The 3′ Untranslated Region of Sindbis Virus Represses Deadenylation of Viral Transcripts in Mosquito and Mammalian Cells

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Published inJournal of Virology Vol. 82; no. 2; pp. 880 - 892
Main Authors Garneau, Nicole L., Sokoloski, Kevin J., Opyrchal, Mateusz, Neff, C. Preston, Wilusz, Carol J., Wilusz, Jeffrey
Format Journal Article
LanguageEnglish
Published Washington, DC American Society for Microbiology 01.01.2008
American Society for Microbiology (ASM)
Subjects
3' Untranslated Regions - genetics
3' Untranslated Regions - physiology
Aedes
Aedes albopictus
Alphavirus
Animals
Biological and medical sciences
Cell Line
Cercopithecus aethiops
Cricetinae
Fundamental and applied biological sciences. Psychology
Genome and Regulation of Viral Gene Expression
Host-Pathogen Interactions
Microbiology
Miscellaneous
Molecular Weight
Proteins - chemistry
Proteins - isolation & purification
RNA Stability
RNA, Viral - metabolism
Sequence Deletion
Sindbis virus
Sindbis Virus - genetics
Sindbis Virus - metabolism
Venezuelan equine encephalitis virus
Virology
Virus
Vertebrata
Mammalia
Messenger RNA
Gene
Togaviridae
Alphavirus
In vitro
Virology
Sindbis virus
Online AccessGet full text
ISSN0022-538X
1098-5514
1098-5514
DOI10.1128/JVI.01205-07

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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 positive-sense transcripts of Sindbis virus (SINV) resemble cellular mRNAs in that they possess a 5' cap and a 3' poly(A) tail. It is likely, therefore, that SINV RNAs must successfully overcome the cytoplasmic mRNA decay machinery of the cell in order to establish an efficient, productive infection. In this study, we have taken advantage of a temperature-sensitive polymerase to shut off viral transcription, and we demonstrate that SINV RNAs are subject to decay during a viral infection in both C6/36 (Aedes albopictus) and baby hamster kidney cells. Interestingly, in contrast to most cellular mRNAs, the decay of SINV RNAs was not initiated by poly(A) tail shortening in either cell line except when most of the 3' untranslated region (UTR) was deleted from the virus. This block in deadenylation of viral transcripts was recapitulated in vitro using C6/36 mosquito cell cytoplasmic extracts. Two distinct regions of the 319-base SINV 3' UTR, the repeat sequence elements and a U-rich domain, were shown to be responsible for mediating the repression of deadenylation of viral mRNAs. Through competition studies performed in parallel with UV cross-linking and functional assays, mosquito cell factors-including a 38-kDa protein-were implicated in the repression of deadenylation mediated by the SINV 3' UTR. This same 38-kDa protein was also implicated in mediating the repression of deadenylation by the 3' UTR of another alphavirus, Venezuelan equine encephalitis virus. In summary, these data provide clear evidence that SINV transcripts do indeed interface with the cellular mRNA decay machinery during an infection and that the virus has evolved a way to avoid the major deadenylation-dependent pathway of mRNA decay.The positive-sense transcripts of Sindbis virus (SINV) resemble cellular mRNAs in that they possess a 5' cap and a 3' poly(A) tail. It is likely, therefore, that SINV RNAs must successfully overcome the cytoplasmic mRNA decay machinery of the cell in order to establish an efficient, productive infection. In this study, we have taken advantage of a temperature-sensitive polymerase to shut off viral transcription, and we demonstrate that SINV RNAs are subject to decay during a viral infection in both C6/36 (Aedes albopictus) and baby hamster kidney cells. Interestingly, in contrast to most cellular mRNAs, the decay of SINV RNAs was not initiated by poly(A) tail shortening in either cell line except when most of the 3' untranslated region (UTR) was deleted from the virus. This block in deadenylation of viral transcripts was recapitulated in vitro using C6/36 mosquito cell cytoplasmic extracts. Two distinct regions of the 319-base SINV 3' UTR, the repeat sequence elements and a U-rich domain, were shown to be responsible for mediating the repression of deadenylation of viral mRNAs. Through competition studies performed in parallel with UV cross-linking and functional assays, mosquito cell factors-including a 38-kDa protein-were implicated in the repression of deadenylation mediated by the SINV 3' UTR. This same 38-kDa protein was also implicated in mediating the repression of deadenylation by the 3' UTR of another alphavirus, Venezuelan equine encephalitis virus. In summary, these data provide clear evidence that SINV transcripts do indeed interface with the cellular mRNA decay machinery during an infection and that the virus has evolved a way to avoid the major deadenylation-dependent pathway of mRNA decay.
