Epigenetic regulation of miR-302 by JMJD1C inhibits neural differentiation of human embryonic stem cells

J Biol Chem. 2014 Jan 24;289(4):2384-95. doi: 10.1074/jbc.M113.535799. Epub 2013 Dec 6.

Abstract

It has been recently reported that the regulatory circuitry formed by OCT4, miR-302, and NR2F2 controls both pluripotency and neural differentiation of human embryonic stem cells (hESCs). We show here that JMJD1C, a histone 3 lysine 9 (H3K9) demethylase expressed in hESCs, directly interacts with this circuitry. hESCs with stable knockdown of JMJD1C remain pluripotent while having reduced miR-302 expression, decreased BMP signaling, and enhanced TGFβ signaling. JMJD1C binds to the miR-302 promoter and reduces H3K9 methylation. Withdrawal of basic fibroblast growth factor (bFGF) from the culture induces neural differentiation of the knockdown, but not the control, cells within 3 days, accompanied by elevated NR2F2 expression. This can be attenuated with miR-302 mimics or an H3K9 methytransferase inhibitor. Together, our findings suggest that JMJD1C represses neural differentiation of hESCs at least partially by epigenetically sustaining miR-302 expression and that JMJD1C knockdown is sufficient to trigger neural differentiation upon withdrawal of exogenous bFGF.

Keywords: Embryonic Stem Cell; Epigenetics; Histone Methylation; MicroRNA; Neurodifferentiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bone Morphogenetic Proteins / genetics
  • Bone Morphogenetic Proteins / metabolism
  • COUP Transcription Factor I / genetics
  • COUP Transcription Factor I / metabolism
  • Cell Differentiation / physiology*
  • Cell Line
  • Embryonic Stem Cells / cytology
  • Embryonic Stem Cells / metabolism*
  • Epigenesis, Genetic / physiology*
  • Fibroblast Growth Factor 2 / genetics
  • Fibroblast Growth Factor 2 / metabolism
  • Humans
  • Jumonji Domain-Containing Histone Demethylases / genetics
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • MicroRNAs / biosynthesis*
  • MicroRNAs / genetics
  • Neurons / cytology
  • Neurons / metabolism
  • Oxidoreductases, N-Demethylating / genetics
  • Oxidoreductases, N-Demethylating / metabolism*
  • Promoter Regions, Genetic / physiology
  • Signal Transduction / physiology*
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism

Substances

  • Bone Morphogenetic Proteins
  • COUP Transcription Factor I
  • MIRN302A microRNA, human
  • MicroRNAs
  • NR2F1 protein, human
  • Transforming Growth Factor beta
  • Fibroblast Growth Factor 2
  • JMJD1C protein, human
  • Jumonji Domain-Containing Histone Demethylases
  • Oxidoreductases, N-Demethylating

Associated data

  • GEO/GSE46485