ERG signaling in prostate cancer is driven through PRMT5-dependent methylation of the Androgen Receptor

Elife. 2016 May 16:5:e13964. doi: 10.7554/eLife.13964.

Abstract

The TMPRSS2:ERG gene fusion is common in androgen receptor (AR) positive prostate cancers, yet its function remains poorly understood. From a screen for functionally relevant ERG interactors, we identify the arginine methyltransferase PRMT5. ERG recruits PRMT5 to AR-target genes, where PRMT5 methylates AR on arginine 761. This attenuates AR recruitment and transcription of genes expressed in differentiated prostate epithelium. The AR-inhibitory function of PRMT5 is restricted to TMPRSS2:ERG-positive prostate cancer cells. Mutation of this methylation site on AR results in a transcriptionally hyperactive AR, suggesting that the proliferative effects of ERG and PRMT5 are mediated through attenuating AR's ability to induce genes normally involved in lineage differentiation. This provides a rationale for targeting PRMT5 in TMPRSS2:ERG positive prostate cancers. Moreover, methylation of AR at arginine 761 highlights a mechanism for how the ERG oncogene may coax AR towards inducing proliferation versus differentiation.

Keywords: PRMT5; TMPRSS2:ERG; androgen receptor; cancer biology; cell biology; human; prostate cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Base Sequence
  • Cell Differentiation
  • Cell Line, Tumor
  • Cell Proliferation
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Male
  • Methylation
  • Models, Molecular
  • Mutation
  • Oncogene Proteins, Fusion / genetics*
  • Oncogene Proteins, Fusion / metabolism
  • Prostate / metabolism
  • Prostate / pathology
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Protein Multimerization
  • Protein Structure, Secondary
  • Protein-Arginine N-Methyltransferases / antagonists & inhibitors
  • Protein-Arginine N-Methyltransferases / genetics*
  • Protein-Arginine N-Methyltransferases / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Receptors, Androgen / chemistry
  • Receptors, Androgen / genetics*
  • Receptors, Androgen / metabolism
  • Serine Endopeptidases / genetics*
  • Serine Endopeptidases / metabolism
  • Signal Transduction
  • Transcriptional Regulator ERG / genetics
  • Transcriptional Regulator ERG / metabolism

Substances

  • AR protein, human
  • ERG protein, human
  • Oncogene Proteins, Fusion
  • RNA, Small Interfering
  • Receptors, Androgen
  • Transcriptional Regulator ERG
  • PRMT5 protein, human
  • Protein-Arginine N-Methyltransferases
  • Serine Endopeptidases
  • TMPRSS2 protein, human

Grants and funding

All authors except Thomas Westerling, Gilles Buchwalter, and Myles Brown received no external funding for this work.