c-Kit-Mediated PI3K/AKT and Wnt/β-Catenin Signaling Drives Resistance to 5α-Reductase Inhibitors in Benign Prostatic Hyperplasia

Prostate. 2025 Dec;85(16):1541-1555. doi: 10.1002/pros.70046. Epub 2025 Sep 29.

Abstract

Background: Resistance to 5α-reductase inhibitors (5ARIs) represents a significant therapeutic challenge in benign prostatic hyperplasia (BPH) clinical management. While the c-Kit-mediated signaling has been implicated in various pathological conditions, its role in BPH and 5ARI resistance remains undefined.

Methods: Patient-derived organoids (PDOs) were established from BPH specimens and characterized through immunofluorescence, immunohistochemistry, and RT-qPCR analysis. Transcriptomic profiling was performed to identify differentially expressed genes between 5ARI-sensitive and resistant samples. The functional significance of c-Kit-mediated signaling was evaluated using selective inhibitor ISCK03. Further analysis identified cellular targets of c-Kit inhibition, and downstream signaling mechanisms were characterized through pathway analysis.

Results: RNA sequencing revealed differentially expressed genes between 5ARI-sensitive and resistant BPH PDOs, with significant enrichment in KIT and related genes. Enhanced c-Kit expression was confirmed in 5ARI-resistant specimens through multiple methodologies. Selective c-Kit inhibition with ISCK03 specifically suppressed 5ARI-resistant PDOs proliferation while sparing sensitive ones. Tests utilizing single-cell-derived organoids identified basal epithelial cells as primary targets of c-Kit inhibition. Mechanistic studies demonstrated that c-Kit maintains 5ARI resistance through the PI3K/AKT and Wnt/β-catenin signaling axis, with c-Kit inhibition significantly downregulating this pathway.

Conclusions: c-Kit-mediated signaling is associated with 5ARI resistance in BPH, potentially through modulation of PI3K/AKT and Wnt/β-catenin pathways. These findings highlight c-Kit as a potential therapeutic target for overcoming 5ARI resistance.

Keywords: 5α‐reductase inhibitors; benign prostatic hyperplasia; c‐Kit; drug resistance; patient‐derived organoids.

MeSH terms

  • 5-alpha Reductase Inhibitors* / pharmacology
  • 5-alpha Reductase Inhibitors* / therapeutic use
  • Humans
  • Male
  • Organoids / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Prostatic Hyperplasia* / drug therapy
  • Prostatic Hyperplasia* / genetics
  • Prostatic Hyperplasia* / metabolism
  • Prostatic Hyperplasia* / pathology
  • Proto-Oncogene Proteins c-akt* / metabolism
  • Proto-Oncogene Proteins c-kit* / genetics
  • Proto-Oncogene Proteins c-kit* / metabolism
  • Wnt Signaling Pathway* / drug effects
  • Wnt Signaling Pathway* / physiology
  • beta Catenin / metabolism

Substances

  • Proto-Oncogene Proteins c-kit
  • Proto-Oncogene Proteins c-akt
  • 5-alpha Reductase Inhibitors
  • Phosphatidylinositol 3-Kinases
  • beta Catenin
  • KIT protein, human