AP-1 activates KCNN4-mediated Ca2+ signaling to induce the Th1/Th17 differentiation of CD4+ cells in chronic non-bacterial prostatitis

Cell Biol Toxicol. 2024 Dec 27;41(1):18. doi: 10.1007/s10565-024-09967-1.

Abstract

The intraprostatic inflammatory infiltrate is characterized by Th1 CD4+ T cells, and its molecular mechanism is not well defined. This study explored the mechanisms responsible for the alteration of Th1/Th17 differentiation of CD4+ T cells in chronic non-bacterial prostatitis (CNP). CNP rats were induced by the administration of testosterone and 17β-estradiol. The Th1/Th17 cell percentage was increased in the prostate tissue of CNP rats, which was accompanied by increased IL-2, IFN-γ, IL-17A, and IL-22 levels. Transcriptome sequencing was performed, followed by KEGG pathway enrichment analysis. Activator protein-1 (AP-1) was enhanced in CD4+ T cells from CNP rats, and its inhibitor SR11302 suppressed Th1/Th17 differentiation and delayed CNP. AP-1 transcriptionally activated the expression of KCNN4, which potentiated mTORC1 in CD4+ T cells by enhancing Ca2+ signaling, thereby promoting Th1/Th17 differentiation. Rapamycin-mediated autophagy activation reversed AP-1/KCNN4/mTORC1-promoted Th1/Th17 differentiation, thereby inhibiting CNP. These results suggest that AP-1-mediated KCNN4 transcription promotes the inhibition of autophagy by mTORC1 through Ca2+ signaling, which supports Th1/Th17 differentiation of CD4+ T cells, resulting in the transformation of CNP to prostatic intraepithelial neoplasia and adenocarcinoma.

Keywords: AP-1; Chronic non-bacterial prostatitis; KCNN4; MTORC1; Th1/Th17.

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes* / drug effects
  • CD4-Positive T-Lymphocytes* / immunology
  • CD4-Positive T-Lymphocytes* / metabolism
  • Calcium Signaling* / drug effects
  • Cell Differentiation* / drug effects
  • Chronic Disease
  • Intermediate-Conductance Calcium-Activated Potassium Channels / genetics
  • Intermediate-Conductance Calcium-Activated Potassium Channels / metabolism
  • Male
  • Prostatitis* / immunology
  • Prostatitis* / metabolism
  • Prostatitis* / pathology
  • Rats
  • Rats, Sprague-Dawley
  • Th1 Cells* / drug effects
  • Th1 Cells* / immunology
  • Th1 Cells* / metabolism
  • Th17 Cells* / drug effects
  • Th17 Cells* / immunology
  • Th17 Cells* / metabolism
  • Transcription Factor AP-1* / metabolism

Substances

  • Transcription Factor AP-1
  • Intermediate-Conductance Calcium-Activated Potassium Channels