Sustained activation of interferon regulatory factor 3 during infection by paramyxoviruses requires MDA5

J Innate Immun. 2014;6(5):650-62. doi: 10.1159/000360764. Epub 2014 Apr 30.

Abstract

Retinoic acid-inducible gene I (RIG-I) and melanoma differentiation-associated gene 5 (MDA5) are the main cytosolic sensors of single-stranded RNA viruses, including paramyxoviruses, and are required to initiate a quick and robust innate antiviral response. Despite different ligand-binding properties, the consensus view is that RIG-I and MDA5 trigger common signal(s) to activate interferon regulatory factor 3 (IRF-3) and NF-κB, and downstream antiviral and proinflammatory cytokine expression. Here, we performed a thorough analysis of the temporal involvement of RIG-I and MDA5 in the regulation of IRF-3 during respiratory syncytial virus (RSV) infection. Based on specific RNA interference-mediated knockdown of RIG-I and MDA5 in A549 cells, we confirmed that RIG-I is critical for the initiation of IRF-3 phosphorylation, dimerization and downstream gene expression. On the other hand, our experiments yielded the first evidence that knockdown of MDA5 leads to early ubiquitination and proteasomal degradation of active IRF-3. Conversely, ectopic expression of MDA5 prolonged RIG-I-induced IRF-3 activation. Altogether, we provide novel mechanistic insight into the temporal involvement of RIG-I and MDA5 in the innate antiviral response. While RIG-I is essential for initial IRF-3 activation, engagement of induced MDA5 is essential to prevent early degradation of IRF-3, thereby sustaining IRF-3-dependent antiviral gene expression. MDA5 plays a similar role during Sendai virus infection suggesting that this model is not restricted to RSV amongst paramyxoviruses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • DEAD Box Protein 58
  • DEAD-box RNA Helicases / genetics
  • DEAD-box RNA Helicases / metabolism*
  • Epithelial Cells / immunology*
  • Epithelial Cells / virology
  • Gene Expression Regulation / genetics
  • Humans
  • Immunity, Innate / genetics
  • Interferon Regulatory Factor-3 / genetics
  • Interferon Regulatory Factor-3 / metabolism*
  • Interferon-Induced Helicase, IFIH1
  • Phosphorylation / genetics
  • Proteolysis
  • RNA, Small Interfering / genetics
  • Receptors, Immunologic
  • Respiratory Syncytial Virus Infections / immunology*
  • Respiratory Syncytial Virus, Human / immunology*
  • Signal Transduction / genetics
  • Ubiquitination / genetics

Substances

  • IRF3 protein, human
  • Interferon Regulatory Factor-3
  • RNA, Small Interfering
  • Receptors, Immunologic
  • RIGI protein, human
  • IFIH1 protein, human
  • DEAD Box Protein 58
  • DEAD-box RNA Helicases
  • Interferon-Induced Helicase, IFIH1