The Open Reading Frame 3a Protein of Severe Acute Respiratory Syndrome-Associated Coronavirus Promotes Membrane Rearrangement and Cell Death

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Published inJournal of Virology Vol. 84; no. 2; pp. 1097 - 1109
Main Authors Freundt, Eric C., Yu, Li, Goldsmith, Cynthia S., Welsh, Sarah, Cheng, Aaron, Yount, Boyd, Liu, Wei, Frieman, Matthew B., Buchholz, Ursula J., Screaton, Gavin R., Lippincott-Schwartz, Jennifer, Zaki, Sherif R., Xu, Xiao-Ning, Baric, Ralph S., Subbarao, Kanta, Lenardo, Michael J.
Format Journal Article
LanguageEnglish
Published United States American Society for Microbiology 01.01.2010
American Society for Microbiology (ASM)
Subjects
ADP-Ribosylation Factor 1 - genetics
ADP-Ribosylation Factor 1 - metabolism
Animals
Cell Death
Cell Membrane - pathology
Cell Membrane - virology
Chlorocebus aethiops
Cytoplasmic Vesicles - metabolism
Cytoplasmic Vesicles - virology
Gene Deletion
Golgi Apparatus - metabolism
Golgi Apparatus - pathology
Host-Pathogen Interactions
Humans
SARS coronavirus
Severe acute respiratory syndrome-related coronavirus - genetics
Severe acute respiratory syndrome-related coronavirus - metabolism
Severe acute respiratory syndrome-related coronavirus - pathogenicity
Transfection
Vero Cells - pathology
Viral Structural Proteins - metabolism
Virus-Cell Interactions
Online AccessGet full text
ISSN0022-538X
1098-5514
1098-5514
DOI10.1128/JVI.01662-09

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Abstract Article Usage Stats Services JVI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue Spotlights in the Current Issue JVI About JVI Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JVI RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0022-538X Online ISSN: 1098-5514 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to JVI .asm.org, visit: JVI       
AbstractList The genome of the severe acute respiratory syndrome-associated coronavirus (SARS-CoV) contains eight open reading frames (ORFs) that encode novel proteins. These accessory proteins are dispensable for in vitro and in vivo replication and thus may be important for other aspects of virus-host interactions. We investigated the functions of the largest of the accessory proteins, the ORF 3a protein, using a 3a-deficient strain of SARS-CoV. Cell death of Vero cells after infection with SARS-CoV was reduced upon deletion of ORF 3a. Electron microscopy of infected cells revealed a role for ORF 3a in SARS-CoV induced vesicle formation, a prominent feature of cells from SARS patients. In addition, we report that ORF 3a is both necessary and sufficient for SARS-CoV-induced Golgi fragmentation and that the 3a protein accumulates and localizes to vesicles containing markers for late endosomes. Finally, overexpression of ADP-ribosylation factor 1 (Arf1), a small GTPase essential for the maintenance of the Golgi apparatus, restored Golgi morphology during infection. These results establish an important role for ORF 3a in SARS-CoV-induced cell death, Golgi fragmentation, and the accumulation of intracellular vesicles.
