Flavonoid extracted from Epimedium attenuate cGAS-STING-mediated diseases by targeting the formation of functional STING signalosome

Immunology. 2024 Jun;172(2):295-312. doi: 10.1111/imm.13771. Epub 2024 Mar 7.

Abstract

Hyperactivation of the cyclic-GMP-AMP synthase (cGAS)-stimulator of interferon genes (STING) signalling pathway has been shown to be associated with the development of a variety of inflammatory diseases, and the discovery of an inhibitor of the cGAS-STING signalling pathway holds great promise in the therapeutic interventions. Epimedium flavonoid (EF), a major active ingredient isolated from the medicinal plant Epimedium, has been reported to have good anti-inflammatory activity, but its exact mechanism of action remains unclear. In the present study, we found that EF in mouse bone marrow-derived macrophages (BMDMs), THP-1 (Tohoku Hospital Pediatrics-1) as well as in human peripheral blood mononuclear cells (hPBMC) inhibited the activation of the cGAS-STING signalling pathway, which subsequently led to a decrease in the expression of type I interferon (IFN-β, CXCL10 and ISG15) and pro-inflammatory cytokines (IL-6 and TNF-α). Mechanistically, EF does not affect STING oligomerization, but inhibits the formation of functional STING signalosome by attenuating the interaction of interferon regulatory factor 3 (IRF3) with STING and TANK-binding kinase 1 (TBK1). Importantly, in vivo experiments, EF has shown promising therapeutic effects on inflammatory diseases mediated by the cGAS-STING pathway, which include the agonist model induced by DMXAA stimulation, the autoimmune inflammatory disease model induced by three prime repair exonuclease 1 (Trex1) deficiency, and the non-alcoholic steatohepatitis (NASH) model induced by a pathogenic amino acid and choline deficiency diet (MCD). To summarize, our study suggests that EF is a potent potential inhibitor component of the cGAS-STING signalling pathway for the treatment of inflammatory diseases mediated by the cGAS-STING signalling pathway.

Keywords: Epimedium flavonoid; autoimmune diseases; cGAS‐STING; inflammatory diseases; non‐alcoholic steatohepatitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Cytokines / metabolism
  • Epimedium* / chemistry
  • Flavonoids* / pharmacology
  • Humans
  • Interferon Regulatory Factor-3 / metabolism
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / immunology
  • Leukocytes, Mononuclear / metabolism
  • Macrophages / drug effects
  • Macrophages / immunology
  • Macrophages / metabolism
  • Membrane Proteins* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Nucleotidyltransferases* / metabolism
  • Protein Serine-Threonine Kinases / metabolism
  • Signal Transduction* / drug effects
  • THP-1 Cells

Substances

  • Nucleotidyltransferases
  • Membrane Proteins
  • Flavonoids
  • Sting1 protein, mouse
  • STING1 protein, human
  • Interferon Regulatory Factor-3
  • cGAS protein, mouse
  • Cytokines
  • Protein Serine-Threonine Kinases
  • cGAS protein, human
  • Tbk1 protein, mouse
  • Anti-Inflammatory Agents