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Cited by 3Genomics and Chromatin DynamicsProtein Structure and DynamicsNuclear Structure and Function

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Disordered regions and folded modules in CAF-1 promote histone deposition in Schizosaccharomyces pombe

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Ouasti, Fouad, Audin, Maxime, Fréon, Karine, Quivy, Jean-Pierre, Tachekort, Mehdi, Cesard, Elizabeth, Thureau, Aurélien, Ropars, Virginie, Fernández Varela, Paloma, Moal, Gwenaelle, Soumana Adamou, Ibrahim, Uryga, Aleksandra, Legrand, Pierre, Andreani, Jessica, Guerois, Raphaël, Almouzni, Geneviève, Lambert, Sarah, Ochsenbein, Francoise·2024·eLife
DOI 10.7554/elife.91461.3

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Abstract

Genome and epigenome integrity in eukaryotes depends on the proper coupling of histone deposition with DNA synthesis. This process relies on the evolutionary conserved histone chaperone CAF-1 for which the links between structure and functions are still a puzzle. While studies of the Saccharomyces cerevisiae CAF-1 complex enabled to propose a model for the histone deposition mechanism, we still lack a framework to demonstrate its generality and in particular, how its interaction with the polymerase accessory factor PCNA is operating. Here, we reconstituted a complete Sp CAF-1 from fission yeast. We characterized its dynamic structure using NMR, SAXS and molecular modeling together with in vitro and in vivo functional studies on rationally designed interaction mutants. Importantly, we identify the unfolded nature of the acidic domain which folds up when binding to histones. We also show how the long KER helix mediates DNA binding and stimulates Sp CAF-1 association with PCNA. Our study highlights how the organization of CAF-1 comprising both disordered regions and folded modules enables the dynamics of multiple interactions to promote synthesis-coupled histone deposition essential for its DNA replication, heterochromatin maintenance, and genome stability functions.

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Metadata

Authors
Ouasti, F., Audin, M., Fréon, K., Quivy, J.-P., Tachekort, M., Cesard, E., Thureau, A., Ropars, V., Fernández Varela, P., Moal, G., Soumana Adamou, I., Uryga, A., Legrand, P., Andreani, J., Guerois, R., Almouzni, G., Lambert, S., & Ochsenbein, F.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Synchrotron SOLEIL (FR)
  • Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Institute Joliot
  • Institut Curie, PSL Research University, CNRS UMR 3348, INSERM U1278, Université Paris-Saclay, Equipe labellisée Ligue contre le Cancer
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2024-02-20
Volume
12
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.91461.3
OpenAlex
W4391981040
Cited by
3
References
1
Citations by year
2025: 2 · 2024: 1
FWCI
0.41
Type
journal article
Language
en
Open access
Licence
Locations
eLife (publishedVersion, cc-by)
Funders
  • Institut National Du Cancer (2016-1-PL BIO-03-CEA1, 2016-1-PLBIO-03-ICR-1)
  • Agence Nationale de la Recherche (ANR-16-CE11-0028, ANR-20-CE18-0038)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
Keywords
histone deposition, Schizosaccharomyces pombe, intrinsically disordered regions, protein structure-function relationship, PCNA, DNA replication, heterochromatin maintenance, genome stability, protein complex reconstitution

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