An epigenetic switch ensures transposon repression upon dynamic loss of DNA methylation in embryonic stem cells

  1. Marius Walter
  2. Aurélie Teissandier
  3. Raquel Pérez-Palacios
  4. Déborah Bourc'his  Is a corresponding author
  1. Institut Curie, France
  2. Isntitut Curie, France

Abstract

DNA methylation is extensively remodeled during mammalian gametogenesis and embryogenesis. Most transposons become hypomethylated, raising the question of their regulation in the absence of DNA methylation. To reproduce a rapid and extensive demethylation, we subjected mouse ES cells to chemically defined hypomethylating culture conditions. Surprisingly, we observed two phases of transposon regulation. After an initial burst of de-repression, various transposon families were efficiently re-silenced. This was accompanied by a reconfiguration of the repressive chromatin landscape: while H3K9me3 was stable, H3K9me2 globally disappeared and H3K27me3 accumulated at transposons. Interestingly, we observed that H3K9me3 and H3K27me3 occupy different transposon families or different territories within the same family, defining three functional categories of adaptive chromatin responses to DNA methylation loss. Our work highlights that H3K9me3 and, most importantly, polycomb-mediated H3K27me3 chromatin pathways can secure the control of a large spectrum of transposons in periods of intense DNA methylation change, ensuring longstanding genome stability.

Article and author information

Author details

  1. Marius Walter

    Department of Genetics and Developmental Biology, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Aurélie Teissandier

    Department of Genetics and Developmental Biology, Isntitut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Raquel Pérez-Palacios

    Department of Genetics and Developmental Biology, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Déborah Bourc'his

    Department of Genetics and Developmental Biology, Institut Curie, Paris, France
    For correspondence
    deborah.bourchis@curie.fr
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Anne C Ferguson-Smith, University of Cambridge, United Kingdom

Version history

  1. Received: September 7, 2015
  2. Accepted: January 27, 2016
  3. Accepted Manuscript published: January 27, 2016 (version 1)
  4. Version of Record published: February 16, 2016 (version 2)

Copyright

© 2016, Walter et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Marius Walter
  2. Aurélie Teissandier
  3. Raquel Pérez-Palacios
  4. Déborah Bourc'his
(2016)
An epigenetic switch ensures transposon repression upon dynamic loss of DNA methylation in embryonic stem cells
eLife 5:e11418.
https://doi.org/10.7554/eLife.11418

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https://doi.org/10.7554/eLife.11418

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