Promotion of TLR7-MyD88-dependent inflammation and autoimmunity in mice through stem-loop changes in Lnc-Atg16l1

Nat Commun. 2024 Nov 25;15(1):10224. doi: 10.1038/s41467-024-54674-4.

Abstract

Uncontrolled TLR signaling can cause inflammatory immunopathology and trigger autoimmune diseases. For example, TLR7 promotes pathogenesis of systemic lupus erythematosus. However, whether RNA structural changes affect nucleic acids-sensing TLRs signaling and impact disease progression is unclear. Here by iCLIP-seq we identify a TLR7-binding long non-coding RNA, Lnc-Atg16l1, and find that it promotes TLR7 and other MyD88-dependent TLRs signaling in various types of immune cells. Depletion of Lnc-Atg16l1 attenuates development of TLR7-linked autoimmune phenotypes in the mouse SLE model. Mechanistically, we find that Lnc-Atg16l1 binds to TLR7 at bases near U84 and MyD88 at bases around A129. The analysis of Lnc-Atg16l1 in situ structures show that it strengthens the interaction between TIR domain of TLR7 and MyD88 through specific stem-loop structure changes as a molecular scaffold after TLR7 activation to promote TLR7 downstream signaling. Therefore, we discover a mechanism for host RNA regulation of innate signaling and autoimmune disease through its structural changes. These findings provide insights into the pro-inflammatory function of self RNA in a structure-dependent manner and suggest a potential target for TLR-related autoimmune disorders.

MeSH terms

  • Animals
  • Autoimmunity* / genetics
  • Disease Models, Animal
  • Female
  • HEK293 Cells
  • Humans
  • Inflammation* / genetics
  • Inflammation* / immunology
  • Lupus Erythematosus, Systemic / genetics
  • Lupus Erythematosus, Systemic / immunology
  • Membrane Glycoproteins* / genetics
  • Membrane Glycoproteins* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myeloid Differentiation Factor 88* / genetics
  • Myeloid Differentiation Factor 88* / metabolism
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / immunology
  • RNA, Long Noncoding* / metabolism
  • Signal Transduction*
  • Toll-Like Receptor 7* / genetics
  • Toll-Like Receptor 7* / metabolism

Substances

  • Toll-Like Receptor 7
  • Myeloid Differentiation Factor 88
  • Tlr7 protein, mouse
  • RNA, Long Noncoding
  • Myd88 protein, mouse
  • Membrane Glycoproteins