Interleukin 1 receptor signaling regulates DUBA expression and facilitates Toll-like receptor 9-driven antiinflammatory cytokine production

J Exp Med. 2010 Dec 20;207(13):2799-807. doi: 10.1084/jem.20101326. Epub 2010 Nov 29.

Abstract

The interleukin 1 receptor (IL-1R) and the Toll-like receptors (TLRs) are highly homologous innate immune receptors that provide the first line of defense against infection. We show that IL-1R type I (IL-1RI) is essential for TLR9-dependent activation of tumor necrosis factor receptor-associated factor 3 (TRAF3) and for production of the antiinflammatory cytokines IL-10 and type I interferon (IFN). Noncanonical K63-linked ubiquitination of TRAF3, which is essential for type I IFN and IL-10 production, was impaired in Il1r1(-/-) CD11c(+) dendritic cells. In contrast, degradative ubiquitination of TRAF3 was not affected in the absence of IL-1R1 signaling. Deubiquitinating enzyme A (DUBA), which selectively cleaves K63-linked ubiquitin chains from TRAF3, was up-regulated in the absence of IL-1R1 signaling. DUBA short interference RNA augmented the TLR9-dependent type I IFN response. Mice deficient in IL-1RI signaling showed reduced expression of IL-10 and type I IFN and increased susceptibility to dextran sulphate sodium-induced colitis and failed to mount a protective type I IFN response after TLR9 ligand (CpG) administration. Our data identifies a new molecular pathway by which IL-1 signaling attenuates TLR9-mediated proinflammatory responses.

Publication types

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

MeSH terms

  • Animals
  • Cells, Cultured
  • Colitis / chemically induced
  • Colitis / genetics
  • Colitis / metabolism
  • Cytokines / metabolism*
  • Dendritic Cells / cytology
  • Dendritic Cells / drug effects
  • Dendritic Cells / metabolism
  • Dextran Sulfate
  • Endopeptidases / genetics
  • Endopeptidases / metabolism*
  • Female
  • Immediate-Early Proteins / genetics
  • Immediate-Early Proteins / metabolism*
  • Immunoblotting
  • Interferon Type I / genetics
  • Interferon Type I / metabolism
  • Interferon-beta / metabolism
  • Interleukin-10 / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Oligodeoxyribonucleotides / pharmacology
  • RNA Interference
  • Receptors, Interleukin-1 / deficiency
  • Receptors, Interleukin-1 / genetics
  • Receptors, Interleukin-1 / physiology*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction
  • TNF Receptor-Associated Factor 3 / genetics
  • TNF Receptor-Associated Factor 3 / metabolism
  • Toll-Like Receptor 9 / genetics
  • Toll-Like Receptor 9 / metabolism*

Substances

  • Cytokines
  • Immediate-Early Proteins
  • Interferon Type I
  • Oligodeoxyribonucleotides
  • Receptors, Interleukin-1
  • TNF Receptor-Associated Factor 3
  • Toll-Like Receptor 9
  • Interleukin-10
  • Interferon-beta
  • Dextran Sulfate
  • Dub2a protein, mouse
  • Endopeptidases