Integrated network analysis reveals a novel role for the cell cycle in 2009 pandemic influenza virus-induced inflammation in macaque lungs

BMC Syst Biol. 2012 Aug 31:6:117. doi: 10.1186/1752-0509-6-117.

Abstract

Background: Annually, influenza A viruses circulate the world causing wide-spread sickness, economic loss, and death. One way to better defend against influenza virus-induced disease may be to develop novel host-based therapies, targeted at mitigating viral pathogenesis through the management of virus-dysregulated host functions. However, mechanisms that govern aberrant host responses to influenza virus infection remain incompletely understood. We previously showed that the pandemic H1N1 virus influenza A/California/04/2009 (H1N1; CA04) has enhanced pathogenicity in the lungs of cynomolgus macaques relative to a seasonal influenza virus isolate (A/Kawasaki/UTK-4/2009 (H1N1; KUTK4)).

Results: Here, we used microarrays to identify host gene sequences that were highly differentially expressed (DE) in CA04-infected macaque lungs, and we employed a novel strategy - combining functional and pathway enrichment analyses, transcription factor binding site enrichment analysis and protein-protein interaction data - to create a CA04 differentially regulated host response network. This network describes enhanced viral RNA sensing, immune cell signaling and cell cycle arrest in CA04-infected lungs, and highlights a novel, putative role for the MYC-associated zinc finger (MAZ) transcription factor in regulating these processes.

Conclusions: Our findings suggest that the enhanced pathology is the result of a prolonged immune response, despite successful virus clearance. Most interesting, we identify a mechanism which normally suppresses immune cell signaling and inflammation is ineffective in the pH1N1 virus infection; a dyregulatory event also associated with arthritis. This dysregulation offers several opportunities for developing strain-independent, immunomodulatory therapies to protect against future pandemics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity / genetics
  • Animals
  • Apoptosis / genetics
  • Binding Sites
  • Caspase 1 / biosynthesis
  • Cell Cycle*
  • Chemotaxis / genetics
  • Computational Biology*
  • Down-Regulation
  • Enzyme Induction / genetics
  • Female
  • Glutathione Transferase / genetics
  • Humans
  • Immunity, Innate / genetics
  • Inflammation / genetics
  • Inflammation / immunology
  • Inflammation / pathology
  • Inflammation / virology
  • Influenza A Virus, H1N1 Subtype / pathogenicity*
  • Lung / immunology
  • Lung / metabolism
  • Lung / pathology*
  • Lung / virology*
  • Macaca
  • Orthomyxoviridae Infections / epidemiology*
  • Pandemics*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Transcription Factors / metabolism

Substances

  • RNA, Messenger
  • Transcription Factors
  • Glutathione Transferase
  • Caspase 1