Linking DNA methylation and histone modification: patterns and paradigms
Abstract
Both DNA methylation and histone modification are involved in establishing patterns of gene repression during development. Certain forms of histone methylation cause local formation of heterochromatin, which is readily reversible, whereas DNA methylation leads to stable long-term repression. It has recently become apparent that DNA methylation and histone modification pathways can be dependent on one another, and that this crosstalk can be mediated by biochemical interactions between SET domain histone methyltransferases and DNA methyltransferases. Relationships between DNA methylation and histone modification have implications for understanding normal development as well as somatic cell reprogramming and tumorigenesis.
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The increase in scale presents computational opportunities, allowing benefitting from 'big data' approaches, most notably deep learning, developed in fields such as image and text analysis, in which data sets tend to have many more samples than were available in genomics thus far.
“On the other hand, the increase in scale presents computational opportunities. It allows benefitting from ‘big data’ approaches, most notably deep learning193, developed in fields such as image and text analysis, in which data sets tend to have many more samples than were available in genomics thus far.”
From Revealing the vectors of cellular identity with single-cell genomics (2016) · cites this paper as [193]
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Integrative analysis of 111 reference human epigenomes
Roadmap Epigenomics Consortium, Kundaje, A., Meuleman, W., Ernst, J., Bilenky, M., Yen, A., Heravi-Moussavi, A., Kheradpour, P., Zhang, Z., Wang, J., et al. (2015) · Nature · doi:10.1038/nature14248 · Cited by 6,368 · see citing works
Human DNA methylomes at base resolution show widespread epigenomic differences
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Establishing, maintaining and modifying DNA methylation patterns in plants and animals
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“The remaining unmethylated CG dinucleotides are mostly found near gene promoters in dense clusters known as CpG islands”
BackgroundA decade of exploring the cancer epigenome—biological and translational implications
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Cell-free nucleic acids as biomarkers in cancer patients
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Parental olfactory experience influences behavior and neural structure in subsequent generations
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Epigenome-wide association studies for common human diseases
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“This could be achieved using ChIP–seq experiments, either for the many histone modifications known to correlate with DNA”
MethodThe epigenetics of epithelial-mesenchymal plasticity in cancer
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Dnmt3a is essential for hematopoietic stem cell differentiation
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“Histone modifications are thought to have a primary and dynamic role in the epigenetic regulation of gene expression during developmen”
BackgroundTET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity
Williams, K., Christensen, J., Pedersen, M. T., Johansen, J. V., Cloos, P. A. C., Rappsilber, J., & Helin, K. (2011) · Nature · doi:10.1038/nature10066 · Cited by 1,021 · see citing works
Acute Exercise Remodels Promoter Methylation in Human Skeletal Muscle
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“DNA methylation is a major epigenetic modification that suppresses gene expression by modulating the access of the transcription machinery to the chromatin or by recruiting methyl binding proteins (Cedar and Bergman, 2009).”
BackgroundDNA Methylation in MammalsPreprint
Li, E., & Zhang, Y. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a019133 · Cited by 952 · see citing works
Molecular Signals of Epigenetic States
Bonasio, R., Tu, S., & Reinberg, D. (2010) · Science · doi:10.1126/science.1191078 · Cited by 912 · see citing works
DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines
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“DNA methylation is thought to interact with histone modifications during the regulation of gene-expression [36,37].”
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“Numerous studies have shown a dynamic interaction between H3K27me3 and DNA methylation (Cedar and Bergman, 2009). n lysate or immunoprecipitated HA-tagged H3.”
BackgroundComprehensive Analysis of Silencing Mutants Reveals Complex Regulation of the Arabidopsis Methylome
Stroud, H., Greenberg, M. V. C., Feng, S.-H., Bernatavichute, Y. V., & Jacobsen, S. (2013) · Cell · doi:10.1016/j.cell.2012.10.054 · Cited by 819 · see citing works
“Relationship between Histone Modifications and DNA Methylation There is growing evidence regarding interplays between histone modifications and DNAmethylation (Cedar and Bergman, 2009).”
