The orphan nuclear receptor LRH-1 and ERα activate GREB1 expression to induce breast cancer cell proliferation

PLoS One. 2012;7(2):e31593. doi: 10.1371/journal.pone.0031593. Epub 2012 Feb 16.

Abstract

Background: Liver Receptor Homolog 1 (LRH-1, NR5A2) is an orphan nuclear receptor that is over-expressed in cancers in tissues such as the breast, colon and pancreas. LRH-1 plays important roles in embryonic development, steroidogenesis and cholesterol homeostasis. In tumor cells, LRH-1 induces proliferation and cell cycle progression. High LRH-1 expression is demonstrated in breast cancers, positively correlating with ERα status and aromatase activity. LRH-1 dependent cellular mechanisms in breast cancer epithelial cells are poorly defined. Hence in the present study we investigated the actions of LRH-1 in estrogen receptor α (ERα) positive breast cancer cells.

Results: The study aimed to investigate LRH-1 dependent mechanisms that promote breast cancer proliferation. We identified that LRH-1 regulated the expression of Growth Regulation by Estrogen in Breast Cancer 1 (GREB1) in MCF-7 and MDA-MB-231 cells. Over-expression of LRH-1 increased GREB1 mRNA levels while knockdown of LRH-1 reduced its expression. GREB1 is a well characterised ERα target gene, with three estrogen response elements (ERE) located on its promoter. Chromatin immunoprecipitation studies provided evidence of the co-localisation of LRH-1 and ERα at all three EREs. With electrophoretic mobility shift assays, we demonstrated direct binding of LRH-1 to EREs located on GREB1 and Trefoil Factor 1 (TFF1, pS2) promoters. LRH-1 and ERα co-operatively activated transcription of ERE luciferase reporter constructs suggesting an overlap in regulation of target genes in breast cancer cells. Over-expression of LRH-1 resulted in an increase in cell proliferation. This effect was more pronounced with estradiol treatment. In the presence of ICI 182,780, an ERα antagonist, LRH-1 still induced proliferation.

Conclusions: We conclude that in ER-positive breast cancer cells, LRH-1 promotes cell proliferation by enhancing ERα mediated transcription of target genes such as GREB-1. Collectively these findings indicate the importance of LRH-1 in the progression of hormone-dependent breast cancer and implicate LRH-1 as a potential avenue for drug development.

Publication types

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

MeSH terms

  • Breast Neoplasms / pathology*
  • Cell Line, Tumor
  • Cell Proliferation*
  • Estrogen Receptor alpha / physiology*
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Neoplasm Proteins / genetics*
  • Orphan Nuclear Receptors / physiology*
  • Promoter Regions, Genetic
  • Receptors, Cytoplasmic and Nuclear / physiology*
  • Response Elements
  • Transcription, Genetic

Substances

  • Estrogen Receptor alpha
  • GREB1 protein, human
  • NR5A2 protein, human
  • Neoplasm Proteins
  • Orphan Nuclear Receptors
  • Receptors, Cytoplasmic and Nuclear