IFN-epsilon mediates TNF-alpha-induced STAT1 phosphorylation and induction of retinoic acid-inducible gene-I in human cervical cancer cells

J Immunol. 2007 Oct 1;179(7):4542-9. doi: 10.4049/jimmunol.179.7.4542.

Abstract

Retinoic acid inducible gene-I (RIG-I) plays important roles during innate immune responses to viral infections and as a transducer of cytokine signaling. The mechanisms of RIG-I up-regulation after cytokine stimulation are incompletely characterized. It was previously reported that IFN-gamma induces the expression of RIG-I in endothelial cells. In this study, we characterized the mechanism of type I IFN-mediated up-regulation of RIG-I in HeLa cells and found that, in addition to type I IFN, TNF-alpha, a cytokine that regulates innate immune responses, induced expression of RIG-I. To investigate whether TNF-alpha- and type I IFN-mediated up-regulations of RIG-I were causally related, we studied the kinetics of these responses. Our results were consistent with a model in which TNF-alpha functioned upstream of type I IFNs. The ability of TNF-alpha to up-regulate RIG-I required protein synthesis, expression of functional type I IFNRs, and STAT1 signaling. We also found that IFN-epsilon was the only IFN isoform expressed constitutively in HeLa cells and that its expression was up-regulated in response to stimulation with TNF-alpha. The mechanism of up-regulation involved stabilization of IFN-epsilon mRNA in the absence of transcriptional activation. Silencing the expression of IFN-epsilon attenuated STAT1 expression and phosphorylation and inhibited RIG-I expression, providing additional support for the participation of IFN-epsilon upstream of STAT1. Our findings support a sequential mechanism whereby TNF-alpha leads to stabilization of IFN-epsilon mRNA, increased IFN-epsilon synthesis, engagement of type I IFNRs, increased STAT1 expression and phosphorylation, and up-regulation of RIG-I expression. These findings have implications for our understanding of the immune responses that follow cytokine stimulation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • DEAD Box Protein 58
  • DEAD-box RNA Helicases / metabolism*
  • Female
  • HeLa Cells
  • Humans
  • Interferons / genetics
  • Interferons / metabolism*
  • Phosphorylation / drug effects
  • Promoter Regions, Genetic / genetics
  • RNA, Messenger / genetics
  • Receptors, Immunologic
  • Receptors, Interferon / classification
  • Receptors, Interferon / metabolism
  • STAT1 Transcription Factor / metabolism*
  • Signal Transduction
  • Tumor Necrosis Factor-alpha / pharmacology*
  • Up-Regulation / drug effects
  • Uterine Cervical Neoplasms / genetics
  • Uterine Cervical Neoplasms / metabolism*

Substances

  • IFNE protein, human
  • RNA, Messenger
  • Receptors, Immunologic
  • Receptors, Interferon
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Tumor Necrosis Factor-alpha
  • Interferons
  • RIGI protein, human
  • DEAD Box Protein 58
  • DEAD-box RNA Helicases