Prostate cancer is the most frequently diagnosed non-skin cancer and a leading cause of cancer-related death in men worldwide. The key driver of prostate cancer is the androgen receptor (AR); thus, AR-targeted therapies are the primary treatment strategy for metastatic prostate cancer. While most men initially respond to AR-targeted therapies, they are not always curative and patients inevitably progress to a highly aggressive and lethal disease state termed castration-resistant prostate cancer (CRPC). Therefore, the development of new and effective treatment options for CRPC is essential to improve patient outcomes.
A plausible therapeutic target in CRPC is cyclin-dependent kinase 9 (CDK9), which regulates transcriptional elongation by phosphorylating RNA polymerase II. Dysregulated transcriptional activity due to elevated CDK9 activity has been observed in various haematological and solid cancers, and CDK9 inhibitors are now being investigated in clinical trials. In this study, we describe the efficacy of a novel and orally bioavailable CDK9 inhibitor, CDKI-73, in prostate cancer. CDKI-73 potently inhibits proliferation in a range of prostate cancer cell lines representing distinct CRPC subtypes and causes cell death by apoptosis. CDKI-73 was also found to be highly effective in more clinically relevant systems, including patient-derived organoids, patient-derived tumour explants and mouse xenografts. Mechanistically, CDKI-73-mediated inhibition of RNA polymerase II serine 2 phosphorylation resulted in reduced expression of anti-apoptotic factors and defects in overall transcription. Moreover, transcriptomic and epigenomic approaches revealed that CDKI-73 suppressed signalling pathways regulated by AR, MYC and BRD4, which are key drivers of dysregulated transcription in prostate cancer, and led to reprogramming of cancer-associated super-enhancers. These latter findings prompted the evaluation of CDKI-73 with the BRD4 inhibitor AZD5153, a combination that was synergistic in patient-derived organoids and in vivo. Collectively, our evaluation provides new insights into CDK9’s oncogenic activity and reveals CDKI-73 as a promising therapeutic agent for prostate cancer.