CTCF confers local nucleosome resiliency after DNA replication and during mitosis
- Institut Pasteur, France
- University of California, San Francisco, United States
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.
Data availability
Sequencing data generated for this study have been deposited in GEO with accession GSE131356.Publicly available datasets used here: Festuccia et al. 2019; GEO accession: GSE122589; Teves et al. 2018; GEO accession: GSE109963; Stewart-Morgan et al. 2019; GEO accession: GSE128643
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CTCF confers local nucleosome resiliency after DNA replication and during mitosisNCBI Gene Expression Omnibus, GSE131356.
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Role of TBP in reactivation of transcription following mitosis [RNA-Seq]NCBI Gene Expression Omnibus, GSE109963.
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Transcription factor activity and nucleosome organisation in mitosisNCBI Gene Expression Omnibus, GSE122589.
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Transcription Restart Establishes Chromatin Accessibility after DNA ReplicationNCBI Gene Expression Omnibus, GSE128643.
Article and author information
Author details
Michel Cohen-Tannoudji
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.
Reviewing Editor
- Deborah Bourc'his, Institut Curie, France
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).
Version history
- Received: April 23, 2019
- Accepted: October 9, 2019
- Accepted Manuscript published: October 10, 2019 (version 1)
- Version of Record published: November 11, 2019 (version 2)
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.
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CTCF confers local nucleosome resiliency after DNA replication and during mitosis
eLife 8:e47898.
https://doi.org/10.7554/eLife.47898
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