Biphasic RLR-IFN-β response controls the balance between antiviral immunity and cell damage

J Immunol. 2013 Feb 1;190(3):1192-200. doi: 10.4049/jimmunol.1202326. Epub 2013 Jan 2.

Abstract

In RNA virus-infected cells, retinoic acid-inducible gene-I-like receptors (RLRs) sense foreign RNAs and activate signaling cascades to produce IFN-α/β. However, not every infected cell produces IFN-α/β that exhibits cellular heterogeneity in antiviral immune responses. Using the IFN-β-GFP reporter system, we observed bimodal IFN-β production in the uniformly stimulated cell population with intracellular dsRNA. Mathematical simulation proposed the strength of autocrine loop via RLR as one of the contributing factor for biphasic IFN-β expression. Bimodal IFN-β production with intracellular dsRNA was disturbed by blockage of IFN-α/β secretion or by silencing of the IFN-α/β receptor. Amplification of RLRs was critical in the generation of bimodality of IFN-β production, because IFN-β(high) population expressed more RLRs than IFN-β(low) population. In addition, bimodality in IFN-β production results in biphasic cellular response against infection, because IFN-β(high) population was more prone to apoptosis than IFN-β(low) population. These results suggest that RLR-mediated biphasic cellular response may act to restrict the number of cells expressing IFN-β and undergoing apoptosis in the infected population.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / immunology*
  • Autocrine Communication / immunology*
  • Brefeldin A / pharmacology
  • DEAD Box Protein 58
  • DEAD-box RNA Helicases / antagonists & inhibitors
  • DEAD-box RNA Helicases / biosynthesis
  • DEAD-box RNA Helicases / genetics
  • DEAD-box RNA Helicases / physiology*
  • Gene Expression Regulation / immunology*
  • Genes, Reporter
  • Hep G2 Cells / drug effects
  • Hep G2 Cells / metabolism
  • Humans
  • Interferon Inducers / pharmacology
  • Interferon-Induced Helicase, IFIH1
  • Interferon-beta / biosynthesis*
  • Interferon-beta / genetics
  • Interferon-beta / immunology
  • Interferon-beta / metabolism
  • Models, Immunological*
  • Poly I-C / pharmacology
  • Protein Transport / drug effects
  • RNA Interference
  • RNA, Double-Stranded / pharmacology
  • RNA, Small Interfering / pharmacology
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Fusion Proteins / immunology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Stochastic Processes
  • Transcription, Genetic
  • Transfection
  • Virus Diseases / immunology*

Substances

  • Interferon Inducers
  • RNA, Double-Stranded
  • RNA, Small Interfering
  • Recombinant Fusion Proteins
  • Brefeldin A
  • Interferon-beta
  • Ddx58 protein, mouse
  • Ifih1 protein, mouse
  • DEAD Box Protein 58
  • DEAD-box RNA Helicases
  • Interferon-Induced Helicase, IFIH1
  • Poly I-C