760</PMID><DateCreated><Year>2017</Year><Month>10</Month><Day>27</Day></DateCreated><DateRevised><Year>2017</Year><Month>11</Month><Day>18</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1553-7374</ISSN><JournalIssue CitedMedium="Internet"><Volume>13</Volume><Issue>10</Issue><PubDate><Year>2017</Year><Month>Oct</Month></PubDate></JournalIssue><Title>PLoS pathogens</Title><ISOAbbreviation>PLoS Pathog.</ISOAbbreviation></Journal><ArticleTitle>Membrane alterations induced by nonstructural proteins of human norovirus.</ArticleTitle><Pagination><MedlinePgn>e1006705</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.ppat.1006705</ELocationID><Abstract><AbstractText>Human noroviruses (huNoV) are the most frequent cause of non-bacterial acute gastroenteritis worldwide, particularly genogroup II genotype 4 (GII.4) variants. The viral nonstructural (NS) proteins encoded by the ORF1 polyprotein induce vesical clusters harboring the viral replication sites. Little is known so far about the ultrastructure of these replication organelles or the contribution of individual NS proteins to their biogenesis. We compared the ultrastructural changes induced by expression of norovirus ORF1 polyproteins with those induced upon infection with murine norovirus (MNV). Characteristic membrane alterations induced by ORF1 expression resembled those found in MNV infected cells, consisting of vesicle accumulations likely built from the endoplasmic reticulum (ER) which included single membrane vesicles (SMVs), double membrane vesicles (DMVs) and multi membrane vesicles (MMVs). In-depth analysis using electron tomography suggested that MMVs originate through the enwrapping of SMVs with tubular structures similar to mechanisms reported for picornaviruses. Expression of GII.4 NS1-2, NS3 and NS4 fused to GFP revealed distinct membrane alterations when analyzed by correlative light and electron microscopy. Expression of NS1-2 induced proliferation of smooth ER membranes forming long tubular structures that were affected by mutations in the active center of the putative NS1-2 hydrolase domain. NS3 was associated with ER membranes around lipid droplets (LDs) and induced the formation of convoluted membranes, which were even more pronounced in case of NS4. Interestingly, NS4 was the only GII.4 protein capable of inducing SMV and DMV formation when expressed individually. Our work provides the first ultrastructural analysis of norovirus GII.4 induced vesicle clusters and suggests that their morphology and biogenesis is most similar to picornaviruses. We further identified NS4 as a key factor in the formation of membrane alterations of huNoV and provide models of the putative membrane topologies of NS1-2, NS3 and NS4 to guide future studies.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Doerflinger</LastName><ForeName>Sylvie Y</ForeName><Initials>SY</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Virology, Heidelberg University, Heidelberg, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Schaller Research Group at the University of Heidelberg and the DKFZ, Heidelberg, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cortese</LastName><ForeName>Mirko</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Romero-Brey</LastName><ForeName>Inés</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Menne</LastName><ForeName>Zach</ForeName><Initials>Z</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-0723-8981</Identifier><AffiliationInfo><Affiliation>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tubiana</LastName><ForeName>Thibault</ForeName><Initials>T</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-6490-4602</Identifier><AffiliationInfo><Affiliation>Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ Paris Sud, Université Paris-Saclay, Gif sur Yvette cedex, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schenk</LastName><ForeName>Christian</ForeName><Initials>C</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-7259-1135</Identifier><AffiliationInfo><Affiliation>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>White</LastName><ForeName>Peter A</ForeName><Initials>PA</Initials><AffiliationInfo><Affiliation>School of Biotechnology and Biomolecular Sciences, Faculty of Science, University of New South Wales, Sydney, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bartenschlager</LastName><ForeName>Ralf</ForeName><Initials>R</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-5601-9307</Identifier><AffiliationInfo><Affiliation>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>German Center for Infection Research (DZIF), Heidelberg University, Heidelberg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bressanelli</LastName><ForeName>Stéphane</ForeName><Initials>S</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-0921-6727</Identifier><AffiliationInfo><Affiliation>Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ Paris Sud, Université Paris-Saclay, Gif sur Yvette cedex, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hansman</LastName><ForeName>Grant S</ForeName><Initials>GS</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Virology, Heidelberg University, Heidelberg, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Schaller Research Group at the University of Heidelberg and the DKFZ, Heidelberg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lohmann</LastName><ForeName>Volker</ForeName><Initials>V</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-8719-7608</Identifier><AffiliationInfo><Affiliation>Department of Infectious Diseases, Molecular Virology, Heidelberg University, Im Neuenheimer Feld 345, Heidelberg, Germany.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2017</Year><Month>10</Month><Day>27</Day></ArticleDate></Article><MedlineJournalInfo><Country>United 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IdType="doi">10.1371/journal.ppat.1006705</ArticleId><ArticleId IdType="pii">PPATHOGENS-D-17-00937</ArticleId><ArticleId IdType="pmc">PMC5678787</ArticleId></ArticleIdList></PubmedData></pubmed></record>Pour manipuler ce document sous Unix (Dilib)
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