The genome of the severe acute respiratory syndrome-associated coronavirus (SARS-CoV) contains eight open reading frames (ORFs) that encode novel proteins. These accessory proteins are dispensable for in vitro and in vivo replication and thus may be important for other aspects of virus-host interactions. We investigated the functions of the largest of the accessory proteins, the ORF 3a protein, using a 3a-deficient strain of SARS-CoV. Cell death of Vero cells after infection with SARS-CoV was reduced upon deletion of ORF 3a. Electron microscopy of infected cells revealed a role for ORF 3a in SARS-CoV induced vesicle formation, a prominent feature of cells from SARS patients. In addition, we report that ORF 3a is both necessary and sufficient for SARS-CoV-induced Golgi fragmentation and that the 3a protein accumulates and localizes to vesicles containing markers for late endosomes. Finally, overexpression of ADP-ribosylation factor 1 (Arf1), a small GTPase essential for the maintenance of the Golgi apparatus, restored Golgi morphology during infection. These results establish an important role for ORF 3a in SARS-CoV-induced cell death, Golgi fragmentation, and the accumulation of intracellular vesicles.The genome of the severe acute respiratory syndrome-associated coronavirus (SARS-CoV) contains eight open reading frames (ORFs) that encode novel proteins. These accessory proteins are dispensable for in vitro and in vivo replication and thus may be important for other aspects of virus-host interactions. We investigated the functions of the largest of the accessory proteins, the ORF 3a protein, using a 3a-deficient strain of SARS-CoV. Cell death of Vero cells after infection with SARS-CoV was reduced upon deletion of ORF 3a. Electron microscopy of infected cells revealed a role for ORF 3a in SARS-CoV induced vesicle formation, a prominent feature of cells from SARS patients. In addition, we report that ORF 3a is both necessary and sufficient for SARS-CoV-induced Golgi fragmentation and that the 3a protein accumulates and localizes to vesicles containing markers for late endosomes. Finally, overexpression of ADP-ribosylation factor 1 (Arf1), a small GTPase essential for the maintenance of the Golgi apparatus, restored Golgi morphology during infection. These results establish an important role for ORF 3a in SARS-CoV-induced cell death, Golgi fragmentation, and the accumulation of intracellular vesicles.
Article Usage Stats Services JVI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue Spotlights in the Current Issue JVI About JVI Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JVI RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0022-538X Online ISSN: 1098-5514 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to JVI .asm.org, visit: JVI       
Author Li Yu
Aaron Cheng
Kanta Subbarao
Cynthia S. Goldsmith
Ralph S. Baric
Sherif R. Zaki
Boyd Yount
Matthew B. Frieman
Gavin R. Screaton
Ursula J. Buchholz
Xiao-Ning Xu
Jennifer Lippincott-Schwartz
Michael J. Lenardo
Wei Liu
Eric C. Freundt
Sarah Welsh
AuthorAffiliation Laboratory of Immunology, 1 Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, 2 Infectious Disease Pathology Branch, Division of Viral and Rickettsial Diseases, Center for Disease Control and Prevention, Atlanta, Georgia 30333, 3 Department of Epidemiology, School of Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7435, 4 Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, 5 Hammersmith Hospital, Imperial College, London W12 0NN, United Kingdom, 6 Medical Research Council Human Immunology Unit, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, University of Oxford, Oxford OX3 9DS, United Kingdom 7
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/19889773$$D View this record in MEDLINE/PubMed
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E.C.F. and L.Y. contributed equally to this study.
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References e_1_3_2_26_2
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The genome of the severe acute respiratory syndrome-associated coronavirus (SARS-CoV) contains eight open reading frames (ORFs) that encode novel proteins....
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SubjectTerms ADP-Ribosylation Factor 1 - genetics
ADP-Ribosylation Factor 1 - metabolism
Animals
Cell Death
Cell Membrane - pathology
Cell Membrane - virology
Chlorocebus aethiops
Cytoplasmic Vesicles - metabolism
Cytoplasmic Vesicles - virology
Gene Deletion
Golgi Apparatus - metabolism
Golgi Apparatus - pathology
Host-Pathogen Interactions
Humans
SARS coronavirus
Severe acute respiratory syndrome-related coronavirus - genetics
Severe acute respiratory syndrome-related coronavirus - metabolism
Severe acute respiratory syndrome-related coronavirus - pathogenicity
Transfection
Vero Cells - pathology
Viral Structural Proteins - metabolism
Virus-Cell Interactions
Title The Open Reading Frame 3a Protein of Severe Acute Respiratory Syndrome-Associated Coronavirus Promotes Membrane Rearrangement and Cell Death
URI http://jvi.asm.org/content/84/2/1097.abstract
https://www.ncbi.nlm.nih.gov/pubmed/19889773
https://www.proquest.com/docview/21328853
https://www.proquest.com/docview/733633673
https://pubmed.ncbi.nlm.nih.gov/PMC2798367
Volume 84
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