TLR4 signaling and macrophage inflammatory responses are dampened by GIV/Girdin

Proc Natl Acad Sci U S A. 2020 Oct 27;117(43):26895-26906. doi: 10.1073/pnas.2011667117. Epub 2020 Oct 14.

Abstract

Sensing of pathogens by Toll-like receptor 4 (TLR4) induces an inflammatory response; controlled responses confer immunity but uncontrolled responses cause harm. Here we define how a multimodular scaffold, GIV (a.k.a. Girdin), titrates such inflammatory response in macrophages. Upon challenge with either live microbes or microbe-derived lipopolysaccharides (a ligand for TLR4), macrophages with GIV mount a more tolerant (hypo-reactive) transcriptional response and suppress proinflammatory cytokines and signaling pathways (i.e., NFkB and CREB) downstream of TLR4 compared to their GIV-depleted counterparts. Myeloid-specific gene-depletion studies confirmed that the presence of GIV ameliorates dextran sodium sulfate-induced colitis and sepsis-induced death. The antiinflammatory actions of GIV are mediated via its C-terminally located TIR-like BB-loop (TILL) motif which binds the cytoplasmic TIR modules of TLR4 in a manner that precludes receptor dimerization; such dimerization is a prerequisite for proinflammatory signaling. Binding of GIV's TILL motif to TIR modules inhibits proinflammatory signaling via other TLRs, suggesting a convergent paradigm for fine-tuning macrophage inflammatory responses.

Keywords: Girdin; TIR domain; ccdc88a; inflammation; macrophages.

Publication types

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

MeSH terms

  • Animals
  • Colitis / metabolism
  • Disease Models, Animal
  • Female
  • HEK293 Cells
  • Humans
  • Macrophages / metabolism
  • Mice
  • Mice, Knockout
  • Microfilament Proteins / metabolism*
  • RAW 264.7 Cells
  • Sepsis / metabolism
  • Signal Transduction
  • Toll-Like Receptor 4 / metabolism*
  • Vesicular Transport Proteins / metabolism*

Substances

  • Ccdc88a protein, mouse
  • Microfilament Proteins
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Vesicular Transport Proteins
  • girdin protein, mouse