Infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes.
Identifieur interne : 001111 ( PubMed/Corpus ); précédent : 001110; suivant : 001112Infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes.
Auteurs : Helena J. Maier ; Philippa C. Hawes ; Eleanor M. Cottam ; Judith Mantell ; Paul Verkade ; Paul Monaghan ; Tom Wileman ; Paul BrittonSource :
- mBio [ 2150-7511 ] ; 2013.
English descriptors
- KwdEn :
- Animals, Cell Line, Chickens, Coronavirus Infections (veterinary), Coronavirus Infections (virology), Endoplasmic Reticulum (chemistry), Endoplasmic Reticulum (ultrastructure), Endoplasmic Reticulum (virology), Humans, Infectious bronchitis virus (genetics), Infectious bronchitis virus (physiology), Intracellular Membranes (chemistry), Intracellular Membranes (ultrastructure), Intracellular Membranes (virology), Poultry Diseases (virology), Virus Replication.
- MESH :
- chemistry : Endoplasmic Reticulum, Intracellular Membranes.
- genetics : Infectious bronchitis virus.
- physiology : Infectious bronchitis virus.
- ultrastructure : Endoplasmic Reticulum, Intracellular Membranes.
- veterinary : Coronavirus Infections.
- virology : Coronavirus Infections, Endoplasmic Reticulum, Intracellular Membranes, Poultry Diseases.
- Animals, Cell Line, Chickens, Humans, Virus Replication.
Abstract
Replication of positive-sense RNA viruses is associated with the rearrangement of cellular membranes. Previous work on the infection of tissue culture cell lines with the betacoronaviruses mouse hepatitis virus and severe acute respiratory syndrome coronavirus (SARS-CoV) showed that they generate double-membrane vesicles (DMVs) and convoluted membranes as part of a reticular membrane network. Here we describe a detailed study of the membrane rearrangements induced by the avian gammacoronavirus infectious bronchitis virus (IBV) in a mammalian cell line but also in primary avian cells and in epithelial cells of ex vivo tracheal organ cultures. In all cell types, structures novel to IBV infection were identified that we have termed zippered endoplasmic reticulum (ER) and spherules. Zippered ER lacked luminal space, suggesting zippering of ER cisternae, while spherules appeared as uniform invaginations of zippered ER. Electron tomography showed that IBV-induced spherules are tethered to the zippered ER and that there is a channel connecting the interior of the spherule with the cytoplasm, a feature thought to be necessary for sites of RNA synthesis but not seen previously for membrane rearrangements induced by coronaviruses. We also identified DMVs in IBV-infected cells that were observed as single individual DMVs or were connected to the ER via their outer membrane but not to the zippered ER. Interestingly, IBV-induced spherules strongly resemble confirmed sites of RNA synthesis for alphaviruses, nodaviruses, and bromoviruses, which may indicate similar strategies of IBV and these diverse viruses for the assembly of RNA replication complexes.
DOI: 10.1128/mBio.00801-13
PubMed: 24149513
Links to Exploration step
pubmed:24149513Le document en format XML
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Cottam</name></author><author><name sortKey="Mantell, Judith" sort="Mantell, Judith" uniqKey="Mantell J" first="Judith" last="Mantell">Judith Mantell</name></author><author><name sortKey="Verkade, Paul" sort="Verkade, Paul" uniqKey="Verkade P" first="Paul" last="Verkade">Paul Verkade</name></author><author><name sortKey="Monaghan, Paul" sort="Monaghan, Paul" uniqKey="Monaghan P" first="Paul" last="Monaghan">Paul Monaghan</name></author><author><name sortKey="Wileman, Tom" sort="Wileman, Tom" uniqKey="Wileman T" first="Tom" last="Wileman">Tom Wileman</name></author><author><name sortKey="Britton, Paul" sort="Britton, Paul" uniqKey="Britton P" first="Paul" last="Britton">Paul Britton</name></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2013">2013</date><idno type="RBID">pubmed:24149513</idno><idno type="pmid">24149513</idno><idno type="doi">10.1128/mBio.00801-13</idno><idno type="wicri:Area/PubMed/Corpus">001111</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">001111</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes.</title><author><name sortKey="Maier, Helena J" sort="Maier, Helena J" uniqKey="Maier H" first="Helena J" last="Maier">Helena J. Maier</name><affiliation><nlm:affiliation>The Pirbright Institute, Compton Laboratory, Compton, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Hawes, Philippa C" sort="Hawes, Philippa C" uniqKey="Hawes P" first="Philippa C" last="Hawes">Philippa C. Hawes</name></author><author><name sortKey="Cottam, Eleanor M" sort="Cottam, Eleanor M" uniqKey="Cottam E" first="Eleanor M" last="Cottam">Eleanor M. Cottam</name></author><author><name sortKey="Mantell, Judith" sort="Mantell, Judith" uniqKey="Mantell J" first="Judith" last="Mantell">Judith Mantell</name></author><author><name sortKey="Verkade, Paul" sort="Verkade, Paul" uniqKey="Verkade