The Dual Inhibition of RNA Pol I Transcription and PIM Kinase as a New Therapeutic Approach to Treat Advanced Prostate Cancer

Clin Cancer Res. 2016 Nov 15;22(22):5539-5552. doi: 10.1158/1078-0432.CCR-16-0124. Epub 2016 Aug 2.

Abstract

Purpose: The MYC oncogene is frequently overexpressed in prostate cancer. Upregulation of ribosome biogenesis and function is characteristic of MYC-driven tumors. In addition, PIM kinases activate MYC signaling and mRNA translation in prostate cancer and cooperate with MYC to accelerate tumorigenesis. Here, we investigate the efficacy of a single and dual approach targeting ribosome biogenesis and function to treat prostate cancer.

Experimental design: The inhibition of ribosomal RNA (rRNA) synthesis with CX-5461, a potent, selective, and orally bioavailable inhibitor of RNA polymerase I (Pol I) transcription, has been successfully exploited therapeutically but only in models of hematologic malignancy. CX-5461 and CX-6258, a pan-PIM kinase inhibitor, were tested alone and in combination in prostate cancer cell lines, in Hi-MYC- and PTEN-deficient mouse models and in patient-derived xenografts (PDX) of metastatic tissue obtained from a patient with castration-resistant prostate cancer.

Results: CX-5461 inhibited anchorage-independent growth and induced cell-cycle arrest in prostate cancer cell lines at nanomolar concentrations. Oral administration of 50 mg/kg CX-5461 induced TP53 expression and activity and reduced proliferation (MKI67) and invasion (loss of ductal actin) in Hi-MYC tumors, but not in PTEN-null (low MYC) tumors. While 100 mg/kg CX-6258 showed limited effect alone, its combination with CX-5461 further suppressed proliferation and dramatically reduced large invasive lesions in both models. This rational combination strategy significantly inhibited proliferation and induced cell death in PDX of prostate cancer.

Conclusions: Our results demonstrate preclinical efficacy of targeting the ribosome at multiple levels and provide a new approach for the treatment of prostate cancer. Clin Cancer Res; 22(22); 5539-52. ©2016 AACR.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Azepines / pharmacology
  • Benzothiazoles / pharmacology
  • Cell Cycle Checkpoints / drug effects
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Female
  • Humans
  • Indoles / pharmacology
  • Male
  • Mice
  • Naphthyridines / pharmacology
  • PTEN Phosphohydrolase / metabolism
  • Prostate / drug effects
  • Prostate / metabolism
  • Prostatic Neoplasms / drug therapy*
  • Prostatic Neoplasms / metabolism
  • Protein Kinase Inhibitors / pharmacology*
  • Proto-Oncogene Proteins c-myc / metabolism
  • Proto-Oncogene Proteins c-pim-1 / antagonists & inhibitors*
  • RNA Polymerase I / antagonists & inhibitors*
  • Signal Transduction / drug effects
  • Transcription, Genetic / drug effects*
  • Xenograft Model Antitumor Assays / methods

Substances

  • Antineoplastic Agents
  • Azepines
  • Benzothiazoles
  • CX 5461
  • CX-6258
  • Indoles
  • Naphthyridines
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins c-myc
  • Proto-Oncogene Proteins c-pim-1
  • proto-oncogene proteins pim
  • RNA Polymerase I
  • PTEN Phosphohydrolase