Unique Signatures of Long Noncoding RNA Expression in Response to Virus Infection and Altered Innate Immune Signaling

ABSTRACT Studies of the host response to virus infection typically focus on protein-coding genes. However, non-protein-coding RNAs (ncRNAs) are transcribed in mammalian cells, and the roles of many of these ncRNAs remain enigmas. Using next-generation sequencing, we performed a whole-transcriptome a...

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Autores principales:	Xinxia Peng, Lisa Gralinski, Christopher D. Armour, Martin T. Ferris, Matthew J. Thomas, Sean Proll, Birgit G. Bradel-Tretheway, Marcus J. Korth, John C. Castle, Matthew C. Biery, Heather K. Bouzek, David R. Haynor, Matthew B. Frieman, Mark Heise, Christopher K. Raymond, Ralph S. Baric, Michael G. Katze
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2010
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0fa768ca0bf14feebd7178bad2e46226
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spelling	oai:doaj.org-article:0fa768ca0bf14feebd7178bad2e462262021-11-15T15:38:17ZUnique Signatures of Long Noncoding RNA Expression in Response to Virus Infection and Altered Innate Immune Signaling10.1128/mBio.00206-102150-7511https://doaj.org/article/0fa768ca0bf14feebd7178bad2e462262010-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00206-10https://doaj.org/toc/2150-7511ABSTRACT Studies of the host response to virus infection typically focus on protein-coding genes. However, non-protein-coding RNAs (ncRNAs) are transcribed in mammalian cells, and the roles of many of these ncRNAs remain enigmas. Using next-generation sequencing, we performed a whole-transcriptome analysis of the host response to severe acute respiratory syndrome coronavirus (SARS-CoV) infection across four founder mouse strains of the Collaborative Cross. We observed differential expression of approximately 500 annotated, long ncRNAs and 1,000 nonannotated genomic regions during infection. Moreover, studies of a subset of these ncRNAs and genomic regions showed the following. (i) Most were similarly regulated in response to influenza virus infection. (ii) They had distinctive kinetic expression profiles in type I interferon receptor and STAT1 knockout mice during SARS-CoV infection, including unique signatures of ncRNA expression associated with lethal infection. (iii) Over 40% were similarly regulated in vitro in response to both influenza virus infection and interferon treatment. These findings represent the first discovery of the widespread differential expression of long ncRNAs in response to virus infection and suggest that ncRNAs are involved in regulating the host response, including innate immunity. At the same time, virus infection models provide a unique platform for studying the biology and regulation of ncRNAs. IMPORTANCE Most studies examining the host transcriptional response to infection focus only on protein-coding genes. However, there is growing evidence that thousands of non-protein-coding RNAs (ncRNAs) are transcribed from mammalian genomes. While most attention to the involvement of ncRNAs in virus-host interactions has been on small ncRNAs such as microRNAs, it is becoming apparent that many long ncRNAs (>200 nucleotides [nt]) are also biologically important. These long ncRNAs have been found to have widespread functionality, including chromatin modification and transcriptional regulation and serving as the precursors of small RNAs. With the advent of next-generation sequencing technologies, whole-transcriptome analysis of the host response, including long ncRNAs, is now possible. Using this approach, we demonstrated that virus infection alters the expression of numerous long ncRNAs, suggesting that these RNAs may be a new class of regulatory molecules that play a role in determining the outcome of infection.Xinxia PengLisa GralinskiChristopher D. ArmourMartin T. FerrisMatthew J. ThomasSean ProllBirgit G. Bradel-TrethewayMarcus J. KorthJohn C. CastleMatthew C. BieryHeather K. BouzekDavid R. HaynorMatthew B. FriemanMark HeiseChristopher K. RaymondRalph S. BaricMichael G. KatzeAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 1, Iss 5 (2010)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Xinxia Peng Lisa Gralinski Christopher D. Armour Martin T. Ferris Matthew J. Thomas Sean Proll Birgit G. Bradel-Tretheway Marcus J. Korth John C. Castle Matthew C. Biery Heather K. Bouzek David R. Haynor Matthew B. Frieman Mark Heise Christopher K. Raymond Ralph S. Baric Michael G. Katze Unique Signatures of Long Noncoding RNA Expression in Response to Virus Infection and Altered Innate Immune Signaling