Enhancer function: new insights into the regulation of tissue-specific gene expression
Ong, C.-T., & Corces, V. G. (2011) · Nature Reviews Genetics · doi:10.1038/nrg2957 · Cited by 929 · see citing works
Distinct epigenomic landscapes of pluripotent and lineage-committed human cells
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“H3K9me3 or H3K27me3 and DNA methylation than previously proposed (Cedar and Bergman, 2009; Suzuki and Bird, 2008).”
BackgroundDNA Methylation: Superior or Subordinate in the Epigenetic Hierarchy?
Jin, B., Li, Y., & Robertson, K. D. (2011) · Genes & Cancer · doi:10.1177/1947601910393957 · Cited by 818 · see citing works
“2) after DNA replication.(24) Trimethylation of histone H3 lysine 9 (H3K9), histone H3 lysine 27 (H3K27), and histone H4 lysine 20 (H4K20) has been suggested to be a prerequisite for subsequent DNA methylation, which appears to be attributable to physical associations between the components of these histone methylatio…”
BackgroundSerrano-Gomez, S. J., Maziveyi, M., & Alahari, S. K. (2016) · Molecular Cancer · doi:10.1186/s12943-016-0502-x · Cited by 817 · see citing works
“to access genes within the region [36].”
BackgroundThe genetic architecture of multiple myeloma
Morgan, G. J., Walker, B. A., & Davies, F. E. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3257 · Cited by 913 · see citing works
De Novo Epigenetic Programs Inhibit PD-1 Blockade-Mediated T Cell Rejuvenation
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“transcription factors and epigenetic modifications are associated with changes in chromatin accessibility, recent evidence supports the notion that DNA methylation is a critical epigenetic mechanism for establishing stable gene-silencing programs (Bintu et al., 2016; Cedar and Bergman, 2009).”
SDH mutations establish a hypermethylator phenotype in paraganglioma
Letouzé, E., Martinelli, C., Loriot, C., Burnichon, N., Abermil, N., Ottolenghi, C., Janin, M., Menara, M., Nguyen, A. T., Benit, P., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.04.018 · Cited by 776 · see citing works
“As both H3K9 and H3K27 methylation are closely linked with DNA methylation (Cedar and Bergman, 2009), these effects on histone methylation may contribute to the establishment of the hypermethylator phenotype.”
BackgroundRethinking how DNA methylation patterns are maintained
Jones, P. A., & Liang, G. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2651 · Cited by 767 · see citing works
“It is generally thought that patterns are established during embryonic development and are then faithfully inherited in somatic cells by a 'maintenance' mechanis”
BackgroundRevealing the vectors of cellular identity with single-cell genomics
Wagner, A., Regev, A., & Yosef, N. (2016) · Nature Biotechnology · doi:10.1038/nbt.3711 · Cited by 632 · see citing works
“These methods hold promise for elucidating the epigenetic controls of cellular identity 193,194 .”
MethodEpigenomic Analysis of Multilineage Differentiation of Human Embryonic Stem Cells
Xie, W., Schultz, M. D., Lister, R., Hou, Z., Rajagopal, N., Ray, P. R., Whitaker, J. W., Tian, S., Hawkins, R. D., Leung, D., et al. (2013) · Cell · doi:10.1016/j.cell.2013.04.022 · Cited by 721 · see citing works
“Z, that are incompatible to DNA methylation (Cedar and Bergman, 2009).”
