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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Additional file 15 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
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Additional file 14 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
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Additional file 13 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
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Additional file 5 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
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Additional file 6 of Detecting cell-of-origin and cancer-specific methylation features of cell-free DNA from Nanopore sequencing
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Additional file 1 of Detecting cell-of-origin and cancer-specific methylation features of cell-free DNA from Nanopore sequencing
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Additional file 1 of Characterizing DNA methylation signatures and their potential functional roles in Merkel cell carcinoma
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Additional file 10 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757337
Additional file 2 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757313
Additional file 3 of Local CpG density affects the trajectory and variance of age-associated DNA methylation changes
Higham, J., Kerr, L., Zhang, Q., Walker, R. M., Harris, S. E., Howard, D. M., Hawkins, E. L., Sandu, A.-L., Steele, J. D., Waiter, G. D., et al. (2022) · Figshare · doi:10.6084/m9.figshare.21351316
Additional file 11 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757340
Additional file 4 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558393
Additional file 6 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558399
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Additional file 2 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558387
Additional file 1 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757310
Additional file 9 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757334
Additional file 3 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757316
Additional file 1 of Evaluation of whole-genome DNA methylation sequencing library preparation protocols
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Additional file 1 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558384
Additional file 12 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558417
Additional file 3 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558390
Additional file 9 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558408
Additional file 1 of Distinctive epigenomic alterations in NF1-deficient cutaneous and plexiform neurofibromas drive differential MKK/p38 signaling
Grit, J. L., Johnson, B. K., Dischinger, P. S., J. Essenburg, C., Adams, M., Campbell, S., Pollard, K., Pratilas, C. A., Triche, T. J., Graveel, C. R., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13565676
Additional file 6 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757325
Additional file 11 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558414
Additional file 1 of Partial erosion on under-methylated regions and chromatin reprogramming contribute to oncogene activation in IDH mutant gliomas
Wang, X., Dai, L., Liu, Y., Li, C., Fan, D., Zhou, Y., Li, P., Kong, Q., & Su, J. (2023) · Figshare · doi:10.6084/m9.figshare.22721486
Additional file 4 of Distinctive epigenomic alterations in NF1-deficient cutaneous and plexiform neurofibromas drive differential MKK/p38 signaling
Grit, J. L., Johnson, B. K., Dischinger, P. S., J. Essenburg, C., Adams, M., Campbell, S., Pollard, K., Pratilas, C. A., Triche, T. J., Graveel, C. R., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13565685
Additional file 3 of Comprehensive analyses of partially methylated domains and differentially methylated regions in esophageal cancer reveal both cell-type- and cancer-specific epigenetic regulation
Zheng, Y., Ziman, B., Ho, A. S., Sinha, U. K., Xu, L.-Y., Li, E., Koeffler, H. P., Berman, B. P., & Lin, D.-C. (2023) · Figshare · doi:10.6084/m9.figshare.24030888
Self-citation
Additional file 5 of Susceptibility to hormone-mediated cancer is reflected by different tick rates of the epithelial and general epigenetic clock
Barrett, J. J. E., Herzog, C., Kim, Y.-N., Bartlett, T. E., Jones, A., Evans, I., Cibula, D., Zikan, M., Bjørge, L., Harbeck, N., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19211743
Additional file 8 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558405
Additional file 4 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757319
Additional file 7 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757328
Additional file 3 of Distinctive epigenomic alterations in NF1-deficient cutaneous and plexiform neurofibromas drive differential MKK/p38 signaling
Grit, J. L., Johnson, B. K., Dischinger, P. S., J. Essenburg, C., Adams, M., Campbell, S., Pollard, K., Pratilas, C. A., Triche, T. J., Graveel, C. R., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13565682
Additional file 5 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757322
Additional file 1 of Local CpG density affects the trajectory and variance of age-associated DNA methylation changes
Higham, J., Kerr, L., Zhang, Q., Walker, R. M., Harris, S. E., Howard, D. M., Hawkins, E. L., Sandu, A.-L., Steele, J. D., Waiter, G. D., et al. (2022) · Figshare · doi:10.6084/m9.figshare.21351310
Additional file 2 of Characterization of universal features of partially methylated domains across tissues and species
Decato, B. E., Qu, J., Ji, X., Wagenblast, E., Knott, S., Hannon, G. J., & Smith, A. D. (2020) · Figshare · doi:10.6084/m9.figshare.13046954
