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Cited by 240Epigenetics and DNA MethylationGenomics and Chromatin DynamicsGenetic Syndromes and Imprinting

Redistribution of H3K27me3 upon DNA hypomethylation results in de-repression of Polycomb target genes

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Reddington, James P, Perricone, Sara M, Nestor, Colm E, Reichmann, Judith, Youngson, Neil A, Suzuki, Masako, Reinhardt, Diana, Dunican, Donncha S +8 more·2013·Genome Biology
DOI 10.1186/gb-2013-14-3-r25PMC PMC4053768
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Abstract

Background: DNA methylation and the Polycomb repression system are epigenetic mechanisms that play important roles in maintaining transcriptional repression. Recent evidence suggests that DNA methylation can attenuate the binding of Polycomb protein components to chromatin and thus plays a role in determining their genomic targeting. However, whether this role of DNA methylation is important in the context of transcriptional regulation is unclear. Results: By genome-wide mapping of the Polycomb Repressive Complex 2-signature histone mark, H3K27me3, in severely DNA hypomethylated mouse somatic cells, we show that hypomethylation leads to widespread H3K27me3 redistribution, in a manner that reflects the local DNA methylation status in wild-type cells. Unexpectedly, we observe striking loss of H3K27me3 and Polycomb Repressive Complex 2 from Polycomb target gene promoters in DNA hypomethylated cells, including Hox gene clusters. Importantly, we show that many of these genes become ectopically expressed in DNA hypomethylated cells, consistent with loss of Polycomb-mediated repression. Conclusions: An intact DNA methylome is required for appropriate Polycomb-mediated gene repression by constraining Polycomb Repressive Complex 2 targeting. These observations identify a previously unappreciated role for DNA methylation in gene regulation and therefore influence our understanding of how this epigenetic mechanism contributes to normal development and disease.

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  • The enrichment in EZH2 and SUZ12 binding sites is consistent with the observed enrichment of methylation differences in PRC2 repressed regions and previous observations that DNA methylation often interact with PRC2 binding.

    “consistent with the observed enrichment of methylation differences in PRC2 repressed regions (Additional file 1: Fig. S3c) and previous observations that DNA methylation often interact with PRC2 binding [52, 53].”

    From Sex-specific DNA methylation differences in Alzheimer’s disease pathology (2021) · cites this paper as [52]

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Authors
Reddington, J. P., Perricone, S. M., Nestor, C. E., Reichmann, J., Youngson, N. A., Suzuki, M., Reinhardt, D., Dunican, D. S., Prendergast, J. G., Mjoseng, H., Ramsahoye, B. H., Whitelaw, E., Greally, J. M., Adams, I. R., Bickmore, W. A., & Meehan, R. R.
Affiliations
  • Institute of Genetics and Cancer (GB)
  • Western General Hospital (GB)
  • QIMR Berghofer Medical Research Institute (AU)
  • Albert Einstein College of Medicine (US)
Corresponding author
Meehan, Richard R
ORCID
Venue
Genome Biology
Publisher
Springer Science and Business Media LLC
Published
2013-03-25
Volume
14
Issue
3
Pages
R25-R25
ISSN
  • 1465-6906 (ISSN-L)
  • 1474-760X
DOI
10.1186/gb-2013-14-3-r25
PMC
PMC4053768
OpenAlex
W2136079563
Cited by
240
References
7
Citations by year
2026: 11 · 2025: 17 · 2024: 13 · 2023: 11 · 2022: 19 · 2021: 21 · 2020: 24 · 2019: 18 · 2018: 19 · 2017: 20 · 2016: 21 · 2015: 14 · 2014: 19 · 2013: 13
FWCI
10.01
Type
journal article
Language
en
Open access
Licence
Locations
  • Genome biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DiVA (Linkoping University) (submittedVersion, other-oa)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
Funders
  • Cleveland Clinic
  • Wellcome Trust
  • Vrije Universiteit Amsterdam
  • Hebrew University of Jerusalem
  • Medical Research Council
  • Biotechnology and Biological Sciences Research Council (BB/J021032/1)
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 › Genetics › Genetic Syndromes and Imprinting
Keywords
H3K27me3, DNA hypomethylation, polycomb repressive complex 2, Polycomb target genes, gene repression, Hox gene clusters, epigenetic regulation, DNA methylation
MeSH terms
DNA (Cytosine-5-)-Methyltransferase 1, Animals, DNA (Cytosine-5-)-Methyltransferases, Embryo, Mammalian, Fibroblasts, Gene Expression Regulation, Genes, Homeobox, Multigene Family, Histones, Lysine, Models, Genetic, Promoter Regions, Genetic, Repressor Proteins, DNA Methylation, Epigenesis, Genetic, Mice, Polycomb Repressive Complex 2

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