The Honey Bee Epigenomes: Differential Methylation of Brain DNA in Queens and Workers
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“Our study provides experimental evidence that at least 560 differentially methylated ubiquitously expressed genes are involved in generating molecular brain diversity in female honey bees. Although it is still unclear how methylation might be linked to the gene regulatory networks, it has been proposed that DNA methyl…”
BackgroundNext-Generation Systemic Acquired Resistance
Luna, E., Bruce, T. J. A., ROBERTS, M. R., Flors, V., & Ton, J. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.187468 · Cited by 725 · see citing works
Structure and Function of Mammalian DNA Methyltransferases
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Histone acetylation: molecular mnemonics on the chromatin
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Prenatal environmental exposures, epigenetics, and disease
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“Two examples include coordinated epigenetic modifications of chromatin by DNA methylation and posttranslational covalent modifications of histone proteins [4,11,12] and micro-RNA-induced suppression of gene expression during development [13].”
Transposable Elements, Epigenetics, and Genome Evolution
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“Mammalian genomes are chemically modified by DNA cytosine methylation, an inheritable epigenetic mark that is implicated in many biological and pathological processes, including gene regulation, genomic imprinting, X-chromosome inactivation, suppression of transposable elements, and tumorigenesis (Cedar and Bergman 20…”
BackgroundLineage plasticity in cancer: a shared pathway of therapeutic resistance
Quintanal-Villalonga, À., Chan, J. M., Yu, H. A., Pe’er, D., Sawyers, C. L., Sen, T., & Rudin, C. M. (2020) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-020-0340-z · Cited by 573 · see citing works
Epigenetic modifications in cancer
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“Histone modifications influence chromatin structure which plays an important role in gene regulation and carcinogenesis (16).”
BackgroundMethyl-cpG-binding domain proteins: readers of the epigenome
Du, Q., Luu, P.-L., Stirzaker, C., & Clark, S. J. (2015) · Epigenomics · doi:10.2217/epi.15.39 · Cited by 544 · see citing works
DNA methylation dynamics in health and disease
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Self-citationEpigenetic and immune function profiles associated with posttraumatic stress disorder
Uddin, M., Aiello, A. E., Wildman, D. E., Koenen, K. C., Pawelec, G., de los Santos, R., Goldmann, E., & Galea, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910794107 · Cited by 518 · see citing works
“Although the bulk of these genes’ activity is typically thought to occur early in development (36), recent work has suggested that their enzymatic productsmay also play a role in DNA methylation maintenance during somatic cell division (35).”
BackgroundDelcuve, G. P., Khan, D. H., & Davie, J. R. (2012) · Clinical Epigenetics · doi:10.1186/1868-7083-4-5 · Cited by 505 · see citing works
“H3K9me3, on the other hand, is associated with DNA methylation and is a stable mark, denoting permanent silencing [58,59].”
BackgroundSpheroid Culture of Mesenchymal Stem Cells
Cesarz, Z., & Tamama, K. (2016) · Stem Cells International · doi:10.1155/2016/9176357 · Cited by 475 · see citing works
“[135] H.”
BackgroundEpigenetic mechanisms in diabetic complications and metabolic memory
Reddy, M. A., Zhang, E., & Natarajan, R. D. (2014) · Diabetologia · doi:10.1007/s00125-014-3462-y · Cited by 498 · see citing works
“Overall, the crosstalk and interplay between histone PTMs, DNAme and ncRNAs provides another layer of epigenetic regulation to impact gene expression [62, 63], which, if dysregulated, can result in diabetes and associated complications.”
Unravelling the biology of SCLC: implications for therapy
Sabari, J. K., Lok, B. H., Laird, J. H., Poirier, J. T., & Rudin, C. M. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.71 · Cited by 495 · see citing works
TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS
Deplus, R., Delatte, B., Schwinn, M. K., Defrance, M., Méndez, J., Murphy, N., Dawson, M. A., Volkmar, M., Putmans, P., Calonne, E., et al. (2013) · The EMBO Journal · doi:10.1038/emboj.2012.357 · Cited by 488 · see citing works
“Until recently, the only known epigenetic mark on DNA was 5-methylcytosine (mC), established and propagated by DNA methyltransferases, and generally associated with gene repression (Suzuki and Bird, 2008; Cedar and Bergman, 2009; Ndlovu et al , 2011).”
