AR loss in prostate cancer stroma mediated by NF-κB and p38-MAPK signaling disrupts stromal morphogen production

Oncogene. 2024 Jun;43(27):2092-2103. doi: 10.1038/s41388-024-03064-7. Epub 2024 May 20.

Abstract

Androgen Receptor (AR) activity in prostate stroma is required to maintain prostate homeostasis. This is mediated through androgen-dependent induction and secretion of morphogenic factors that drive epithelial cell differentiation. However, stromal AR expression is lost in aggressive prostate cancer. The mechanisms leading to stromal AR loss and morphogen production are unknown. We identified TGFβ1 and TNFα as tumor-secreted factors capable of suppressing AR mRNA and protein expression in prostate stromal fibroblasts. Pharmacological and RNAi approaches identified NF-κB as the major signaling pathway involved in suppressing AR expression by TNFα. In addition, p38α- and p38δ-MAPK were identified as suppressors of AR expression independent of TNFα. Two regions of the AR promoter were responsible for AR suppression through TNFα. FGF10 and Wnt16 were identified as androgen-induced morphogens, whose expression was lost upon TNFα treatment and enhanced upon p38-MAPK inhibition. Wnt16, through non-canonical Jnk signaling, was required for prostate basal epithelial cell survival. These findings indicate that stromal AR loss is mediated by secreted factors within the TME. We identified TNFα/TGFβ as two possible factors, with TNFα mediating its effects through NF-κB or p38-MAPK to suppress AR mRNA transcription. This leads to loss of androgen-regulated stromal morphogens necessary to maintain normal epithelial homeostasis.

MeSH terms

  • Cell Line, Tumor
  • Gene Expression Regulation, Neoplastic
  • Humans
  • MAP Kinase Signaling System / genetics
  • Male
  • NF-kappa B* / metabolism
  • Prostate / metabolism
  • Prostate / pathology
  • Prostatic Neoplasms* / genetics
  • Prostatic Neoplasms* / metabolism
  • Prostatic Neoplasms* / pathology
  • Receptors, Androgen* / genetics
  • Receptors, Androgen* / metabolism
  • Signal Transduction
  • Stromal Cells* / metabolism
  • Stromal Cells* / pathology
  • Transforming Growth Factor beta1 / genetics
  • Transforming Growth Factor beta1 / metabolism
  • Tumor Necrosis Factor-alpha / metabolism
  • Wnt Proteins / genetics
  • Wnt Proteins / metabolism
  • p38 Mitogen-Activated Protein Kinases* / genetics
  • p38 Mitogen-Activated Protein Kinases* / metabolism

Substances

  • NF-kappa B
  • Receptors, Androgen
  • p38 Mitogen-Activated Protein Kinases
  • Tumor Necrosis Factor-alpha
  • AR protein, human
  • Transforming Growth Factor beta1
  • Wnt Proteins