Interaction of glucocorticoid receptor (GR) with estrogen receptor (ER) α and activator protein 1 (AP1) in dexamethasone-mediated interference of ERα activity

J Biol Chem. 2013 Aug 16;288(33):24020-34. doi: 10.1074/jbc.M113.473819. Epub 2013 Jun 28.

Abstract

The role of glucocorticoids in the inhibition of estrogen (17-β-estradiol (E2))-regulated estrogen receptor (ER)-positive breast cancer cell proliferation is well established. We and others have seen that synthetic glucocorticoid dexamethasone (Dex) antagonizes E2-stimulated endogenous ERα target gene expression. However, how glucocorticoids negatively regulate the ERα signaling pathway is still poorly understood. ChIP studies using ERα- and glucocorticoid receptor (GR)-positive MCF-7 cells revealed that GR occupies several ERα-binding regions (EBRs) in cells treated with E2 and Dex simultaneously. Interestingly, there was little or no GR loading to these regions when cells were treated with E2 or Dex alone. The E2+Dex-dependent GR recruitment is associated with the displacement of ERα and steroid receptor coactivator-3 from the target EBRs leading to the repression of ERα-mediated transcriptional activation. The recruitment of GR to EBRs requires assistance from ERα and FOXA1 and is facilitated by AP1 binding within the EBRs. The GR binding to EBRs is mediated via direct protein-protein interaction between the GR DNA-binding domain and ERα. Limited mutational analyses indicate that arginine 488 located within the C-terminal zinc finger domain of the GR DNA-binding domain plays a critical role in stabilizing this interaction. Together, the results of this study unravel a novel mechanism involved in glucocorticoid inhibition of ERα transcriptional activity and E2-mediated cell proliferation and thus establish a foundation for future exploitation of the GR signaling pathway in the treatment of ER-positive breast cancer.

Keywords: AP1 Transcription Factor; Breast Cancer; Estrogen; Estrogen Receptor; Glucocorticoid Receptor; Glucocorticoids.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Arginine / metabolism
  • Binding Sites / genetics
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Chromosomes, Human / genetics
  • Dexamethasone / pharmacology*
  • Enhancer Elements, Genetic / genetics
  • Estradiol / pharmacology
  • Estrogen Receptor alpha / genetics
  • Estrogen Receptor alpha / metabolism*
  • Gene Expression Regulation, Neoplastic / drug effects
  • Hepatocyte Nuclear Factor 3-alpha / metabolism
  • Humans
  • Ligands
  • Models, Biological
  • Molecular Sequence Data
  • Nuclear Receptor Coactivator 3 / metabolism
  • Promoter Regions, Genetic / genetics
  • Protein Binding / drug effects
  • Protein Stability / drug effects
  • RNA, Small Interfering / metabolism
  • Rats
  • Receptors, Glucocorticoid / chemistry
  • Receptors, Glucocorticoid / metabolism*
  • Transcription Factor AP-1 / metabolism*
  • Transcription, Genetic / drug effects

Substances

  • ESR1 protein, human
  • Estrogen Receptor alpha
  • FOXA1 protein, human
  • Hepatocyte Nuclear Factor 3-alpha
  • Ligands
  • RNA, Small Interfering
  • Receptors, Glucocorticoid
  • Transcription Factor AP-1
  • Estradiol
  • Dexamethasone
  • Arginine
  • NCOA3 protein, human
  • Nuclear Receptor Coactivator 3