Epigenetic repression of regulator of G-protein signaling 2 promotes androgen-independent prostate cancer cell growth

Int J Cancer. 2012 Apr 1;130(7):1521-31. doi: 10.1002/ijc.26138. Epub 2011 Jun 9.

Abstract

G-protein-coupled receptor (GPCR)-stimulated androgen-independent activation of androgen receptor (AR) contributes to acquisition of a hormone-refractory phenotype by prostate cancer. We previously reported that regulator of G-protein signaling (RGS) 2, an inhibitor of GPCRs, inhibits androgen-independent AR activation (Cao et al., Oncogene 2006;25:3719-34). Here, we show reduced RGS2 protein expression in human prostate cancer specimens compared to adjacent normal or hyperplastic tissue. Methylation-specific PCR analysis and bisulfite sequencing indicated that methylation of the CpG island in the RGS2 gene promoter correlated with RGS2 downregulation in prostate cancer. In vitro methylation of this promoter suppressed reporter gene expression in transient transfection studies, whereas reversal of this promoter methylation with 5-aza-2'-deoxycytidine (5-Aza-dC) induced RGS2 reexpression in androgen-independent prostate cancer cells and inhibited their growth under androgen-deficient conditions. Interestingly, the inhibitory effect of 5-Aza-dC was significantly reduced by an RGS2-targeted short hairpin RNA, indicating that reexpressed RGS2 contributed to this growth inhibition. Restoration of RGS2 levels by ectopic expression in androgen-independent prostate cancer cells suppressed growth of xenografts in castrated mice. Thus, RGS2 promoter hypermethylation represses its expression and unmasks a latent pathway for AR transactivation in prostate cancer cells. Targeting this reversible process may provide a new strategy for suppressing prostate cancer progression by reestablishing its androgen sensitivity.

Publication types

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

MeSH terms

  • Androgens / genetics
  • Androgens / metabolism*
  • Animals
  • Azacitidine / analogs & derivatives
  • Azacitidine / pharmacology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • CpG Islands / drug effects
  • CpG Islands / genetics
  • DNA Methylation / drug effects
  • DNA Methylation / genetics
  • Decitabine
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Epigenomics / methods
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • HEK293 Cells
  • Humans
  • Male
  • Mice
  • Mice, Nude
  • Promoter Regions, Genetic / drug effects
  • Prostate / drug effects
  • Prostate / metabolism
  • Prostatic Neoplasms / genetics*
  • Prostatic Neoplasms / metabolism*
  • Prostatic Neoplasms / pathology
  • RGS Proteins / antagonists & inhibitors
  • RGS Proteins / genetics*
  • RGS Proteins / metabolism
  • RNA, Small Interfering / genetics
  • Receptors, Androgen / genetics
  • Receptors, Androgen / metabolism
  • Receptors, G-Protein-Coupled

Substances

  • Androgens
  • RGS Proteins
  • RGS2 protein, human
  • RNA, Small Interfering
  • Receptors, Androgen
  • Receptors, G-Protein-Coupled
  • Decitabine
  • Azacitidine