Circulating Tumor Cells and Circulating Tumor DNA
Alix‐Panabières, C., Schwarzenbach, H., & Pantel, K. (2011) · Annual Review of Medicine · doi:10.1146/annurev-med-062310-094219 · Cited by 485 · see citing works
Genome, epigenome and RNA sequences of monozygotic twins discordant for multiple sclerosis
Baranzini, S. E., Mudge, J., van Velkinburgh, J. C., Khankhanian, P., Khrebtukova, I., Miller, N. A., Zhang, L., Farmer, A. D., Bell, C. J., Kim, R. W., et al. (2010) · Nature · doi:10.1038/nature08990 · Cited by 476 · see citing works
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“H3K4me3 was also previously found to be inversely correlated with DNA methylation [9], with evidence for causality pointing in both directions.”
BackgroundInfluentialDong, C., Wu, Y., Yao, J., Wang, Y., Yu, Y., Rychahou, P. G., Evers, B. M., & Zhou, B. P. (2012) · Journal of Clinical Investigation · doi:10.1172/jci57349 · Cited by 468 · see citing works
“In the first mode, G9a creates H3K9me2 via its catalytic activity, which subsequently recruits HP1 and DNMTs for DNA methyla - tion (17).”
InfluentialSex differences in neural mechanisms mediating reward and addiction
Becker, J. B., & Chartoff, E. H. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0125-6 · Cited by 455 · see citing works
Season of Conception in Rural Gambia Affects DNA Methylation at Putative Human Metastable Epialleles
Waterland, R. A., Kellermayer, R., Laritsky, E., Rayco‐Solon, P., Harris, R. A., Travisano, M., Zhang, W., Torskaya, M. S., Zhang, J., Shen, L., et al. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001252 · Cited by 454 · see citing works
“Of various interacting epigenetic mechanisms including cytosine methylation in DNA, covalent histone modifications, and autoregulatory DNA binding proteins, DNA methylation is recognized as the most stable epigenetic mark [14], making it a prime candidate to mediate the life-long epigenetic changes postulated in the d…”
BackgroundProgramming of DNA Methylation Patterns
Cedar, H., & Bergman, Y. (2012) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052610-091920 · Cited by 439 · see citing works
“Polycomb complex: a complex of proteins bound at specific genes where they cause repression, probably through histone modification modification is probably mediated by histone methylases capable of generating heterochromatin and then recruiting Dnmts that carry out targeted local methylation many days after the initia…”
BackgroundSelf-citationMaddocks, O. D. K., Labuschagne, C. F., Adams, P. D., & Vousden, K. H. (2016) · Molecular Cell · doi:10.1016/j.molcel.2015.12.014 · Cited by 440 · see citing works
“The function of methylation reactions is context and substrate dependent; for example, DNA and histone methylation are epigenetic modifications that have important influences on chromatin structure and regulation of gene expression (Cedar and Bergman, 2009; Gut and Verdin, 2013).”
BackgroundChouliaras, L., Mastroeni, D., Delvaux, E., Grover, A., Kenis, G., Hof, P. R., Steinbusch, H. W. M., Coleman, P. D., Rutten, B. P. F., & van den Hove, D. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.02.021 · Cited by 422 · see citing works
“Methylation of CpG di-nucleotides is catalyzed by DNAmethyltransferases (Dnmts), disrupts the binding of transcription factors and recruits proteins known as methylCpGebinding domain proteins (MBDs) that are associated with chromatin compaction and gene silencing (Cedar and Bergman, 2009).”
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“The DNA methyltransferases DNMT3A/B and DNMT1 are responsible for the establishment and maintenance of the DNA methylation mark, respectively (Cedar and Bergman 2009).”
