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Cited by 89Epigenetics and DNA MethylationGenomics and Chromatin DynamicsChromatin Remodeling and Cancer

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Chromatin remodeling of histone H3 variants by DDM1 underlies epigenetic inheritance of DNA methylation

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Lee, Seung Cho, Adams, Dexter W., Ipsaro, Jonathan J., Cahn, Jonathan, Lynn, Jason, Kim, Hyun-Soo, Berube, Benjamin, Major, Viktoria, Calarco, Joseph P., LeBlanc, Chantal, Bhattacharjee, Sonali, Ramu, Umamaheswari, Grimanelli, Daniel, Jacob, Yannick, Voigt, Philipp, Joshua-Tor, Leemor, Martienssen, Robert A.·2023·Cell
DOI 10.1016/j.cell.2023.08.001PMC PMC10529913

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Abstract

Summary Epigenetic inheritance refers to the faithful replication of DNA methylation and histone modification independent of DNA sequence. Nucleosomes block access to DNA methyltransferases, unless they are remodeled by DECREASE IN DNA METHYLATION1 (DDM1 Lsh/HELLS ), a Snf2-like master regulator of epigenetic inheritance. We show that DDM1 activity results in replacement of the transcriptional histone variant H3.3 for the replicative variant H3.1 during the cell cycle. In ddm1 mutants, DNA methylation can be restored by loss of the H3.3 chaperone HIRA, while the H3.1 chaperone CAF-1 becomes essential. The single-particle cryo-EM structure at 3.2 Å of DDM1 with a variant nucleosome reveals direct engagement at SHL2 with histone H3.3 at or near variant residues required for assembly, as well as with the deacetylated H4 tail. An N-terminal autoinhibitory domain binds H2A variants to allow remodeling, while a disulfide bond in the helicase domain is essential for activity in vivo and in vitro . We show that differential remodeling of H3 and H2A variants in vitro reflects preferential deposition in vivo . DDM1 co-localizes with H3.1 and H3.3 during the cell cycle, and with the DNA methyltransferase MET1 Dnmt1 . DDM1 localization to the chromosome is blocked by H4K16 acetylation, which accumulates at DDM1 targets in ddm1 mutants, as does the sperm cell specific H3.3 variant MGH3 in pollen, which acts as a placeholder nucleosome in the germline and contributes to epigenetic inheritance.

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Metadata

Authors
Lee, S. C., Adams, D. W., Ipsaro, J. J., Cahn, J., Lynn, J., Kim, H.-S., Berube, B., Major, V., Calarco, J. P., LeBlanc, C., Bhattacharjee, S., Ramu, U., Grimanelli, D., Jacob, Y., Voigt, P., Joshua-Tor, L., & Martienssen, R. A.
Affiliations
  • Howard Hughes Medical Institute (US)
  • Wellcome Centre for Cell Biology (GB)
  • Institut de Recherche pour le Développement (FR)
Corresponding author
Martienssen, Robert A.
ORCID
Venue
Cell
Publisher
Elsevier BV
Published
2023-09
Volume
186
Issue
19
Pages
4100-4116.e15
ISSN
0092-8674 (ISSN-L)
DOI
10.1016/j.cell.2023.08.001
PMC
PMC10529913
OpenAlex
W4386226589
Cited by
89
References
1
Citations by year
2026: 22 · 2025: 40 · 2024: 21 · 2023: 5
FWCI
7.84
Type
journal article
Language
en
Open access
Licence
Locations
  • Cell (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed (publishedVersion)
  • Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (acceptedVersion, cc-by)
  • PubMed Central (submittedVersion, cc-by)
  • HAL (submittedVersion)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
Funders
  • NIGMS (R01 GM067014)
  • Biotechnology and Biological Sciences Research Council (BBS/E/B/000C0421)
  • Cold Spring Harbor Laboratory (35GM128661)
  • National Institutes of Health
  • Horizon 2020 Framework Programme
  • European Research Council
  • National Science Foundation
  • École Normale Supérieure
  • NCI
  • ERC (639253)
  • Horizon 2020
  • Howard Hughes Medical Institute
  • Wellcome Trust (101527/Z/13/Z, 203149, 104175/Z/14/Z)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords
chromatin remodeling, histone H3 variant, DDM1, histone H3.3, H4K16 acetylation, DNA methylation, epigenetic inheritance, male germline, spermatozoa

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