A promiscuous lipid-binding protein diversifies the subcellular sites of toll-like receptor signal transduction

Cell. 2014 Feb 13;156(4):705-16. doi: 10.1016/j.cell.2014.01.019.

Abstract

The Toll-like receptors (TLRs) of the innate immune system are unusual in that individual family members are located on different organelles, yet most activate a common signaling pathway important for host defense. It remains unclear how this common signaling pathway can be activated from multiple subcellular locations. Here, we report that, in response to natural activators of innate immunity, the sorting adaptor TIRAP regulates TLR signaling from the plasma membrane and endosomes. TLR signaling from both locations triggers the TIRAP-dependent assembly of the myddosome, a protein complex that controls proinflammatory cytokine expression. The actions of TIRAP depend on the promiscuity of its phosphoinositide-binding domain. Different lipid targets of this domain direct TIRAP to different organelles, allowing it to survey multiple compartments for the presence of activated TLRs. These data establish how promiscuity, rather than specificity, can be a beneficial means of diversifying the subcellular sites of innate immune signal transduction.

Publication types

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

MeSH terms

  • Animals
  • Cell Membrane / metabolism
  • Endosomes / metabolism
  • Herpes Simplex / immunology
  • Immunity, Innate*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Membrane Glycoproteins / metabolism*
  • Mice, Inbred C57BL
  • Myeloid Differentiation Factor 88 / metabolism
  • Receptors, Interleukin-1 / metabolism*
  • Signal Transduction*
  • Toll-Like Receptors / immunology
  • Toll-Like Receptors / metabolism*

Substances

  • Membrane Glycoproteins
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Receptors, Interleukin-1
  • TIRAP protein, mouse
  • Toll-Like Receptors

Associated data

  • GEO/GSE50436