Cited by 419Epigenetics and DNA MethylationGenetic Syndromes and ImprintingGenomics and Chromatin Dynamics

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DNA methylation loss in late-replicating domains is linked to mitotic cell division

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Zhou, Wanding, Dinh, Huy Q., Ramjan, Zachary, Weisenberger, Daniel J., Nicolet, Charles M., Shen, Hui, Laird, Peter W., Berman, Benjamin P.·2018·Nature Genetics

DOI 10.1038/s41588-018-0073-4PMC PMC5893360

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Abstract

DNA methylation loss occurs frequently in cancer genomes, primarily within lamina-associated, late-replicating regions termed partially methylated domains (PMDs). We profiled 39 diverse primary tumors and 8 matched adjacent tissues using whole-genome bisulfite sequencing (WGBS) and analyzed them alongside 343 additional human and 206 mouse WGBS datasets. We identified a local CpG sequence context associated with preferential hypomethylation in PMDs. Analysis of CpGs in this context ('solo-WCGWs') identified previously undetected PMD hypomethylation in almost all healthy tissue types. PMD hypomethylation increased with age, beginning during fetal development, and appeared to track the accumulation of cell divisions. In cancer, PMD hypomethylation depth correlated with somatic mutation density and cell cycle gene expression, consistent with its reflection of mitotic history and suggesting its application as a mitotic clock. We propose that late replication leads to lifelong progressive methylation loss, which acts as a biomarker for cellular aging and which may contribute to oncogenesis.

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The DNA methylation landscape of multiple myeloma shows extensive inter- and intrapatient heterogeneity that fuels transcriptomic variability
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Characterizing DNA methylation signatures and their potential functional roles in Merkel cell carcinoma
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DNA methylation age is not affected in psoriatic skin tissue
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Background
Distinctive epigenomic alterations in NF1-deficient cutaneous and plexiform neurofibromas drive differential MKK/p38 signaling
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InfluentialSelf-citation
Inhibition of DNMT1 methyltransferase activity via glucose-regulated O-GlcNAcylation alters the epigenome
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Influential
CDCA7-associated global aberrant DNA hypomethylation translates to localized, tissue-specific transcriptional responses
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“[31]) within the combined ovca + commonPMD set.”
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Aging by the clock and yet without a program
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Background
Cell cycle gene alterations associate with a redistribution of mutation risk across chromosomal domains in human cancers
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Genome-wide single-molecule analysis of long-read DNA methylation reveals heterogeneous patterns at heterochromatin that reflect nucleosome organisation
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“It has been previously described that PMDs are characterized by their association with late-replication domains (40), hence we analyzed DMRs based on their association with late or early phase replication.”
BackgroundInfluential
Scalable screening of ternary-code DNA methylation dynamics associated with human traits
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“These include methods for profiling bulk tissues 23 or fluorescence-activated cell sorting (FACS)-puri- fied cells (e.g., bulk deep WGBS or nanopore sequencing), 24 targeted genome capture (e.g., reduced representation bisulfite sequencing [RRBS] 25 ), and the use of data techniques to interpret…”
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Homogeneous fluorescent biosensing method for DNA methyltransferase activity analysis and inhibitor screening based on highly efficient isothermal amplification
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“However, such assumption may not fully hold as recent methylation studies in large cancer datasets have revealed that a bulk of methylation alterations observed in cancers might be a consequence of global epigenetic remodeling mechanism including (i) global loss via replication related errors; and (ii) CpG island/shor…”
Background
Progressive Domain Segregation in Early Embryonic Development and Underlying Correlation to Genetic and Epigenetic Changes
Quan, H., Tian, H., Liu, S., Xue, Y., Zhang, Y., Xie, W., & Gao, Y. Q. (2021) · Cells · doi:10.3390/cells10102521 · Cited by 14
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Background
Spatial co-fragmentation pattern of cell-free DNA recapitulates in vivo chromatin organization and identifies tissues-of-originPreprint
Liu, Y., Liu, T.-Y., Weinberg, D. E., White, B., Torre, C. J. D. L., Tan, C. L., Schmitt, A. D., Selvaraj, S., Tran, V., Laurent, L. C., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/564773 · Cited by 15
“…we collected 65 published datasets (Hi-C, H3K4me1 and WGBS) from 16 cell/tissue/cancer types representing different normal and cancer cell types (Supplemental Table 2-3)(Zhou et al. 2018; Stunnenberg et al. 2016; Roadmap Epigenomics Consortium et al. 2015; ENCODE Project Consortium 2012).”
Method
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“Furthermore, isolated CpGs are especially prone to lose methylation.”
BackgroundInfluential
Accelerated epigenetic aging and DNA methylation alterations in Berardinelli–Seip congenital lipodystrophy
Qannan, A., Bejaoui, Y., Izadi, M., Yousri, N. A., Razzaq, A., Christiansen, C., Martin, G. M., Bell, J. T., Horvath, S., Oshima, J., et al. (2023) · Human Molecular Genetics · doi:10.1093/hmg/ddad016 · Cited by 14
“which are located in a WCGW context in partially methylated domains (PMDs), lose methylation in response to cell proliferation (40).”
Background
Epigenomic Characterization of Lymphoid Neoplasms
Duran‐Ferrer, M., & Martín-Subero, J. I. (2023) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-051122-100856 · Cited by 16
Charting differentially methylated regions in cancer with Rocker-meth
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“We studied the association between hypo-blocks and a recent catalog of PMDs 40 and found an extremely signi ﬁ cant overlap between these two classes of events (Fig.”
BackgroundMethodInfluential
Susceptibility to hormone-mediated cancer is reflected by different tick rates of the epithelial and general epigenetic clock
Barrett, J. J. E., Herzog, C. M. S., Kim, Y., Bartlett, T. E., Jones, A., Evans, I., Cibula, D., Zikán, M., Bjørge, L., Harbeck, N., et al. (2022) · Genome biology · doi:10.1186/s13059-022-02603-3 · Cited by 14
Computational characterization of domain‐segregated 3D chromatin structure and segmented DNA methylation status in carcinogenesis
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Human brain organoids record the passage of time over multiple years in culturePreprint
Faravelli, I., Antón-Bolaños, N., Wei, A., Faits, T., Kumar, A. S., Andreadis, S., Kästli, R., Crespo, M. M., Steiger, M., Leible, D., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.01.679721 · Cited by 14
Molecular Mechanisms of DNMT3A-3L-Mediated de novo DNA Methylation on Chromatin
Yan, Y., Zhou, X. E., Thomas, S. L., Liu, M., Lai, G.-Q., Worden, E. J., Jones, P. A., & Xu, T.-H. (2025) · doi:10.1101/2025.06.10.658647 · Cited by 14
Genomic hypomethylation in cell-free DNA predicts responses to checkpoint blockade in lung and breast cancer
Kim, K., Kim, H. M., Shin, I., Noh, S.-J., Kim, J. Y., Suh, K. J., Kim, Y.-N., Lee, J., Cho, D.-Y., Kim, S. H., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-49639-4 · Cited by 13
“This genomic demethylation process is especially observed in late-replicating partial methylation domains (PMDs) of rapidly dividing cancer genomes 18 .”
Glucocorticoids paradoxically promote steroid resistance in B cell acute lymphoblastic leukemia through CXCR4/PLC signaling
Abdoul‐Azize, S., Hami, R., Riou, G., Derambure, C., Charbonnier, C., Vannier, J., Guzmán, M. L., Schneider, P., & Boyer, O. (2024) · Nature Communications · doi:10.1038/s41467-024-48818-9 · Cited by 14
“15b, c), an epigenetic modi ﬁ cation observed in B-ALL 50 well described as a tumor stimulator that promotes mitotic cell division 51 .”
MethyLasso: a segmentation approach to analyze DNA methylation patterns and identify differentially methylated regions from whole-genome datasets
Balaramane, D., Spill, Y. G., Weber, M., & Bardet, A. F. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae880 · Cited by 13

