Polycomb- and Methylation-Independent Roles of EZH2 as a Transcription Activator

Cell Rep. 2018 Dec 4;25(10):2808-2820.e4. doi: 10.1016/j.celrep.2018.11.035.

Abstract

Enhancer of Zeste 2 (EZH2) is the enzymatic subunit of Polycomb Repressive Complex 2 (PRC2), which catalyzes histone H3 lysine 27 trimethylation (H3K27me3) at target promoters for gene silencing. Here, we report that EZH2 activates androgen receptor (AR) gene transcription through direct occupancy at its promoter. Importantly, this activating role of EZH2 is independent of PRC2 and its methyltransferase activities. Genome-wide assays revealed extensive EZH2 occupancy at promoters marked by either H3K27ac or H3K27me3, leading to gene activation or repression, respectively. Last, we demonstrate enhanced efficacy of enzymatic EZH2 inhibitors when used in combination with AR antagonists in blocking the dual roles of EZH2 and suppressing prostate cancer progression in vitro and in vivo. Taken together, our study reports EZH2 as a transcriptional activator, a key target of which is AR, and suggests a drug-combinatory approach to treat advanced prostate cancer.

Keywords: AR antagonist enzalutamide; ChIP-seq; EPZ-6438; GSK126; androgen receptor inhibitor; enzymatic EZH2 inhibitor; epigenetic silencing; transcription activator.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Androgens / metabolism
  • Animals
  • Base Sequence
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Cell Line, Tumor
  • Cell Proliferation
  • Enhancer of Zeste Homolog 2 Protein / metabolism*
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • Histone Methyltransferases / metabolism
  • Humans
  • Male
  • Methylation
  • Mice, Inbred NOD
  • Polycomb Repressive Complex 2 / metabolism*
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / pathology
  • Protein Binding
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Androgen / genetics
  • Receptors, Androgen / metabolism
  • Signal Transduction
  • Trans-Activators / metabolism*
  • Transcription, Genetic

Substances

  • AR protein, human
  • Androgens
  • RNA, Messenger
  • Receptors, Androgen
  • Trans-Activators
  • Histone Methyltransferases
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • Polycomb Repressive Complex 2