JMJD6 Licenses ERα-Dependent Enhancer and Coding Gene Activation by Modulating the Recruitment of the CARM1/MED12 Co-activator Complex

Mol Cell. 2018 Apr 19;70(2):340-357.e8. doi: 10.1016/j.molcel.2018.03.006. Epub 2018 Apr 5.

Abstract

Whereas the actions of enhancers in gene transcriptional regulation are well established, roles of JmjC-domain-containing proteins in mediating enhancer activation remain poorly understood. Here, we report that recruitment of the JmjC-domain-containing protein 6 (JMJD6) to estrogen receptor alpha (ERα)-bound active enhancers is required for RNA polymerase II recruitment and enhancer RNA production on enhancers, resulting in transcriptional pause release of cognate estrogen target genes. JMJD6 is found to interact with MED12 in the mediator complex to regulate its recruitment. Unexpectedly, JMJD6 is necessary for MED12 to interact with CARM1, which methylates MED12 at multiple arginine sites and regulates its chromatin binding. Consistent with its role in transcriptional activation, JMJD6 is required for estrogen/ERα-induced breast cancer cell growth and tumorigenesis. Our data have uncovered a critical regulator of estrogen/ERα-induced enhancer coding gene activation and breast cancer cell potency, providing a potential therapeutic target of ER-positive breast cancers.

Keywords: JmjC domain-containing protein; breast cancer; enhancer; enhancer RNA; estrogen receptor; mediator; protein arginine methyltransferase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Binding Sites
  • Breast Neoplasms / enzymology*
  • Breast Neoplasms / genetics
  • Breast Neoplasms / pathology
  • Cell Proliferation* / drug effects
  • Estradiol / pharmacology
  • Estrogen Receptor alpha / agonists
  • Estrogen Receptor alpha / genetics
  • Estrogen Receptor alpha / metabolism*
  • Female
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • Humans
  • Jumonji Domain-Containing Histone Demethylases / genetics
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • MCF-7 Cells
  • Mediator Complex / genetics
  • Mediator Complex / metabolism*
  • Mice, Inbred BALB C
  • Mice, Nude
  • Protein Binding
  • Protein Transport
  • Protein-Arginine N-Methyltransferases / genetics
  • Protein-Arginine N-Methyltransferases / metabolism*
  • Signal Transduction
  • Transcriptional Activation* / drug effects

Substances

  • ESR1 protein, human
  • Estrogen Receptor alpha
  • MED12 protein, human
  • Mediator Complex
  • Estradiol
  • JMJD6 protein, human
  • Jumonji Domain-Containing Histone Demethylases
  • Protein-Arginine N-Methyltransferases
  • coactivator-associated arginine methyltransferase 1