Authors: Zhou, W., Dinh, H. Q., Ramjan, Z., Weisenberger, D. J., Nicolet, C. M., Shen, H., Laird, P. W., & Berman, B. P.
Affiliations: Van Andel Institute (US)
Cedars-Sinai Medical Center (US)
University of Southern California (US)
Corresponding author: Shen, Hui
Laird, Peter W.
Berman, Benjamin P.
ORCID: Zhou, Wanding
Dinh, Huy Q.
Weisenberger, Daniel J.
Nicolet, Charles M.
Shen, Hui
Laird, Peter W.
Berman, Benjamin P.
Venue: Nature Genetics
Publisher: Springer Science and Business Media LLC
Published: 2018-04
Volume: 50
Issue: 4
Pages: 591-602
ISSN: 1061-4036 (ISSN-L)
1546-1718
DOI: 10.1038/s41588-018-0073-4
PMC: PMC5893360
OpenAlex: W2795164082
Cited by: 405
References: 78
Citations by year: 2026: 40 · 2025: 52 · 2024: 58 · 2023: 59 · 2022: 55 · 2021: 57 · 2020: 43 · 2019: 26 · 2018: 15
FWCI: 12.47
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Genetics (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Ovarian Cancer Research Fund (373933)
University of Southern California
Cedars-Sinai Medical Center
National Institutes of Health
National Human Genome Research Institute (R01HG006705)
National Cancer Institute (U24CA143882, R01CA170550, CA184826, U24CA210969, U01CA184826)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords: DNA methylation loss, partially methylated domains, cellular aging, cell cycle gene expression, cancer epigenetics, fetal development, carcinogenesis, age-related methylation
MeSH terms: Whole Genome Sequencing, Aging, Animals, Cell Division, DNA Replication, DNA, Neoplasm, Female, Humans, Male, Mitosis, Neoplasms, Pregnancy, CpG Islands, DNA Methylation, Embryonic Development, Mice

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DNA methylation loss in late-replicating domains is linked to mitotic cell division

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