Infectious Bronchitis Virus Generates Spherules from Zippered Endoplasmic Reticulum Membranes
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 do...
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| Format: | Online |
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American Society of Microbiology
2013
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| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3812713/ |
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pubmed-38127132013-10-31 Infectious Bronchitis Virus Generates Spherules from Zippered Endoplasmic Reticulum Membranes Maier, Helena J. Hawes, Philippa C. Cottam, Eleanor M. Mantell, Judith Verkade, Paul Monaghan, Paul Wileman, Tom Britton, Paul Research Article 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. American Society of Microbiology 2013-10-22 /pmc/articles/PMC3812713/ /pubmed/24149513 http://dx.doi.org/10.1128/mBio.00801-13 Text en Copyright © 2013 Maier et al. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 3.0 Unported license (http://creativecommons.org/licenses/by/3.0/) , which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. |
| repository_type |
Open Access Journal |
| institution_category |
Foreign Institution |
| institution |
US National Center for Biotechnology Information |
| building |
NCBI PubMed |
| collection |
Online Access |
| language |
English |
| format |
Online |
| author |
Maier, Helena J. Hawes, Philippa C. Cottam, Eleanor M. Mantell, Judith Verkade, Paul Monaghan, Paul Wileman, Tom Britton, Paul |
| spellingShingle |
Maier, Helena J. Hawes, Philippa C. Cottam, Eleanor M. Mantell, Judith Verkade, Paul Monaghan, Paul Wileman, Tom Britton, Paul Infectious Bronchitis Virus Generates Spherules from Zippered Endoplasmic Reticulum Membranes |
| author_facet |
Maier, Helena J. Hawes, Philippa C. Cottam, Eleanor M. Mantell, Judith Verkade, Paul Monaghan, Paul Wileman, Tom Britton, Paul |
| author_sort |
Maier, Helena J. |
| title |
Infectious Bronchitis Virus Generates Spherules from Zippered Endoplasmic Reticulum Membranes |
| title_short |
Infectious Bronchitis Virus Generates Spherules from Zippered Endoplasmic Reticulum Membranes |
| title_full |
Infectious Bronchitis Virus Generates Spherules from Zippered Endoplasmic Reticulum Membranes |
| title_fullStr |
Infectious Bronchitis Virus Generates Spherules from Zippered Endoplasmic Reticulum Membranes |
| title_full_unstemmed |
Infectious Bronchitis Virus Generates Spherules from Zippered Endoplasmic Reticulum Membranes |
| title_sort |
infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes |
| description |
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. |
| publisher |
American Society of Microbiology |
| publishDate |
2013 |
| url |
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3812713/ |
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1612021789778509824 |