Additional file 7 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558402
Additional file 12 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757343
Additional file 10 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558411
Additional file 5 of Distinctive epigenomic alterations in NF1-deficient cutaneous and plexiform neurofibromas drive differential MKK/p38 signaling
Grit, J. L., Johnson, B. K., Dischinger, P. S., J. Essenburg, C., Adams, M., Campbell, S., Pollard, K., Pratilas, C. A., Triche, T. J., Graveel, C. R., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13565688
Additional file 13 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558420
Additional file 8 of Pan-cancer analysis revealed H3K4me1 at bivalent promoters premarks DNA hypermethylation during tumor development and identified the regulatory role of DNA methylation in relation to histone modifications
Lu, Y., Cao, Q., Yu, Y., Sun, Y., Jiang, X., & Li, X. (2023) · Figshare · doi:10.6084/m9.figshare.22757331
Additional file 2 of Distinctive epigenomic alterations in NF1-deficient cutaneous and plexiform neurofibromas drive differential MKK/p38 signaling
Grit, J. L., Johnson, B. K., Dischinger, P. S., Essenburg, C. J., Adams, M., Campbell, S., Pollard, K., Pratilas, C. A., Triche, T. J., Graveel, C. R., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13565679
Additional file 3 of A novel immune classification reveals distinct immune escape mechanism and genomic alterations: implications for immunotherapy in hepatocellular carcinoma
Liu, Z., Zhang, Y., Shi, C., Zhou, X., Xu, K., 焦德超, Sun, Z., & Han, X. (2021) · Figshare · doi:10.6084/m9.figshare.13532479
Additional file 1 of Comprehensive analyses of partially methylated domains and differentially methylated regions in esophageal cancer reveal both cell-type- and cancer-specific epigenetic regulation
Zheng, Y., Ziman, B., Ho, A. S., Sinha, U. K., Xu, L.-Y., Li, E., Koeffler, H. P., Berman, B. P., & Lin, D.-C. (2023) · Figshare · doi:10.6084/m9.figshare.24030882
Self-citation
CMAtlas: a comprehensive DNA methylation atlas for exploring epigenetic alterations in 34 human cancer types
Liu, M., Jiang, L., Zhang, L., Chen, T. L., Wang, X., Liang, Y., Shi, X., Ren, J., & Zheng, Y. (2026) · Bioinformatics · doi:10.1093/bioinformatics/btag022
“WGBS data were acquired from GEO, SRA, and previously published datasets (Zhou et al. 2018). scMeth-seq data were collected from GEO and scMethBank (Zong et al. 2022).”
DNMT1 overexpression disrupts DNA methylation homeostasis in mouse embryonic stem cellsPreprint
Elder, E., Lemieux, A., & McGraw, S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.26.701550
“While PMDs did not emerge in the Dnmt1 tet/tet methylome, its increased CpG-to-CpG variability could point to a consequence of defective methylation maintenance that, in cancer, culminates in the disproportionate methylation loss in PMDs versus non-PMD regions 52 .”
Conserved Human CpG Dinucleotides Identify Enriched Ageing-related Signals in Developmental Pathways and the BrainPreprint
Christofidou, P., & Bell, C. G. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.20.707043
Tissue-specific Mitotic Clocks Link Cumulative Stem Cell Divisions to Human Cancer SusceptibilityPreprint
Schumacher, F. R., & Wu, Y. (2026) · Research Square · doi:10.21203/rs.3.rs-9013656/v1
An unbiased approach to measure aberrant DNA methylation alterations
Downs, B. M., Hu, J., Park, J. S., Lei, H., Wang, T.-H., Pisanic, T. R., Hsieh, K., & Hoang, T. M. (2026) · Nature Communications · doi:10.1038/s41467-026-71089-5
“…whether the hypomethylation alterations identi ﬁ ed using the relative Δ Meth and Δ Meth approaches associated at different frequences within the genomic compartments of PMDs, HMDs and neither PMDs/HMDs, which studies have shown have distinct biological functions for tumor development 30 – 33 .”
Mouse embryonic stem cells exhibit cancer-like DNA methylation landscapes upon DNMT1 overexpressionPreprint
Elder, E., Lemieux, A., & McGraw, S. (2026) · Research Square · doi:10.21203/rs.3.rs-9052961/v1
Development of targeted methylome modifications in mammal cells
Lleida, A. A. (2018) · theses.fr (ABES) · doi:10.70675/6e05a7d8z70caz4650zb774z4d6156ab4205
Etude de l'implication de mécanismes épigénétiques dans la physiopathologie du myélome multiple et dans la différenciation plasmocytaire normale
Herviou, L. (2018) · theses.fr (ABES) · doi:10.70675/fba1f3d9z0660z49e2z827ezc947e8cdb04c
Analyse de signatures transcriptomiques et épigénétiques des carcinomes hépatocellulaires
Meunier, L. (2020) · theses.fr (ABES) · doi:10.70675/d5e7c2e4zaff4z46eaza0fcza52f9c3d46f1
L’hétérogénéité épigénétique intra et inter-patient dans le cas du myélome multiple
Derrien, J. (2020) · theses.fr (ABES) · doi:10.70675/ca772ec8z1a68z4ddazb884z2870e3f967b6
Impasses dans le diagnostic moléculaire des maladies rares : apport d'une meilleure caractérisation fonctionnelle des variants dans le cadre des myopathies et des lipodystrophies héréditaires
Cérino, M. (2021) · theses.fr (ABES) · doi:10.70675/8245c7bez1129z48daz9349zdb6a6dbe4f59
Dissection of coordinated interferon response by promoter elements with enhancer activity
Santiago‐Algarra, D. (2020) · theses.fr (ABES) · doi:10.70675/a064ee17zbea2z412azb9b6z12839deb2851
How Somatic Mutations cause Aging without Causing AgingPreprint
Wolf, A. M. (2026) · SSRN Electronic Journal · doi:10.2139/ssrn.6431458
OmniAge: a compendium of aging omic biomarkers links mitotic clocks to clonal hematopoiesis and causalityPreprint
Du, Z., Ling, Y., Tong, H., Guo, X. S., & Teschendorff, A. E. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.29.720033

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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