1. Chromosomes and Gene Expression
Download icon

CTCF confers local nucleosome resiliency after DNA replication and during mitosis

Research Article
  • Cited 0
  • Views 878
  • Annotations
Cite this article as: eLife 2019;8:e47898 doi: 10.7554/eLife.47898

Abstract

The access of Transcription Factors (TFs) to their cognate DNA binding motifs requires a precise control over nucleosome positioning. This is especially important following DNA replication and during mitosis, both resulting in profound changes in nucleosome organization over TF binding regions. Using mouse Embryonic Stem (ES) cells, we show that the TF CTCF displaces nucleosomes from its binding site and locally organizes large and phased nucleosomal arrays, not only in interphase steady-state but also immediately after replication and during mitosis. Correlative analyses suggest this is associated with fast gene reactivation following replication and mitosis. While regions bound by other TFs (Oct4/Sox2), display major rearrangement, the post-replication and mitotic nucleosome positioning activity of CTCF is not unique: Esrrb binding regions are also characterized by persistent nucleosome positioning. Therefore, selected TFs such as CTCF and Esrrb act as resilient TFs governing the inheritance of nucleosome positioning at regulatory regions throughout the cell-cycle.

Article and author information

Author details

  1. Nick Owens

    Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2151-9923
  2. Thaleia Papadopoulou

    Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Nicola Festuccia

    Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexandra Tachtsidi

    Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Inma Gonzalez

    Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Agnes Dubois

    Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Sandrine Vandormael-Pournin

    Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Elphège P Nora

    Gladstone Institutes, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Benoit Bruneau

    Gladstone Institutes, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0804-7597
  10. Michel Cohen-Tannoudji

    Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6405-2657
  11. Pablo Navarro

    Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    For correspondence
    pablo.navarro-gil@pasteur.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2700-6598

Funding

Institut Pasteur

  • Michel Cohen-Tannoudji
  • Pablo Navarro

Centre National de la Recherche Scientifique

  • Michel Cohen-Tannoudji
  • Pablo Navarro

Agence Nationale de la Recherche (Investissement d'Avenir; Revive Labex; ANR-10-LABX-73)

  • Pablo Navarro

Agence Nationale de la Recherche (ANR 16 CE12 0004 01 MITMAT)

  • Pablo Navarro

Ligue Contre le Cancer (LNCC EL2018 NAVARRO)

  • Pablo Navarro

European Research Council (ERC-CoG-2017 BIND)

  • Pablo Navarro

European Molecular Biology Organization (ALTF523-2013)

  • Elphège P Nora

Human Frontier Science Program

  • Elphège P Nora

Fondation Schlumberger (FRM FSER 2017)

  • Pablo Navarro

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments were conducted according to the French and European regulations on care and protection of laboratory animals (EC Directive 86/609, French Law 2001-486 issued on June 6, 2001) and were approved by the Institut Pasteur ethics committee (n{degree sign} dha180008).

Reviewing Editor

  1. Deborah Bourc'his, Institut Curie, France

Publication history

  1. Received: April 23, 2019
  2. Accepted: October 9, 2019
  3. Accepted Manuscript published: October 10, 2019 (version 1)

Copyright

© 2019, Owens 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.

Metrics

  • 878
    Page views
  • 192
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Cell Biology
    2. Chromosomes and Gene Expression
    Andrey Poleshko et al.
    Research Article Updated
    1. Chromosomes and Gene Expression
    Daniel S Saxton, Jasper Rine
    Research Article