A noncoding RNA produced by arthropod-borne flaviviruses inhibits the cellular exoribonuclease XRN1 and alters host mRNA stability

All arthropod-borne flaviviruses generate a short noncoding RNA (sfRNA) from the viral 3' untranslated region during infection due to stalling of the cellular 5'-to-3' exonuclease XRN1. We show here that formation of sfRNA also inhibits XRN1 activity. Cells infected with Dengue or Kun...

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Published inRNA (Cambridge) Vol. 18; no. 11; pp. 2029 - 2040
Main Authors Moon, Stephanie L, Anderson, John R, Kumagai, Yutaro, Wilusz, Carol J, Akira, Shizuo, Khromykh, Alexander A, Wilusz, Jeffrey
Format Journal Article
LanguageEnglish
Published United States Cold Spring Harbor Laboratory Press 01.11.2012
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Abstract All arthropod-borne flaviviruses generate a short noncoding RNA (sfRNA) from the viral 3' untranslated region during infection due to stalling of the cellular 5'-to-3' exonuclease XRN1. We show here that formation of sfRNA also inhibits XRN1 activity. Cells infected with Dengue or Kunjin viruses accumulate uncapped mRNAs, decay intermediates normally targeted by XRN1. XRN1 repression also resulted in the increased overall stability of cellular mRNAs in flavivirus-infected cells. Importantly, a mutant Kunjin virus that cannot form sfRNA but replicates to normal levels failed to affect host mRNA stability or XRN1 activity. Expression of sfRNA in the absence of viral infection demonstrated that sfRNA formation was directly responsible for the stabilization of cellular mRNAs. Finally, numerous cellular mRNAs were differentially expressed in an sfRNA-dependent fashion in a Kunjin virus infection. We conclude that flaviviruses incapacitate XRN1 during infection and dysregulate host mRNA stability as a result of sfRNA formation.
AbstractList All arthropod-borne flaviviruses generate a short noncoding RNA (sfRNA) from the viral 3' untranslated region during infection due to stalling of the cellular 5'-to-3' exonuclease XRN1. We show here that formation of sfRNA also inhibits XRN1 activity. Cells infected with Dengue or Kunjin viruses accumulate uncapped mRNAs, decay intermediates normally targeted by XRN1. XRN1 repression also resulted in the increased overall stability of cellular mRNAs in flavivirus-infected cells. Importantly, a mutant Kunjin virus that cannot form sfRNA but replicates to normal levels failed to affect host mRNA stability or XRN1 activity. Expression of sfRNA in the absence of viral infection demonstrated that sfRNA formation was directly responsible for the stabilization of cellular mRNAs. Finally, numerous cellular mRNAs were differentially expressed in an sfRNA-dependent fashion in a Kunjin virus infection. We conclude that flaviviruses incapacitate XRN1 during infection and dysregulate host mRNA stability as a result of sfRNA formation.
Cells infected with arthropod-borne flaviviruses (e.g., Dengue or Kunjin viruses) accumulate uncapped mRNAs or viral genomes, decay intermediates normally targeted by cellular 5′-to-3′ exonuclease XRN1. These viruses also generate a short noncoding RNA (sfRNA) from the viral 3′ untranslated region during infection, due to the stalling of the XRN1. This paper shows that XRN1 can be found associated with sfRNA during infection and that this results in the repression of its activity. Cellular mRNAs are also stabilized by sfRNA, likely as a result of the shutdown of the 5′-to-3′ mRNA decay pathway. All arthropod-borne flaviviruses generate a short noncoding RNA (sfRNA) from the viral 3′ untranslated region during infection due to stalling of the cellular 5′-to-3′ exonuclease XRN1. We show here that formation of sfRNA also inhibits XRN1 activity. Cells infected with Dengue or Kunjin viruses accumulate uncapped mRNAs, decay intermediates normally targeted by XRN1. XRN1 repression also resulted in the increased overall stability of cellular mRNAs in flavivirus-infected cells. Importantly, a mutant Kunjin virus that cannot form sfRNA but replicates to normal levels failed to affect host mRNA stability or XRN1 activity. Expression of sfRNA in the absence of viral infection demonstrated that sfRNA formation was directly responsible for the stabilization of cellular mRNAs. Finally, numerous cellular mRNAs were differentially expressed in an sfRNA-dependent fashion in a Kunjin virus infection. We conclude that flaviviruses incapacitate XRN1 during infection and dysregulate host mRNA stability as a result of sfRNA formation.
