Sterile inflammation via TRPM8 RNA-dependent TLR3-NF-kB/IRF3 activation promotes antitumor immunity in prostate cancer

EMBO J. 2024 Mar;43(5):780-805. doi: 10.1038/s44318-024-00040-5. Epub 2024 Feb 5.

Abstract

Inflammation is a common condition of prostate tissue, whose impact on carcinogenesis is highly debated. Microbial colonization is a well-documented cause of a small percentage of prostatitis cases, but it remains unclear what underlies the majority of sterile inflammation reported. Here, androgen- independent fluctuations of PSA expression in prostate cells have lead us to identify a prominent function of the Transient Receptor Potential Cation Channel Subfamily M Member 8 (TRPM8) gene in sterile inflammation. Prostate cells secret TRPM8 RNA into extracellular vesicles (EVs), which primes TLR3/NF-kB-mediated inflammatory signaling after EV endocytosis by epithelial cancer cells. Furthermore, prostate cancer xenografts expressing a translation-defective form of TRPM8 RNA contain less collagen type I in the extracellular matrix, significantly more infiltrating NK cells, and larger necrotic areas as compared to control xenografts. These findings imply sustained, androgen-independent expression of TRPM8 constitutes as a promoter of anticancer innate immunity, which may constitute a clinically relevant condition affecting prostate cancer prognosis.

Keywords: Immunity; Inflammation; PSA; Prostate; TRP.

MeSH terms

  • Androgens
  • Animals
  • Humans
  • Inflammation / genetics
  • Interferon Regulatory Factor-3
  • Male
  • Membrane Proteins
  • NF-kappa B / genetics
  • Prostatic Neoplasms* / genetics
  • TRPM Cation Channels* / genetics
  • Toll-Like Receptor 3 / genetics

Substances

  • Androgens
  • Interferon Regulatory Factor-3
  • IRF3 protein, human
  • Membrane Proteins
  • NF-kappa B
  • TLR3 protein, human
  • Toll-Like Receptor 3
  • TRPM Cation Channels
  • TRPM8 channel-associated factor 1 protein, human
  • TRPM8 protein, human