Genome-Scale Oscillations in DNA Methylation during Exit from Pluripotency

Cell Syst. 2018 Jul 25;7(1):63-76.e12. doi: 10.1016/j.cels.2018.06.012.

Abstract

Pluripotency is accompanied by the erasure of parental epigenetic memory, with naïve pluripotent cells exhibiting global DNA hypomethylation both in vitro and in vivo. Exit from pluripotency and priming for differentiation into somatic lineages is associated with genome-wide de novo DNA methylation. We show that during this phase, co-expression of enzymes required for DNA methylation turnover, DNMT3s and TETs, promotes cell-to-cell variability in this epigenetic mark. Using a combination of single-cell sequencing and quantitative biophysical modeling, we show that this variability is associated with coherent, genome-scale oscillations in DNA methylation with an amplitude dependent on CpG density. Analysis of parallel single-cell transcriptional and epigenetic profiling provides evidence for oscillatory dynamics both in vitro and in vivo. These observations provide insights into the emergence of epigenetic heterogeneity during early embryo development, indicating that dynamic changes in DNA methylation might influence early cell fate decisions.

Keywords: DNA methylation; biophysical modeling; dynamics; embryo; epigenetic; pluripotency; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation
  • Cellular Reprogramming
  • CpG Islands / genetics
  • DNA (Cytosine-5-)-Methyltransferases / metabolism
  • DNA Methylation / genetics
  • DNA Methylation / physiology*
  • Embryo, Mammalian / cytology
  • Epigenesis, Genetic / genetics
  • Epigenomics
  • Gene Expression Regulation, Developmental / genetics*
  • Genome
  • Genomic Imprinting
  • Germ Cells / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mouse Embryonic Stem Cells / physiology
  • Pluripotent Stem Cells / cytology
  • Pluripotent Stem Cells / metabolism*
  • Pluripotent Stem Cells / physiology

Substances

  • DNA (Cytosine-5-)-Methyltransferases