Cited by 536Epigenetics and DNA MethylationGenomics and Chromatin DynamicsGenetic Syndromes and Imprinting

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The histone mark H3K36me2 recruits DNMT3A and shapes the intergenic DNA methylation landscape

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Weinberg, Daniel N., Papillon-Cavanagh, Simon, Chen, Haifen, Yue, Yuan, Chen, Xiao, Rajagopalan, Kartik N., Horth, Cynthia, McGuire, John T., Xu, Xinjing, Nikbakht, Hamid, Lemiesz, Agata E., Marchione, Dylan M., Marunde, Matthew R., Meiners, Matthew J., Cheek, Marcus A., Keogh, Michael-Christopher, Bareke, Eric, Djedid, Anissa, Harutyunyan, Ashot S., Jabado, Nada, Garcia, Benjamin A., Li, Haitao, Allis, C. David, Majewski, Jacek, Lu, Chao·2019·Nature

DOI 10.1038/s41586-019-1534-3PMC PMC6742567

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Abstract

Enzymes that catalyse CpG methylation in DNA, including the DNA methyltransferases 1 (DNMT1), 3A (DNMT3A) and 3B (DNMT3B), are indispensable for mammalian tissue development and homeostasis 1-4. They are also implicated in human developmental disorders and cancers 5-8, supporting the critical role of DNA methylation in the specification and maintenance of cell fate. Previous studies have suggested that post-translational modifications of histones are involved in specifying patterns of DNA methyltransferase localization and DNA methylation at promoters and actively transcribed gene bodies 9-11. However, the mechanisms that control the establishment and maintenance of intergenic DNA methylation remain poorly understood. Tatton-Brown-Rahman syndrome (TBRS) is a childhood overgrowth disorder that is defined by germline mutations in DNMT3A. TBRS shares clinical features with Sotos syndrome (which is caused by haploinsufficiency of NSD1, a histone methyltransferase that catalyses the dimethylation of histone H3 at K36 (H3K36me2)8,12,13), which suggests that there is a mechanistic link between these two diseases. Here we report that NSD1-mediated H3K36me2 is required for the recruitment of DNMT3A and maintenance of DNA methylation at intergenic regions. Genome-wide analysis shows that the binding and activity of DNMT3A colocalize with H3K36me2 at non-coding regions of euchromatin. Genetic ablation of Nsd1 and its paralogue Nsd2 in mouse cells results in a redistribution of DNMT3A to H3K36me3-modified gene bodies and a reduction in the methylation of intergenic DNA. Blood samples from patients with Sotos syndrome and NSD1-mutant tumours also exhibit hypomethylation of intergenic DNA. The PWWP domain of DNMT3A shows dual recognition of H3K36me2 and H3K36me3 in vitro, with a higher binding affinity towards H3K36me2 that is abrogated by TBRS-derived missense mutations. Together, our study reveals a trans-chromatin regulatory pathway that connects aberrant intergenic CpG methylation to human neoplastic and developmental overgrowth.

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Authors: Weinberg, D. N., Papillon-Cavanagh, S., Chen, H., Yue, Y., Chen, X., Rajagopalan, K. N., Horth, C., McGuire, J. T., Xu, X., Nikbakht, H., Lemiesz, A. E., Marchione, D. M., Marunde, M. R., Meiners, M. J., Cheek, M. A., Keogh, M.-C., Bareke, E., Djedid, A., Harutyunyan, A. S., Jabado, N., Garcia, B. A., Li, H., Allis, C. D., Majewski, J., & Lu, C.
Affiliations: Rockefeller University (US)
Center for Life Sciences (CN)
Columbia University Irving Medical Center (US)
McGill University (CA)
University of Pennsylvania (US)
McGill University Health Centre (CA)
Corresponding author: Allis, C. David
Majewski, Jacek
ORCID: Weinberg, Daniel N.
Chen, Xiao
Rajagopalan, Kartik N.
Horth, Cynthia
Xu, Xinjing
Nikbakht, Hamid
Marchione, Dylan M.
Marunde, Matthew R.
Meiners, Matthew J.
Cheek, Marcus A.
Keogh, Michael-Christopher
Bareke, Eric
Djedid, Anissa
Harutyunyan, Ashot S.
Jabado, Nada
Garcia, Benjamin A.
Li, Haitao
Allis, C. David
Majewski, Jacek
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2019-09-04
Volume: 573
Issue: 7773
Pages: 281-286
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-019-1534-3
PMC: PMC6742567
OpenAlex: W2972254987
Cited by: 524
References: 47
Citations by year: 2026: 48 · 2025: 66 · 2024: 85 · 2023: 79 · 2022: 95 · 2021: 97 · 2020: 46 · 2019: 7
FWCI: 20.43
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Cancer Institute (P01CA196539, R00CA212257, F30CA224971, P30CA013696)
National Institute of General Medical Sciences (T32GM008275, R44GM117683, R44GM116584, T32GM007739)
National Institute of Environmental Health Sciences (P30ES013508)
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: H3K36me3, DNMT3A, DNA methylation, intergenic regions, CpG methylation, NSD1, NSD2, PWWP domain, histone modifications, Sotos syndrome, Tatton-Brown-Rahman syndrome, overgrowth disorder, histone methyltransferase
MeSH terms: Protein Domains, DNA Methyltransferase 3A, Animals, Cell Line, DNA (Cytosine-5-)-Methyltransferases, Growth Disorders, Histones, Humans, Protein Binding, DNA Methylation, Protein Transport, DNA, Intergenic, Mice, Genome-Wide Association Study, Sotos Syndrome

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The histone mark H3K36me2 recruits DNMT3A and shapes the intergenic DNA methylation landscape

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