Structural basis for TIR domain-mediated innate immune signaling by Toll-like receptor adaptors TRIF and TRAM

Proc Natl Acad Sci U S A. 2025 Jan 14;122(2):e2418988122. doi: 10.1073/pnas.2418988122. Epub 2025 Jan 9.

Abstract

Innate immunity relies on Toll-like receptors (TLRs) to detect pathogen-associated molecular patterns. The TIR (Toll/interleukin-1 receptor) domain-containing TLR adaptors TRIF (TIR domain-containing adaptor-inducing interferon-β) and TRAM (TRIF-related adaptor molecule) are essential for MyD88-independent TLR signaling. However, the structural basis of TRIF and TRAM TIR domain-based signaling remains unclear. Here, we present cryo-EM structures of filaments formed by TRIF and TRAM TIR domains at resolutions of 3.3 Å and 5.6 Å, respectively. Both structures reveal two-stranded parallel helical arrangements. Functional studies underscore the importance of intrastrand interactions, mediated by the BB-loop, and interstrand interactions in TLR4-mediated signaling. We also report the crystal structure of the monomeric TRAM TIR domain bearing the BB loop mutation C117H, which reveals conformational differences consistent with its inactivity. Our findings suggest a unified signaling mechanism by the TIR domains of the four signaling TLR adaptors MyD88, MAL, TRIF, and TRAM and reveal potential therapeutic targets for immunity-related disorders.

Keywords: MyD88-independent TLR signaling; TIR domain; cryo-EM; helical reconstruction.

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport* / chemistry
  • Adaptor Proteins, Vesicular Transport* / genetics
  • Adaptor Proteins, Vesicular Transport* / immunology
  • Adaptor Proteins, Vesicular Transport* / metabolism
  • Cryoelectron Microscopy
  • Crystallography, X-Ray
  • HEK293 Cells
  • Humans
  • Immunity, Innate*
  • Models, Molecular
  • Myeloid Differentiation Factor 88 / chemistry
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / metabolism
  • Protein Domains
  • Receptors, Interleukin-1 / chemistry
  • Receptors, Interleukin-1 / genetics
  • Receptors, Interleukin-1 / immunology
  • Receptors, Interleukin-1 / metabolism
  • Signal Transduction* / immunology
  • Toll-Like Receptor 4 / chemistry
  • Toll-Like Receptor 4 / immunology
  • Toll-Like Receptor 4 / metabolism
  • Toll-Like Receptors / immunology
  • Toll-Like Receptors / metabolism

Substances

  • Adaptor Proteins, Vesicular Transport
  • TICAM1 protein, human
  • Receptors, Interleukin-1
  • Toll-Like Receptor 4
  • TICAM2 protein, human
  • Myeloid Differentiation Factor 88
  • Toll-Like Receptors
  • TLR4 protein, human
  • Adaptor Proteins, Signal Transducing