BackgroundInfluentialEpigenetics across the human lifespan
Kanherkar, R. R., Bhatia-Dey, N., & Csoka, A. B. (2014) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2014.00049 · Cited by 407 · see citing works
“Addition or removal of methyl groups on DNA (see above) and histones and acetyl groups on histones are the prime mechanisms of changing the epigenetic landscape (Cedar and Bergman, 2009).”
BackgroundEpigenetic reprogramming in mouse pre-implantation development and primordial germ cells
Saitou, M., Kagiwada, S., & Kurimoto, K. (2011) · Development · doi:10.1242/dev.050849 · Cited by 410 · see citing works
“5mC and histone modifications 5mC and histone modifications act in concert to form an appropriate epigenome during development and in adult cells (Cedar and Bergman, 2009).”
BackgroundRapid adaptive responses to climate change in corals
Torda, G., Donelson, J. M., Aranda, M., Barshis, D. J., Bay, L. K., Berumen, M. L., Bourne, D. G., Cantin, N. E., Forêt, S., Matz, M. V., et al. (2017) · Nature Climate Change · doi:10.1038/nclimate3374 · Cited by 410 · see citing works
Epigenetics and cardiovascular disease
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Genetics and epigenetics of rheumatoid arthritis
Viatte, S., Plant, D., & Raychaudhuri, S. (2013) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2012.237 · Cited by 399 · see citing works
Polymerase-IV occupancy at RNA-directed DNA methylation sites requires SHH1
Law, J. A., Du, J.-M., Hale, C. J., Feng, S.-H., Krajewski, K., Palanca, A., Strahl, B., Patel, D., & Jacobsen, S. (2013) · Nature · doi:10.1038/nature12178 · Cited by 378 · see citing works
Regulation of mammalian DNA methyltransferases: a route to new mechanisms
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Identification of genetic elements that autonomously determine DNA methylation states
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“, making it possible that chromatin could be a determining factor in establishing global methylation patterns in mammals, as wel”
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“…independently regulate gene transcription, recent studies have shown that DNA methylation and histone modifications can also work in concordance (Cedar and Bergman, 2009); for example, gene transcription could also be regulated by association of Dnmt1, methyl CpG binding protein 2 (MeCP2) and…”
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“The molecular basis includes the methylation of cytosines in CpG dinucleotides, which, together with histone modifications, noncoding RNAs, and localization, influence the accessibility of a genomic locus to the transcriptional machinery (Bernstein et al., 2007; Cedar & Bergman, 2009).”
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“While histone modification has been shown to play a role in a variety of host processes, including cell development (37), host metabolism (38), and ISG induction (36), these findings represent additional evidence that pathogens can exploit the same repression processes to modulate and control the host IFN response (39…”
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- Authors
- Cedar, H., & Bergman, Y.
- Affiliations
- Hebrew University of Jerusalem (IL)
- Corresponding author
- Cedar, Howard
- Venue
- Nature Reviews Genetics
- Published
- 2009-05
- Volume
- 10
- Issue
- 5
- Pages
- 295-304
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W1976626368
- Cited by
- 2,267
- References
- 108
- Citations by year
- 2026: 50 · 2025: 68 · 2024: 87 · 2023: 90 · 2022: 107 · 2021: 135 · 2020: 130 · 2019: 119 · 2018: 131 · 2017: 165 · 2016: 169 · 2015: 183 · 2014: 169 · 2013: 163 · 2012: 184
- FWCI
- 12.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- 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 › Cancer-related gene regulation
- Keywords
- DNA methylation, histone modifications, epigenetic crosstalk, gene repression, heterochromatin, DNA methyltransferases, chromatin structure, somatic cell reprogramming, carcinogenesis, development (biology)
- MeSH terms
- Histone Methyltransferases, Animals, DNA, Heterochromatin, Histones, Humans, Models, Biological, Neoplasms, Histone-Lysine N-Methyltransferase, DNA-Cytosine Methylases, DNA Methylation
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