Coactivation of liver receptor homologue-1 by peroxisome proliferator-activated receptor gamma coactivator-1alpha on aromatase promoter II and its inhibition by activated retinoid X receptor suggest a novel target for breast-specific antiestrogen therapy

Cancer Res. 2005 Dec 15;65(24):11762-70. doi: 10.1158/0008-5472.CAN-05-2792.

Abstract

Aromatase inhibitors target the production of estrogen in breast adipose tissue, but in doing so, also decrease estrogen formation in bone and other sites, giving rise to deleterious side effects, such as bone loss and arthralgia. Thus, it would be clinically useful to selectively inhibit aromatase production in breast. In this regard, we have determined that the orphan nuclear receptor liver receptor homologue-1 (LRH-1) is a specific transcriptional activator of aromatase gene expression in human breast preadipocytes but not in other tissues of postmenopausal women. In this study, we show that the coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha (PGC-1alpha) is a physiologically relevant modulator of LRH-1, and that its transcriptional activity can be inhibited effectively using receptor-interacting peptide antagonists that prevent PGC-1alpha recruitment. Interestingly, we note that all of these peptides also interact in an agonist-dependent manner with retinoid X receptor alpha (RXRalpha), suggesting that these two receptors may compete for limiting cofactors within target cells. In support of this hypothesis, we show that 9-cis-retinoic acid, acting through RXR, inhibits both the basal and PGC-1alpha-induced transcriptional activity of LRH-1. The importance of this finding was confirmed by showing that LRH-1-dependent, PGC-1alpha-stimulated regulation of aromatase gene expression in primary human breast preadipocytes was effectively suppressed by RXR agonists. We infer from these data that LRH-1 is a bona fide target whose inhibition would selectively block aromatase expression in breast, while sparing other sites of expression.

Publication types

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

MeSH terms

  • Adipocytes / cytology
  • Adipocytes / drug effects
  • Adipocytes / metabolism
  • Alitretinoin
  • Animals
  • Antineoplastic Agents / pharmacology
  • Aromatase / chemistry*
  • Aromatase / genetics*
  • Aromatase / metabolism
  • Breast / cytology
  • Breast / drug effects
  • Breast / metabolism*
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Estrogens / metabolism
  • HeLa Cells
  • Heat-Shock Proteins / pharmacology*
  • Humans
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Liver Neoplasms / therapy
  • Mice
  • Peptide Fragments / pharmacology
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Promoter Regions, Genetic / physiology*
  • Receptors, Cytoplasmic and Nuclear / genetics*
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Retinoid X Receptor alpha / metabolism*
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Transcription Factors / pharmacology*
  • Transcription, Genetic
  • Tretinoin / pharmacology

Substances

  • Antineoplastic Agents
  • DNA-Binding Proteins
  • Estrogens
  • Heat-Shock Proteins
  • NR5A2 protein, human
  • Nr5a2 protein, mouse
  • PPARGC1A protein, human
  • Peptide Fragments
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Receptors, Cytoplasmic and Nuclear
  • Retinoid X Receptor alpha
  • Transcription Factors
  • Alitretinoin
  • Tretinoin
  • Aromatase