CTCF confers local nucleosome resiliency after DNA replication and during mitosis

Autor: Nicola Festuccia, Alexandra Tachtsidi, Inma Gonzalez, Thaleia Papadopoulou, Agnès Dubois, Pablo Navarro, Elphège P. Nora, Michel Cohen-Tannoudji, Sandrine Vandormael-Pournin, Benoit G. Bruneau, Nick D.L. Owens
Přispěvatelé: Epigénomique, Prolifération et Identité Cellulaire - Epigenomics, Proliferation and the Identity of Cells (EPIC), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Collège Doctoral, Sorbonne Université (SU), Embryon précoce de mammifères et cellules souches, Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), University of California [San Francisco] (UC San Francisco), University of California (UC), This work was supported by recurrent funding from the Institut Pasteur, the CNRS, and Revive (Investissement d’Avenir, ANR-10-LABX-73). E.P.N. was supported by EMBO (ALTF523-2013), HSFP, and the Roddenberry Stem Cell Center at Gladstone. N.O. is supported by Revive. P.N. acknowledges financial support from the Fondation Schlumberger (FRM FSER 2017), the Agence Nationale de la Recherche (ANR 16 CE120004 01 MITMAT), the Ligue contre le Cancer (LNCC EL2018 NAVARRO) and the European Research Council (ERC-CoG-2017 BIND)., ANR-10-LABX-0073,REVIVE,Stem Cells in Regenerative Biology and Medicine(2010), ANR-16-CE12-0004,MitMAT,Mémoire mitotique de l'activité transcriptionnelle dans les cellules ES(2016), European Project: 773083,ERC-CoG-2017,BIND(2018), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Collège doctoral [Sorbonne universités], Embryon précoce de mammifères et cellules souches - Early Mammalian Development & Stem Cell Biology, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), University of California [San Francisco] (UCSF), University of California, Epigénétique des Cellules Souches - Epigenetics of Stem Cells, Génétique fonctionnelle de la Souris, Génétique Fonctionnelle de la Souris, ANR-10-LABX-0073/10-LABX-0073,REVIVE,Stem Cells in Regenerative Biology and Medicine(2010), European Project
Jazyk: angličtina
Rok vydání: 2019
Předmět:
0301 basic medicine
Nucleosome organization
CCCTC-Binding Factor
Cell division
Mouse
MESH: DNA Replication
[SDV.BC.BC]Life Sciences [q-bio]/Cellular Biology/Subcellular Processes [q-bio.SC]
chemistry.chemical_compound
Mice
0302 clinical medicine
MESH: Animals
MESH: CCCTC-Binding Factor
Biology (General)
MESH: Embryonic Stem Cells
Cells
Cultured
0303 health sciences
Cultured
General Neuroscience
General Medicine
Chromosomes and Gene Expression
MESH: Gene Expression Regulation
3. Good health
Cell biology
Nucleosomes
Medicine
nucleosome positioning
MESH: Cells
Cultured
Research Article
DNA Replication
Transcriptional Activation
chromosomes
replication
QH301-705.5
Science
Cells
Biology
General Biochemistry
Genetics and Molecular Biology
03 medical and health sciences
MESH: Nucleosomes
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]
transcription factors
Genetics
Nucleosome
Animals
Mitosis
Transcription factor
Gene
MESH: Mice
mouse
Embryonic Stem Cells
030304 developmental biology
mitosis
General Immunology and Microbiology
fungi
DNA replication
MESH: Mitosis
Stem Cell Research
CTCF
pluripotency
030104 developmental biology
[SDV.BDD.EO]Life Sciences [q-bio]/Development Biology/Embryology and Organogenesis
chemistry
Gene Expression Regulation
gene expression
MESH: Transcriptional Activation
Generic health relevance
Biochemistry and Cell Biology
030217 neurology & neurosurgery
DNA
Zdroj: eLife
eLife, 2019, 8, ⟨10.1101/563619⟩
eLife, eLife Sciences Publication, 2019, 8, ⟨10.1101/563619⟩
eLife, Vol 8 (2019)
ISSN: 2050-084X
DOI: 10.1101/563619
Popis: 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.
eLife digest A single cell contains several meters of DNA which must be tightly packaged to fit inside. Typically, the DNA is wound around proteins, like a thread around many spools, to form more compact structures called nucleosomes. Before a cell divides in two, however, it needs first to access and replicate its DNA so that each new cell can get a copy of the genetic material. The cell then needs to condense the DNA again so that the two copies can be easily separated via a process called mitosis. These two processes – DNA replication and mitosis – entail major rearrangements of the nucleosomes, which then need to be returned to their original positions. Nucleosomes are also repositioned when cells need to access the coded instructions written in genes. Molecules called transcription factors bind to targets within the DNA to make sure genes are active or inactive at the right times of a cell’s life, but many are evicted from the DNA during its replication and during cell division. Most transcription factors also require nucleosomes to be specifically organized to bind to the DNA, and it remains unclear how the factors re-engage with the DNA and how nucleosomes are managed during and after DNA replication and mitosis. Owens, Papadopoulou et al. set out to understand how nucleosomes are organized immediately after DNA is replicated and while cells divide. Experiments with mouse cells grown in the laboratory showed that certain transcription factors can rebind to their targets within minutes of replication finishing, remain bound to the DNA during cell division, and displace nucleosomes from their binding sites. Owens, Papadopoulou et al. refer to these factors as “resilient transcription factors” and identified two examples, named CTCF and Esrrb. Further experiments showed that, by maintaining the structure of nearby nucleosomes while a cell divides, these resilient transcription factors could quickly reactivate genes immediately after DNA replication and mitosis are complete. These findings show that transcription factors play a fundamental role in maintaining gene regulation from one generation of cells to the next. Further studies on this topic may eventually foster progress in research areas where cell division is paramount, such as regenerative medicine and cancer biology.
Databáze: OpenAIRE
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