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       
The positive-sense transcripts of Sindbis virus (SINV) resemble cellular mRNAs in that they possess a 5′ cap and a 3′ poly(A) tail. It is likely, therefore, that SINV RNAs must successfully overcome the cytoplasmic mRNA decay machinery of the cell in order to establish an efficient, productive infection. In this study, we have taken advantage of a temperature-sensitive polymerase to shut off viral transcription, and we demonstrate that SINV RNAs are subject to decay during a viral infection in both C6/36 ( Aedes albopictus ) and baby hamster kidney cells. Interestingly, in contrast to most cellular mRNAs, the decay of SINV RNAs was not initiated by poly(A) tail shortening in either cell line except when most of the 3′ untranslated region (UTR) was deleted from the virus. This block in deadenylation of viral transcripts was recapitulated in vitro using C6/36 mosquito cell cytoplasmic extracts. Two distinct regions of the 319-base SINV 3′ UTR, the repeat sequence elements and a U-rich domain, were shown to be responsible for mediating the repression of deadenylation of viral mRNAs. Through competition studies performed in parallel with UV cross-linking and functional assays, mosquito cell factors—including a 38-kDa protein—were implicated in the repression of deadenylation mediated by the SINV 3′ UTR. This same 38-kDa protein was also implicated in mediating the repression of deadenylation by the 3′ UTR of another alphavirus, Venezuelan equine encephalitis virus. In summary, these data provide clear evidence that SINV transcripts do indeed interface with the cellular mRNA decay machinery during an infection and that the virus has evolved a way to avoid the major deadenylation-dependent pathway of mRNA decay.
The positive-sense transcripts of Sindbis virus (SINV) resemble cellular mRNAs in that they possess a 5' cap and a 3' poly(A) tail. It is likely, therefore, that SINV RNAs must successfully overcome the cytoplasmic mRNA decay machinery of the cell in order to establish an efficient, productive infection. In this study, we have taken advantage of a temperature-sensitive polymerase to shut off viral transcription, and we demonstrate that SINV RNAs are subject to decay during a viral infection in both C6/36 (Aedes albopictus) and baby hamster kidney cells. Interestingly, in contrast to most cellular mRNAs, the decay of SINV RNAs was not initiated by poly(A) tail shortening in either cell line except when most of the 3' untranslated region (UTR) was deleted from the virus. This block in deadenylation of viral transcripts was recapitulated in vitro using C6/36 mosquito cell cytoplasmic extracts. Two distinct regions of the 319-base SINV 3' UTR, the repeat sequence elements and a U-rich domain, were shown to be responsible for mediating the repression of deadenylation of viral mRNAs. Through competition studies performed in parallel with UV cross-linking and functional assays, mosquito cell factors-including a 38-kDa protein-were implicated in the repression of deadenylation mediated by the SINV 3' UTR. This same 38-kDa protein was also implicated in mediating the repression of deadenylation by the 3' UTR of another alphavirus, Venezuelan equine encephalitis virus. In summary, these data provide clear evidence that SINV transcripts do indeed interface with the cellular mRNA decay machinery during an infection and that the virus has evolved a way to avoid the major deadenylation-dependent pathway of mRNA decay.
Author Jeffrey Wilusz
C. Preston Neff
Nicole L. Garneau
Carol J. Wilusz
Kevin J. Sokoloski
Mateusz Opyrchal
AuthorAffiliation Colorado State University, Department of Microbiology, Immunology and Pathology, Fort Collins, Colorado
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  givenname: C. Preston
  surname: Neff
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Keywords Virus
Vertebrata
Mammalia
Messenger RNA
Gene
Togaviridae
Alphavirus
In vitro
Virology
Sindbis virus
Language English
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N.L.G. and K.J.S. contributed equally to this work.
Corresponding author. Mailing address: Colorado State University, Department of Microbiology, Immunology and Pathology, 1682 Campus Delivery, Fort Collins, CO 80523-1682. Phone: (970) 491-0652. Fax: (970) 491-4941. E-mail: jeffrey.wilusz@colostate.edu
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Snippet Article Usage Stats Services JVI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley...
The positive-sense transcripts of Sindbis virus (SINV) resemble cellular mRNAs in that they possess a 5′ cap and a 3′ poly(A) tail. It is likely, therefore,...
The positive-sense transcripts of Sindbis virus (SINV) resemble cellular mRNAs in that they possess a 5' cap and a 3' poly(A) tail. It is likely, therefore,...
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SubjectTerms 3' Untranslated Regions - genetics
3' Untranslated Regions - physiology
Aedes
Aedes albopictus
Alphavirus
Animals
Biological and medical sciences
Cell Line
Cercopithecus aethiops
Cricetinae
Fundamental and applied biological sciences. Psychology
Genome and Regulation of Viral Gene Expression
Host-Pathogen Interactions
Microbiology
Miscellaneous
Molecular Weight
Proteins - chemistry
Proteins - isolation & purification
RNA Stability
RNA, Viral - metabolism
Sequence Deletion
Sindbis virus
Sindbis Virus - genetics
Sindbis Virus - metabolism
Venezuelan equine encephalitis virus
Virology
Title The 3′ Untranslated Region of Sindbis Virus Represses Deadenylation of Viral Transcripts in Mosquito and Mammalian Cells
URI http://jvi.asm.org/content/82/2/880.abstract
https://www.ncbi.nlm.nih.gov/pubmed/17977976
https://www.proquest.com/docview/20471230
https://www.proquest.com/docview/70179562
https://pubmed.ncbi.nlm.nih.gov/PMC2224598
Volume 82
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