Targeting the KDM4B-AR-c-Myc axis promotes sensitivity to androgen receptor-targeted therapy in advanced prostate cancer

J Pathol. 2020 Oct;252(2):101-113. doi: 10.1002/path.5495. Epub 2020 Aug 28.

Abstract

The histone demethylase KDM4B functions as a key co-activator for the androgen receptor (AR) and plays a vital in multiple cancers through controlling gene expression by epigenetic regulation of H3K9 methylation marks. Constitutively active androgen receptor confers anti-androgen resistance in advanced prostate cancer. However, the role of KDM4B in resistance to next-generation anti-androgens and the mechanisms of KDM4B regulation are poorly defined. Here we found that KDM4B is overexpressed in enzalutamide-resistant prostate cancer cells. Overexpression of KDM4B promoted recruitment of AR to the c-Myc (MYC) gene enhancer and induced H3K9 demethylation, increasing AR-dependent transcription of c-Myc mRNA, which regulates the sensitivity to next-generation AR-targeted therapy. Inhibition of KDM4B significantly inhibited prostate tumor cell growth in xenografts, and improved enzalutamide treatments through suppression of c-Myc. Clinically, KDM4B expression was found upregulated and to correlate with prostate cancer progression and poor prognosis. Our results revealed a novel mechanism of anti-androgen resistance via histone demethylase alteration which could be targeted through inhibition of KDM4B to reduce AR-dependent c-Myc expression and overcome resistance to AR-targeted therapies. © 2020 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.

Keywords: KDM4B; androgen receptor; c-Myc; castration-resistant prostate cancer; enzalutamide resistance; histone demethylase; prostate cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / metabolism*
  • Adenocarcinoma / pathology
  • Androgen Receptor Antagonists / pharmacology
  • Animals
  • Cell Line, Tumor
  • Cell Proliferation / physiology
  • Drug Resistance, Neoplasm / physiology*
  • Humans
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Prostatic Neoplasms, Castration-Resistant / metabolism*
  • Prostatic Neoplasms, Castration-Resistant / pathology
  • Proto-Oncogene Proteins c-myc / metabolism

Substances

  • Androgen Receptor Antagonists
  • MYC protein, human
  • Proto-Oncogene Proteins c-myc
  • Jumonji Domain-Containing Histone Demethylases
  • KDM4B protein, human