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Research Article

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

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
Herbert Virgin, Editor
Vineet D. Menachery
aDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
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Amie J. Eisfeld
cInfluenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Alexandra Schäfer
aDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
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Laurence Josset
dDepartment of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA
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Amy C. Sims
aDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
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Sean Proll
dDepartment of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA
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Shufang Fan
cInfluenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Chengjun Li
cInfluenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Gabriele Neumann
cInfluenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Susan C. Tilton
eBiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Jean Chang
dDepartment of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA
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Lisa E. Gralinski
aDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
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Casey Long
aDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
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Richard Green
dDepartment of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA
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Christopher M. Williams
dDepartment of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA
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Jeffrey Weiss
dDepartment of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA
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Melissa M. Matzke
eBiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Bobbie-Jo Webb-Robertson
eBiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Athena A. Schepmoes
eBiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Anil K. Shukla
eBiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Thomas O. Metz
eBiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Richard D. Smith
eBiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Katrina M. Waters
eBiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Michael G. Katze
dDepartment of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA
fWashington National Primate Research Center, University of Washington, Seattle, Washington, USA
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Yoshihiro Kawaoka
cInfluenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin—Madison, Madison, Wisconsin, USA
gDivision of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Tokyo, Japan
hInstitute of Medical Science, International Research Center for Infectious Diseases, Department of Special Pathogens, University of Tokyo, Tokyo, Japan
iERATO Infection-Induced Host Responses Project, Saitama, Japan
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Ralph S. Baric
aDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
bDepartment of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
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Herbert Virgin
Washington University School of Medicine
Roles: Editor
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DOI: 10.1128/mBio.01174-14
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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.

FOOTNOTES

    • Received 8 April 2014
    • Accepted 21 April 2014
    • Published 20 May 2014
  • Copyright © 2014 Menachery et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses
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
mBio May 2014, 5 (3) e01174-14; DOI: 10.1128/mBio.01174-14

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Pathogenic Influenza Viruses and Coronaviruses Utilize Similar and Contrasting Approaches To Control Interferon-Stimulated Gene Responses
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
mBio May 2014, 5 (3) e01174-14; DOI: 10.1128/mBio.01174-14
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