Raf Kinase Inhibitor Protein Preferentially Promotes TLR3-Triggered Signaling and Inflammation

J Immunol. 2017 May 15;198(10):4086-4095. doi: 10.4049/jimmunol.1601672. Epub 2017 Apr 14.

Abstract

Raf kinase inhibitor protein (RKIP) protects against host immunological responses in nematodes and Drosophila Whether RKIP functions in innate immune responses in mammals remains unknown. In this article, we report that RKIP preferentially regulates the TLR3-mediated immune response in macrophages. RKIP deficiency or silencing significantly decreases polyinosinic:polycytidylic acid [Poly(I:C)]-induced IFN-β, IL-6, and TNF-α production without affecting the counterpart induced by LPS or CpG. Compared with their wild-type counterparts, RKIP-deficient mice produce less IFN-β, IL-6, and TNF-α in serum and display decreased lethality upon peritoneal Poly(I:C) plus d-galactosamine injection. Mechanistically, RKIP interacts with TBK1 and promotes the Poly(I:C)-induced TANK-binding kinase 1/IRF3 activation. Simultaneously, RKIP enhances the Poly(I:C)-induced interaction between TGF-β-activated kinase 1 and MAPK kinase 3 (MKK3), thus promoting MKK3/6 and p38 activation. We further demonstrated that Poly(I:C) treatment, but not LPS treatment, induces RKIP phosphorylation at S109. This action is required for RKIP to promote TANK-binding kinase 1 activation, as well as the interaction between TGF-β-activated kinase 1 and MKK3, which lead to activation of the downstream IRF3 and p38, respectively. Therefore, RKIP acts as a positive-feedback regulator of the TLR3-induced inflammatory response and may be a potential therapeutic target for inflammatory disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Gene Expression Regulation
  • Immunity, Innate
  • Inflammation / immunology*
  • Inflammation / metabolism
  • Interferon Regulatory Factor-3 / immunology
  • Interferon Regulatory Factor-3 / metabolism
  • Interferon-beta / blood
  • Interferon-beta / immunology
  • Interleukin-6 / blood
  • Interleukin-6 / immunology
  • Macrophages / immunology
  • Mice
  • Mitogen-Activated Protein Kinase Kinases / metabolism
  • Phosphatidylethanolamine Binding Protein / deficiency
  • Phosphatidylethanolamine Binding Protein / genetics
  • Phosphatidylethanolamine Binding Protein / metabolism*
  • Phosphorylation
  • Poly I-C / administration & dosage
  • Signal Transduction*
  • Toll-Like Receptor 3 / immunology*
  • Toll-Like Receptor 3 / metabolism*
  • Tumor Necrosis Factor-alpha / blood
  • Tumor Necrosis Factor-alpha / immunology

Substances

  • Interferon Regulatory Factor-3
  • Interleukin-6
  • Irf3 protein, mouse
  • Phosphatidylethanolamine Binding Protein
  • Raf kinase inhibitory protein, mouse
  • TLR3 protein, mouse
  • Toll-Like Receptor 3
  • Tumor Necrosis Factor-alpha
  • Interferon-beta
  • Mitogen-Activated Protein Kinase Kinases
  • Poly I-C