Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor alpha in breast cancer cells

Cancer Res. 2010 Nov 15;70(22):9175-84. doi: 10.1158/0008-5472.CAN-10-1318. Epub 2010 Oct 26.

Abstract

Estrogen receptor α (ERα) upregulation causes abnormal cell proliferation in about two thirds of breast cancers, yet understanding of the underlying mechanisms remains incomplete. Here, we show that high expression of the microRNA miR-375 in ERα-positive breast cell lines is a key driver of their proliferation. miR-375 overexpression was caused by loss of epigenetic marks including H3K9me2 and local DNA hypomethylation, dissociation of the transcriptional repressor CTCF from the miR-375 promoter, and interactions of ERα with regulatory regions of miR-375. Inhibiting miR-375 in ERα-positive MCF-7 cells resulted in reduced ERα activation and cell proliferation. A combination of expression profiling from tumor samples and miRNA target prediction identified RASD1 as a potential miR-375 target. Mechanistic investigations revealed that miR-375 regulates RASD1 by targeting the 3' untranslated region in RASD1 mRNA. Additionally, we found that RASD1 negatively regulates ERα expression. Our findings define a forward feedback pathway in control of ERα expression, highlighting new strategies to treat ERα-positive invasive breast tumors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Base Sequence
  • Binding Sites / genetics
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • CCCTC-Binding Factor
  • Cell Line
  • Cell Line, Tumor
  • Cell Proliferation
  • CpG Islands / genetics
  • DNA Methylation
  • Epigenesis, Genetic*
  • Estrogen Receptor alpha / genetics*
  • Estrogen Receptor alpha / metabolism
  • Feedback, Physiological
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic*
  • HEK293 Cells
  • Histones / metabolism
  • Humans
  • Immunoblotting
  • Lysine / metabolism
  • Methylation
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Molecular Sequence Data
  • Oligonucleotide Array Sequence Analysis
  • RNA Interference
  • Repressor Proteins / metabolism
  • ras Proteins / genetics
  • ras Proteins / metabolism

Substances

  • CCCTC-Binding Factor
  • CTCF protein, human
  • ESR1 protein, human
  • Estrogen Receptor alpha
  • Histones
  • MIRN375 microRNA, human
  • MicroRNAs
  • RASD1 protein, human
  • Repressor Proteins
  • ras Proteins
  • Lysine