P" first="Paul" last="Verkade">Paul Verkade</name></author><author><name sortKey="Monaghan, Paul" sort="Monaghan, Paul" uniqKey="Monaghan P" first="Paul" last="Monaghan">Paul Monaghan</name></author><author><name sortKey="Wileman, Tom" sort="Wileman, Tom" uniqKey="Wileman T" first="Tom" last="Wileman">Tom Wileman</name></author><author><name sortKey="Britton, Paul" sort="Britton, Paul" uniqKey="Britton P" first="Paul" last="Britton">Paul Britton</name></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2013" type="published">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Cell Line</term><term>Chickens</term><term>Coronavirus Infections (veterinary)</term><term>Coronavirus Infections (virology)</term><term>Endoplasmic Reticulum (chemistry)</term><term>Endoplasmic Reticulum (ultrastructure)</term><term>Endoplasmic Reticulum (virology)</term><term>Humans</term><term>Infectious bronchitis virus (genetics)</term><term>Infectious bronchitis virus (physiology)</term><term>Intracellular Membranes (chemistry)</term><term>Intracellular Membranes (ultrastructure)</term><term>Intracellular Membranes (virology)</term><term>Poultry Diseases (virology)</term><term>Virus Replication</term></keywords><keywords scheme="MESH" qualifier="chemistry" xml:lang="en"><term>Endoplasmic Reticulum</term><term>Intracellular Membranes</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Infectious bronchitis virus</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Infectious bronchitis virus</term></keywords><keywords scheme="MESH" qualifier="ultrastructure" xml:lang="en"><term>Endoplasmic Reticulum</term><term>Intracellular Membranes</term></keywords><keywords scheme="MESH" qualifier="veterinary" xml:lang="en"><term>Coronavirus Infections</term></keywords><keywords scheme="MESH" qualifier="virology" xml:lang="en"><term>Coronavirus Infections</term><term>Endoplasmic Reticulum</term><term>Intracellular Membranes</term><term>Poultry Diseases</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Cell Line</term><term>Chickens</term><term>Humans</term><term>Virus Replication</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Replication of positive-sense RNA viruses is associated with the rearrangement of cellular membranes. Previous work on the infection of tissue culture cell lines with the betacoronaviruses mouse hepatitis virus and severe acute respiratory syndrome coronavirus (SARS-CoV) showed that they generate double-membrane vesicles (DMVs) and convoluted membranes as part of a reticular membrane network. Here we describe a detailed study of the membrane rearrangements induced by the avian gammacoronavirus infectious bronchitis virus (IBV) in a mammalian cell line but also in primary avian cells and in epithelial cells of ex vivo tracheal organ cultures. In all cell types, structures novel to IBV infection were identified that we have termed zippered endoplasmic reticulum (ER) and spherules. Zippered ER lacked luminal space, suggesting zippering of ER cisternae, while spherules appeared as uniform invaginations of zippered ER. Electron tomography showed that IBV-induced spherules are tethered to the zippered ER and that there is a channel connecting the interior of the spherule with the cytoplasm, a feature thought to be necessary for sites of RNA synthesis but not seen previously for membrane rearrangements induced by coronaviruses. We also identified DMVs in IBV-infected cells that were observed as single individual DMVs or were connected to the ER via their outer membrane but not to the zippered ER. Interestingly, IBV-induced spherules strongly resemble confirmed sites of RNA synthesis for alphaviruses, nodaviruses, and bromoviruses, which may indicate similar strategies of IBV and these diverse viruses for the assembly of RNA replication complexes.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">24149513</PMID><DateCompleted><Year>2014</Year><Month>04</Month><Day>07</Day></DateCompleted><DateRevised><Year>2019</Year><Month>12</Month><Day>27</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2150-7511</ISSN><JournalIssue CitedMedium="Internet"><Volume>4</Volume><Issue>5</Issue><PubDate><Year>2013</Year><Month>Oct</Month><Day>22</Day></PubDate></JournalIssue><Title>mBio</Title><ISOAbbreviation>mBio</ISOAbbreviation></Journal><ArticleTitle>Infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes.</ArticleTitle><Pagination><MedlinePgn>e00801-13</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1128/mBio.00801-13</ELocationID><ELocationID EIdType="pii" ValidYN="Y">e00801-13</ELocationID><Abstract><AbstractText Label="UNLABELLED">Replication of positive-sense RNA viruses is associated with the rearrangement of cellular membranes. Previous work on the infection of tissue culture cell lines with the betacoronaviruses mouse hepatitis virus and severe acute respiratory syndrome coronavirus (SARS-CoV) showed that they generate double-membrane vesicles (DMVs) and convoluted membranes as part of a reticular membrane network. Here we describe a detailed study of the membrane rearrangements induced by the avian gammacoronavirus infectious bronchitis virus (IBV) in a mammalian cell line but also in primary avian cells and in epithelial cells of ex vivo tracheal organ cultures. In all cell types, structures novel to IBV infection were identified that we have termed zippered endoplasmic reticulum (ER) and spherules. Zippered ER lacked luminal space, suggesting zippering of ER cisternae, while spherules appeared as uniform invaginations of zippered ER. Electron tomography showed that IBV-induced spherules are tethered to the zippered ER and that there is a channel connecting the interior of the spherule with the cytoplasm, a feature thought to be necessary for sites of RNA synthesis but not seen previously for membrane rearrangements induced by coronaviruses. We also identified DMVs in IBV-infected cells that were observed as single individual DMVs or were connected to the ER via their outer membrane but not to the zippered ER. Interestingly, IBV-induced spherules strongly resemble confirmed sites of RNA synthesis for alphaviruses, nodaviruses, and bromoviruses, which may indicate similar strategies of IBV and these diverse viruses for the assembly of RNA replication complexes.</AbstractText><AbstractText Label="IMPORTANCE" NlmCategory="OBJECTIVE">All positive-sense single-stranded RNA viruses induce rearranged cellular membranes, providing a platform for viral replication complex assembly and protecting viral RNA from cellular defenses. We have studied the membrane rearrangements induced by an important poultry pathogen, the gammacoronavirus infectious bronchitis virus (IBV). Previous work studying closely related betacoronaviruses identified double-membrane vesicles (DMVs) and convoluted membranes (CMs) derived from the endoplasmic reticulum (ER) in infected cells. However, the role of DMVs and CMs in viral RNA synthesis remains unclear because these sealed vesicles lack a means of delivering viral RNA to the cytoplasm. Here, we characterized structures novel to IBV infection: zippered ER and small vesicles tethered to the zippered ER termed spherules. Significantly, spherules contain a channel connecting their interior to the cytoplasm and strongly resemble confirmed sites of RNA synthesis for other positive-sense RNA viruses, making them ideal candidates for the site of IBV RNA synthesis.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Maier</LastName><ForeName>Helena J</ForeName><Initials>HJ</Initials><AffiliationInfo><Affiliation>The Pirbright Institute, Compton Laboratory, Compton, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hawes</LastName><ForeName>Philippa C</ForeName><Initials>PC</Initials></Author><Author ValidYN="Y"><LastName>Cottam</LastName><ForeName>Eleanor M</ForeName><Initials>EM</Initials></Author><Author ValidYN="Y"><LastName>Mantell</LastName><ForeName>Judith</ForeName><Initials>J</Initials></Author><Author ValidYN="Y"><LastName>Verkade</LastName><ForeName>Paul</ForeName><Initials>P</Initials></Author><Author ValidYN="Y"><LastName>Monaghan</LastName><ForeName>Paul</ForeName><Initials>P</Initials></Author><Author ValidYN="Y"><LastName>Wileman</LastName><ForeName>Tom</ForeName><Initials>T</Initials></Author><Author ValidYN="Y"><LastName>Britton</LastName><ForeName>Paul</ForeName><Initials>P</Initials></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>BB/E01805X/1</GrantID><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/E018521/1</GrantID><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2013</Year><Month>10</Month><Day>22</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>mBio</MedlineTA><NlmUniqueID>101519231</NlmUniqueID></MedlineJournalInfo><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>MBio. 2013;4(6):e00987-13</RefSource><PMID Version="1">24345746</PMID></CommentsCorrections><CommentsCorrections RefType="CommentIn"><RefSource>Bioengineered. 2014 Sep-Oct;5(5):288-92</RefSource><PMID Version="1">25482229</PMID></CommentsCorrections></CommentsCorrectionsList><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002460" MajorTopicYN="N">Cell Line</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002645" MajorTopicYN="N">Chickens</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018352" MajorTopicYN="N">Coronavirus Infections</DescriptorName><QualifierName UI="Q000662" MajorTopicYN="Y">veterinary</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D004721" MajorTopicYN="N">Endoplasmic Reticulum</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000648" MajorTopicYN="N">ultrastructure</QualifierName><QualifierName UI="Q000821" MajorTopicYN="Y">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D001351" MajorTopicYN="N">Infectious bronchitis virus</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D007425" MajorTopicYN="N">Intracellular Membranes</DescriptorName><QualifierName UI="Q000737" 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