Pluripotency transcription factor Oct4 mediates stepwise nucleosome demethylation and depletion

Mol Cell Biol. 2015 Mar;35(6):1014-25. doi: 10.1128/MCB.01105-14. Epub 2015 Jan 12.

Abstract

The mechanisms whereby the crucial pluripotency transcription factor Oct4 regulates target gene expression are incompletely understood. Using an assay system based on partially differentiated embryonic stem cells, we show that Oct4 opposes the accumulation of local H3K9me2 and subsequent Dnmt3a-mediated DNA methylation. Upon binding DNA, Oct4 recruits the histone lysine demethylase Jmjd1c. Chromatin immunoprecipitation (ChIP) time course experiments identify a stepwise Oct4 mechanism involving Jmjd1c recruitment and H3K9me2 demethylation, transient FACT (facilitates chromatin transactions) complex recruitment, and nucleosome depletion. Genome-wide and targeted ChIP confirms binding of newly synthesized Oct4, together with Jmjd1c and FACT, to the Pou5f1 enhancer and a small number of other Oct4 targets, including the Nanog promoter. Histone demethylation is required for both FACT recruitment and H3 depletion. Jmjd1c is required to induce endogenous Oct4 expression and fully reprogram fibroblasts to pluripotency, indicating that the assay system identifies functional Oct4 cofactors. These findings indicate that Oct4 sequentially recruits activities that catalyze histone demethylation and depletion.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation / genetics
  • Cells, Cultured
  • Chromatin Immunoprecipitation / methods
  • DNA (Cytosine-5-)-Methyltransferases / genetics
  • DNA Methylation / genetics*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Embryonic Stem Cells / metabolism
  • Fibroblasts / metabolism
  • Histones / genetics
  • Histones / metabolism
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Humans
  • Jumonji Domain-Containing Histone Demethylases / genetics
  • Jumonji Domain-Containing Histone Demethylases / metabolism
  • Mice
  • Nucleosomes / genetics
  • Nucleosomes / metabolism*
  • Octamer Transcription Factor-3 / genetics
  • Octamer Transcription Factor-3 / metabolism*
  • Pluripotent Stem Cells / metabolism*
  • Promoter Regions, Genetic / genetics
  • Regulatory Sequences, Nucleic Acid / genetics

Substances

  • DNA-Binding Proteins
  • Histones
  • Homeodomain Proteins
  • Nucleosomes
  • Octamer Transcription Factor-3
  • Jumonji Domain-Containing Histone Demethylases
  • DNA (Cytosine-5-)-Methyltransferases