Increased antiandrogen enzalutamide sensitivity via altering prostate cancer stem cell traits through modulating the androgen receptor-mediated CDR1/circCDR1-AS/miR-1290/BMP4 signaling

Oncogene. 2025 Sep;44(35):3199-3212. doi: 10.1038/s41388-025-03482-1. Epub 2025 Jul 4.

Abstract

While the recent FDA-approved antiandrogen enzalutamide (Enz) might prolong the survival of castration-resistant prostate cancer (CRPC) patients by an additional 4.8 months, most patients eventually might still develop Enz resistance within 6-12 months. Although few genes have been linked to Enz resistance in prostate cancer (PCa), the detailed mechanism(s) are still underinvestigated. Here, we found that Enz might function by altering androgen receptor(AR)-mediated CDR1/circCDR1-AS/miR-1290/BMP4 signaling to modulate PCa stem cells (CSCs) to increase Enz resistance. Mechanistic analysis revealed that Enz/AR signaling can transcriptionally regulate CDR1 expression by reducing binding to androgen response elements (AREs) on the CDR1 5' promoter to alter circCDR1-AS expression. Enz/AR/CDR1/circCDR1-AS signaling might then increase BMP4 expression by altering miR-1290 expression, which involves direct binding to the 3' UTR of BMP4 mRNA. Preclinical studies using a CWR22Rv1 xenograft mouse model and integrative analysis of GEO cohort data further demonstrated that targeting this newly identified Enz/AR/CDR1/circCDR1-AS/miR-1290/BMP4 signaling pathway with miR-1290, circCDR1-AS-shRNA, or BMP4-shRNA may help develop novel therapies to combat Enz resistance at the later stage of CRPC.

MeSH terms

  • Androgen Antagonists* / pharmacology
  • Animals
  • Benzamides* / pharmacology
  • Bone Morphogenetic Protein 4 / genetics
  • Bone Morphogenetic Protein 4 / metabolism
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Male
  • Mice
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Neoplastic Stem Cells* / drug effects
  • Neoplastic Stem Cells* / metabolism
  • Neoplastic Stem Cells* / pathology
  • Nitriles / pharmacology
  • Phenylthiohydantoin* / analogs & derivatives
  • Phenylthiohydantoin* / pharmacology
  • Prostatic Neoplasms* / drug therapy
  • Prostatic Neoplasms* / genetics
  • Prostatic Neoplasms* / pathology
  • Prostatic Neoplasms, Castration-Resistant* / drug therapy
  • Prostatic Neoplasms, Castration-Resistant* / genetics
  • Prostatic Neoplasms, Castration-Resistant* / metabolism
  • Prostatic Neoplasms, Castration-Resistant* / pathology
  • Receptors, Androgen* / genetics
  • Receptors, Androgen* / metabolism
  • Signal Transduction / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • enzalutamide
  • Phenylthiohydantoin
  • Receptors, Androgen
  • MicroRNAs
  • Bone Morphogenetic Protein 4
  • Benzamides
  • BMP4 protein, human
  • Androgen Antagonists
  • Nitriles
  • AR protein, human