Author Moon, Stephanie L
Kumagai, Yutaro
Wilusz, Carol J
Anderson, John R
Khromykh, Alexander A
Wilusz, Jeffrey
Akira, Shizuo
AuthorAffiliation 1 Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado 80523, USA
2 Laboratory of Host Defense, Immunology Frontier Research Center, Department of Host Defense, Research Institute for Microbial Diseases, Osaka University, Suita, Osaka 565-0871, Japan
3 Australian Infectious Disease Research Centre, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia
AuthorAffiliation_xml – name: 3 Australian Infectious Disease Research Centre, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia
– name: 1 Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado 80523, USA
– name: 2 Laboratory of Host Defense, Immunology Frontier Research Center, Department of Host Defense, Research Institute for Microbial Diseases, Osaka University, Suita, Osaka 565-0871, Japan
Author_xml – sequence: 1
  givenname: Stephanie L
  surname: Moon
  fullname: Moon, Stephanie L
  organization: Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado 80523, USA
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  surname: Anderson
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  surname: Wilusz
  fullname: Wilusz, Carol J
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  givenname: Shizuo
  surname: Akira
  fullname: Akira, Shizuo
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  givenname: Alexander A
  surname: Khromykh
  fullname: Khromykh, Alexander A
– sequence: 7
  givenname: Jeffrey
  surname: Wilusz
  fullname: Wilusz, Jeffrey
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23006624$$D View this record in MEDLINE/PubMed
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Snippet All arthropod-borne flaviviruses generate a short noncoding RNA (sfRNA) from the viral 3' untranslated region during infection due to stalling of the cellular...
All arthropod-borne flaviviruses generate a short noncoding RNA (sfRNA) from the viral 3′ untranslated region during infection due to stalling of the cellular...
Cells infected with arthropod-borne flaviviruses (e.g., Dengue or Kunjin viruses) accumulate uncapped mRNAs or viral genomes, decay intermediates normally...
SourceID pubmedcentral
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SourceType Open Access Repository
Aggregation Database
Index Database
StartPage 2029
SubjectTerms 3' Untranslated Regions
Aedes - cytology
Aedes - virology
Animals
Cell Line
Cricetinae
Dengue Virus - genetics
Dengue Virus - physiology
Exoribonucleases - antagonists & inhibitors
Exoribonucleases - chemistry
Exoribonucleases - metabolism
Gene Expression Regulation
Half-Life
Host-Pathogen Interactions
Humans
Insect Proteins - antagonists & inhibitors
Insect Proteins - chemistry
Insect Proteins - metabolism
Microtubule-Associated Proteins - antagonists & inhibitors
Microtubule-Associated Proteins - chemistry
Microtubule-Associated Proteins - metabolism
Oligonucleotide Array Sequence Analysis
RNA Stability
RNA, Messenger - chemistry
RNA, Messenger - metabolism
RNA, Untranslated - chemistry
RNA, Untranslated - metabolism
RNA, Untranslated - physiology
RNA, Viral - chemistry
RNA, Viral - metabolism
RNA, Viral - physiology
Saccharomyces cerevisiae Proteins - antagonists & inhibitors
Saccharomyces cerevisiae Proteins - chemistry
Transcriptome
West Nile virus - genetics
West Nile virus - physiology
Title A noncoding RNA produced by arthropod-borne flaviviruses inhibits the cellular exoribonuclease XRN1 and alters host mRNA stability
URI https://www.ncbi.nlm.nih.gov/pubmed/23006624
https://search.proquest.com/docview/1113216541
https://pubmed.ncbi.nlm.nih.gov/PMC3479393
Volume 18
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