description	ABSTRACT Studies of the host response to virus infection typically focus on protein-coding genes. However, non-protein-coding RNAs (ncRNAs) are transcribed in mammalian cells, and the roles of many of these ncRNAs remain enigmas. Using next-generation sequencing, we performed a whole-transcriptome analysis of the host response to severe acute respiratory syndrome coronavirus (SARS-CoV) infection across four founder mouse strains of the Collaborative Cross. We observed differential expression of approximately 500 annotated, long ncRNAs and 1,000 nonannotated genomic regions during infection. Moreover, studies of a subset of these ncRNAs and genomic regions showed the following. (i) Most were similarly regulated in response to influenza virus infection. (ii) They had distinctive kinetic expression profiles in type I interferon receptor and STAT1 knockout mice during SARS-CoV infection, including unique signatures of ncRNA expression associated with lethal infection. (iii) Over 40% were similarly regulated in vitro in response to both influenza virus infection and interferon treatment. These findings represent the first discovery of the widespread differential expression of long ncRNAs in response to virus infection and suggest that ncRNAs are involved in regulating the host response, including innate immunity. At the same time, virus infection models provide a unique platform for studying the biology and regulation of ncRNAs. IMPORTANCE Most studies examining the host transcriptional response to infection focus only on protein-coding genes. However, there is growing evidence that thousands of non-protein-coding RNAs (ncRNAs) are transcribed from mammalian genomes. While most attention to the involvement of ncRNAs in virus-host interactions has been on small ncRNAs such as microRNAs, it is becoming apparent that many long ncRNAs (>200 nucleotides [nt]) are also biologically important. These long ncRNAs have been found to have widespread functionality, including chromatin modification and transcriptional regulation and serving as the precursors of small RNAs. With the advent of next-generation sequencing technologies, whole-transcriptome analysis of the host response, including long ncRNAs, is now possible. Using this approach, we demonstrated that virus infection alters the expression of numerous long ncRNAs, suggesting that these RNAs may be a new class of regulatory molecules that play a role in determining the outcome of infection.
format	article
author	Xinxia Peng Lisa Gralinski Christopher D. Armour Martin T. Ferris Matthew J. Thomas Sean Proll Birgit G. Bradel-Tretheway Marcus J. Korth John C. Castle Matthew C. Biery Heather K. Bouzek David R. Haynor Matthew B. Frieman Mark Heise Christopher K. Raymond Ralph S. Baric Michael G. Katze
author_facet	Xinxia Peng Lisa Gralinski Christopher D. Armour Martin T. Ferris Matthew J. Thomas Sean Proll Birgit G. Bradel-Tretheway Marcus J. Korth John C. Castle Matthew C. Biery Heather K. Bouzek David R. Haynor Matthew B. Frieman Mark Heise Christopher K. Raymond Ralph S. Baric Michael G. Katze
author_sort	Xinxia Peng
title	Unique Signatures of Long Noncoding RNA Expression in Response to Virus Infection and Altered Innate Immune Signaling
title_short	Unique Signatures of Long Noncoding RNA Expression in Response to Virus Infection and Altered Innate Immune Signaling
title_full	Unique Signatures of Long Noncoding RNA Expression in Response to Virus Infection and Altered Innate Immune Signaling
title_fullStr	Unique Signatures of Long Noncoding RNA Expression in Response to Virus Infection and Altered Innate Immune Signaling
title_full_unstemmed	Unique Signatures of Long Noncoding RNA Expression in Response to Virus Infection and Altered Innate Immune Signaling
title_sort	unique signatures of long noncoding rna expression in response to virus infection and altered innate immune signaling
publisher	American Society for Microbiology
publishDate	2010
url	https://doaj.org/article/0fa768ca0bf14feebd7178bad2e46226
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Unique Signatures of Long Noncoding RNA Expression in Response to Virus Infection and Altered Innate Immune Signaling

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