Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses

ABSTRACT The broad range and diversity of interferon-stimulated genes (ISGs) function to induce an antiviral state within the host, impeding viral pathogenesis. While successful respiratory viruses overcome individual ISG effectors, analysis of the global ISG response and subsequent viral antagonism...

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Autores principales:	Vineet D. Menachery, Amie J. Eisfeld, Alexandra Schäfer, Laurence Josset, Amy C. Sims, Sean Proll, Shufang Fan, Chengjun Li, Gabriele Neumann, Susan C. Tilton, Jean Chang, Lisa E. Gralinski, Casey Long, Richard Green, Christopher M. Williams, Jeffrey Weiss, Melissa M. Matzke, Bobbie-Jo Webb-Robertson, Athena A. Schepmoes, Anil K. Shukla, Thomas O. Metz, Richard D. Smith, Katrina M. Waters, Michael G. Katze, Yoshihiro Kawaoka, Ralph S. Baric
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/758ade4ede57407c9376f7e42de78b98
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spelling	oai:doaj.org-article:758ade4ede57407c9376f7e42de78b982021-11-15T15:47:38ZPathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses10.1128/mBio.01174-142150-7511https://doaj.org/article/758ade4ede57407c9376f7e42de78b982014-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01174-14https://doaj.org/toc/2150-7511ABSTRACT The broad range and diversity of interferon-stimulated genes (ISGs) function to induce an antiviral state within the host, impeding viral pathogenesis. While successful respiratory viruses overcome individual ISG effectors, analysis of the global ISG response and subsequent viral antagonism has yet to be examined. Employing models of the human airway, transcriptomics and proteomics datasets were used to compare ISG response patterns following highly pathogenic H5N1 avian influenza (HPAI) A virus, 2009 pandemic H1N1, severe acute respiratory syndrome coronavirus (SARS-CoV), and Middle East respiratory syndrome CoV (MERS-CoV) infection. The results illustrated distinct approaches utilized by each virus to antagonize the global ISG response. In addition, the data revealed that highly virulent HPAI virus and MERS-CoV induce repressive histone modifications, which downregulate expression of ISG subsets. Notably, influenza A virus NS1 appears to play a central role in this histone-mediated downregulation in highly pathogenic influenza strains. Together, the work demonstrates the existence of unique and common viral strategies for controlling the global ISG response and provides a novel avenue for viral antagonism via altered histone modifications. IMPORTANCE This work combines systems biology and experimental validation to identify and confirm strategies used by viruses to control the immune response. Using a novel screening approach, specific comparison between highly pathogenic influenza viruses and coronaviruses revealed similarities and differences in strategies to control the interferon and innate immune response. These findings were subsequently confirmed and explored, revealing both a common pathway of antagonism via type I interferon (IFN) delay as well as a novel avenue for control by altered histone modification. Together, the data highlight how comparative systems biology analysis can be combined with experimental validation to derive novel insights into viral pathogenesis.Vineet D. MenacheryAmie J. EisfeldAlexandra SchäferLaurence JossetAmy C. SimsSean ProllShufang FanChengjun LiGabriele NeumannSusan C. TiltonJean ChangLisa E. GralinskiCasey LongRichard GreenChristopher M. WilliamsJeffrey WeissMelissa M. MatzkeBobbie-Jo Webb-RobertsonAthena A. SchepmoesAnil K. ShuklaThomas O. MetzRichard D. SmithKatrina M. WatersMichael G. KatzeYoshihiro KawaokaRalph S. BaricAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 3 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Vineet D. Menachery Amie J. Eisfeld Alexandra Schäfer Laurence Josset Amy C. Sims Sean Proll Shufang Fan Chengjun Li Gabriele Neumann Susan C. Tilton Jean Chang Lisa E. Gralinski Casey Long Richard Green Christopher M. Williams Jeffrey Weiss Melissa M. Matzke Bobbie-Jo Webb-Robertson Athena A. Schepmoes Anil K. Shukla Thomas O. Metz Richard D. Smith Katrina M. Waters Michael G. Katze Yoshihiro Kawaoka Ralph S. Baric Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses
description	ABSTRACT The broad range and diversity of interferon-stimulated genes (ISGs) function to induce an antiviral state within the host, impeding viral pathogenesis. While successful respiratory viruses overcome individual ISG effectors, analysis of the global ISG response and subsequent viral antagonism has yet to be examined. Employing models of the human airway, transcriptomics and proteomics datasets were used to compare ISG response patterns following highly pathogenic H5N1 avian influenza (HPAI) A virus, 2009 pandemic H1N1, severe acute respiratory syndrome coronavirus (SARS-CoV), and Middle East respiratory syndrome CoV (MERS-CoV) infection. The results illustrated distinct approaches utilized by each virus to antagonize the global ISG response. In addition, the data revealed that highly virulent HPAI virus and MERS-CoV induce repressive histone modifications, which downregulate expression of ISG subsets. Notably, influenza A virus NS1 appears to play a central role in this histone-mediated downregulation in highly pathogenic influenza strains. Together, the work demonstrates the existence of unique and common viral strategies for controlling the global ISG response and provides a novel avenue for viral antagonism via altered histone modifications. IMPORTANCE This work combines systems biology and experimental validation to identify and confirm strategies used by viruses to control the immune response. Using a novel screening approach, specific comparison between highly pathogenic influenza viruses and coronaviruses revealed similarities and differences in strategies to control the interferon and innate immune response. These findings were subsequently confirmed and explored, revealing both a common pathway of antagonism via type I interferon (IFN) delay as well as a novel avenue for control by altered histone modification. Together, the data highlight how comparative systems biology analysis can be combined with experimental validation to derive novel insights into viral pathogenesis.
format	article
author	Vineet D. Menachery Amie J. Eisfeld Alexandra Schäfer Laurence Josset Amy C. Sims Sean Proll Shufang Fan Chengjun Li Gabriele Neumann Susan C. Tilton Jean Chang Lisa E. Gralinski Casey Long Richard Green Christopher M. Williams Jeffrey Weiss Melissa M. Matzke Bobbie-Jo Webb-Robertson Athena A. Schepmoes Anil K. Shukla Thomas O. Metz Richard D. Smith Katrina M. Waters Michael G. Katze Yoshihiro Kawaoka Ralph S. Baric
author_facet	Vineet D. Menachery Amie J. Eisfeld Alexandra Schäfer Laurence Josset Amy C. Sims Sean Proll Shufang Fan Chengjun Li Gabriele Neumann Susan C. Tilton Jean Chang Lisa E. Gralinski Casey Long Richard Green Christopher M. Williams Jeffrey Weiss Melissa M. Matzke Bobbie-Jo Webb-Robertson Athena A. Schepmoes Anil K. Shukla Thomas O. Metz Richard D. Smith Katrina M. Waters Michael G. Katze Yoshihiro Kawaoka Ralph S. Baric
author_sort	Vineet D. Menachery
title	Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses
title_short	Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses
title_full	Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses
title_fullStr	Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses
title_full_unstemmed	Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses
title_sort	pathogenic influenza viruses and coronaviruses utilize similar and contrasting approaches to control interferon-stimulated gene responses
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/758ade4ede57407c9376f7e42de78b98
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Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses

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