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DNA Methylation: A Mechanism for Embedding Early Life Experiences in the Genome
Open accessAbstract
Although epidemiological data provide evidence that early life experience plays a critical role in human development, the mechanism of how this works remains in question. Recent data from human and animal literature suggest that epigenetic changes, such as DNA methylation, are involved not only in cellular differentiation but also in the modulation of genome function in response to early life experience affecting gene function and the phenotype. Such modulations may serve as a mechanism for life-long genome adaptation. These changes seem to be widely distributed across the genome and to involve central and peripheral systems. Examining the environmental circumstances associated with the onset and reversal of DNA methylation will be critical for understanding risk and resiliency.
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From The applied implications of epigenetics in anxiety, affective and stress-related disorders - A review and synthesis on psychosocial stress, psychotherapy and prevention (2020) · cites this paper as Szyf & Bick, 2013
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Cites
Jenuwein, T., & Allis, C. D. (2001) · Science · doi:10.1126/science.1063127 · Cited by 9,756
The language of covalent histone modifications
Strahl, B. D., & Allis, C. D. (2000) · Nature · doi:10.1038/47412 · Cited by 8,679
Finding the missing heritability of complex diseases
Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., McCarthy, M. I., Ramos, E. M., Cardon, L. R., Chakravarti, A., et al. (2009) · Nature · doi:10.1038/nature08494 · Cited by 8,336
Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., et al. (2003) · Science · doi:10.1126/science.1083968 · Cited by 8,120
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177
Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., Turecki, G., & Meaney, M. J. (2009) · Nature Neuroscience · doi:10.1038/nn.2270 · Cited by 3,531
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170
DNA Methylation and Gene Function
Razin, A., & Riggs, A. D. (1980) · Science · doi:10.1126/science.6254144 · Cited by 2,076
Nongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999) · Science · doi:10.1126/science.286.5442.1155 · Cited by 1,965
Risch, N., Herrell, R., Lehner, T., Liang, K.-Y., Eaves, L., Hoh, J., Griem, A., Kovacs, M., Ott, J., & Merikangas, K. R. (2009) · JAMA · doi:10.1001/jama.2009.878 · Cited by 1,655 · cited 2×
“Although the interaction between genotypes and environmental conditions has been an exciting possibility, there is significant controversy regarding the replicability of these original findings (Risch et al., 2009).”
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008) · Epigenetics · doi:10.4161/epi.3.2.6034 · Cited by 1,432
Lasting epigenetic influence of early-life adversity on the BDNF gene
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.028 · Cited by 1,273
Derepression of BDNF Transcription Involves Calcium-Dependent Phosphorylation of MeCP2
Chen, W. G., Chang, Q., Lin, Y., Meissner, A., West, A. E., Griffith, E. C., Jaenisch, R., & Greenberg, M. E. (2003) · Science · doi:10.1126/science.1086446 · Cited by 1,232
Dynamic DNA methylation programs persistent adverse effects of early-life stress
Murgatroyd, C., Patchev, A. V., Wu, Y., Micale, V., Bockmühl, Y., Fischer, D., Holsboer, F., Wotjak, C. T., Almeida, O. F. X., & Spengler, D. (2009) · Nature Neuroscience · doi:10.1038/nn.2436 · Cited by 1,162
TET1 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
MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex
Ng, H., Zhang, Y., Hendrich, B., Johnson, C. A., Turner, B. M., Erdjument‐Bromage, H., Tempst, P., Reinberg, D., & Bird, A. P. (1999) · Nature Genetics · doi:10.1038/12659 · Cited by 963
Zhou, Z., Hong, E. J., Cohen, S., Zhao, W.-N., Ho, H.-Y. H., Schmidt, L., Chen, W. G., Lin, Y., Savner, E., Griffith, E. C., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.037 · Cited by 877
Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor
Ressler, K. J., Mercer, K. B., Bradley, B., Jovanovic, T., Mahan, A., Kerley, K., Norrholm, S. D., Kilaru, V., Smith, A. K., Myers, A. J., et al. (2011) · Nature · doi:10.1038/nature09856 · Cited by 800
The histone H4 acetyltransferase MOF uses a C2HC zinc finger for substrate recognition
Akhtar, A., & Becker, P. B. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve022 · Cited by 632
A mammalian protein with specific demethylase activity for mCpG DNA
Bhattacharya, S. K., Ramchandani, S., Cervoni, N., & Moshe Szyf, A. (1999) · Nature · doi:10.1038/17533 · Cited by 616
The social environment and the epigenome
Szyf, M., McGowan, P. O., & Meaney, M. J. (2007) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20357 · Cited by 547
Weaver, I. C. G., D'Alessio, A. C., Brown, S. E., Hellstrom, I. C., Dymov, S., Sharma, S., Szyf, M., & Meaney, M. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4164-06.2007 · Cited by 508
Broad Epigenetic Signature of Maternal Care in the Brain of Adult Rats
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C. T., Hallett, M., Meaney, M. J., & Szyf, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014739 · Cited by 452
Associations with early-life socio-economic position in adult DNA methylation
Borghol, N., Suderman, M. J., McArdle, W. L., Racine, A., Hallett, M. T., Pembrey, M. E., Hertzman, C., Power, C., & Szyf, M. (2011) · International Journal of Epidemiology · doi:10.1093/ije/dyr147 · Cited by 429
CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2
Comb, M., & Goodman, H. M. (1990) · Nucleic Acids Research · doi:10.1093/nar/18.13.3975 · Cited by 422
Promoter-Wide Hypermethylation of the Ribosomal RNA Gene Promoter in the Suicide Brain
McGowan, P. O., Sasaki, A., Huang, T. C. T., Unterberger, A., Suderman, M. J., Ernst, C., Meaney, M. J., Turecki, G., & Szyf, M. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002085 · Cited by 379
Genomic mapping of 5-hydroxymethylcytosine in the human brain
Jin, S.-G., Wu, X., Li, A. X., & Pfeifer, G. P. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr120 · Cited by 375
Valproate Induces Replication-independent Active DNA Demethylation
Detich, N., Bovenzi, V., & Szyf, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303740200 · Cited by 345
Self-citationDNA methylation is a reversible biological signal
Ramchandani, S., Bhattacharya, S. K., Cervoni, N., & Moshe Szyf, A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.6107 · Cited by 342
Poulter, M. O., Du, L., Weaver, I. C. G., Palkovits, M., Faludi, G., Merali, Z., Szyf, M., & Anisman, H. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.05.028 · Cited by 331
Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus
Suderman, M., McGowan, P. O., Sasaki, A., Huang, T. C. T., Hallett, M. T., Meaney, M. J., Turecki, G., & Szyf, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121260109 · Cited by 327
DNA methylation patterns Formation and function
Razin, A., & Moshe Szyf, A. (1984) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/0167-4781(84)90043-5 · Cited by 318
Self-citationTelomere length and early severe social deprivation: linking early adversity and cellular aging
Drury, S. S., Theall, K., Gleason, M. M., Smyke, A. T., De Vivo, I., Wong, J. Y. Y., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.53 · Cited by 316
The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells
Provençal, N., Suderman, M. J., Guillemin, C., Massart, R., Ruggiero, A., Wang, D., Bennett, A. J., Pierre, P. J., Friedman, D. P., Côté, S. M., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1470-12.2012 · Cited by 312
Demethylase Activity Is Directed by Histone Acetylation
Cervoni, N., & Szyf, M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m103921200 · Cited by 292
Self-citationNaumova, O. Y., Lee, M., Koposov, R. A., Szyf, M., Dozier, M., & Grigorenko, E. L. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000605 · Cited by 260
Histone deacetylase as a therapeutic target
Krämer, O. H., Göttlicher, M., & Heinzel, T. (2001) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(01)00438-6 · Cited by 256
Ernst, C., Deleva, V., Deng, X., Sequeira, A., Pomarenski, A., Klempan, T., Ernst, N., Quirion, R., Gratton, A., Szyf, M., et al. (2009) · Archives of General Psychiatry · doi:10.1001/archpsyc.66.1.22 · Cited by 235
Linthorst, A., Flachskamm, C., Müller-Preuss, P., Holsboer, F., & Reul, J. M. H. M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02920.1995 · Cited by 234
Simonini, M. V., Camargo, L. M., Dong, E., Maloku, E., Veldić, M., Costa, E., & Guidotti, A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510341103 · Cited by 230
A 10-year perspective of motherless-mother monkey behavior.
Ruppenthal, G. C., & Al, E. (1976) · Journal of Abnormal Psychology · doi:10.1037//0021-843x.85.4.341 · Cited by 218
A 10-year perspective of motherless-mother monkey behavior.
Ruppenthal, G. C., Arling, G. L., Harlow, H. F., et al. (1976) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.85.4.341 · Cited by 193
Wolffe, A. P., Jones, P. L., & Wade, P. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.5894 · Cited by 185
Promoter-specific Activation and Demethylation by MBD2/Demethylase
Detich, N., Théberge, J., & Szyf, M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c200408200 · Cited by 179
Self-citationThe Methyl Donor S-Adenosylmethionine Inhibits Active Demethylation of DNA
Detich, N., Hamm, S., Just, G., Knox, J. D., & Moshe Szyf, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211813200 · Cited by 179
Weidle, U. H., & Grossmann, A. (2000) · PubMed · Cited by 129
Inamdar, N. M., Ehrlich, K. C., & Ehrlich, M. (1991) · Plant Molecular Biology · doi:10.1007/bf00036811 · Cited by 120
EFFECTS OF MATERNAL AND PEER SEPARATIONS ON YOUNG MONKEYS
Suomi, S. J., Collins, M. L., Harlow, H. F., & Ruppenthal, G. C. (1976) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1976.tb00382.x · Cited by 117
Transcriptomics in ecotoxicology
Schirmer, K., Fischer, B. B., Madureira, D. J., & Pillai, S. (2010) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-010-3662-3 · Cited by 114
Adams, R. L. P., Burdon, R. H., & Taylor, J. H. (1982) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238209108714 · Cited by 86
Epigenetic Programming of the rRNA Promoter by MBD3
Brown, S. E., & Szyf, M. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01880-06 · Cited by 73
Self-citationEpigenetic factors and cardiac development
van Weerd, J. H., Koshiba‐Takeuchi, K., Kwon, C. D., & Takeuchi, J. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvr138 · Cited by 71
Epigenetic Programming of the rRNA Promoter by MBD3
Brown, S. E., & Szyf, M. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.02037-07 · Cited by 58
Self-citationEukaryotic DNA methyltransferases – structure and function
Adams, R. L. P. (1995) · Bioessays · doi:10.1002/bies.950170209 · Cited by 55
Power, C., Jefferis, B. J. M. H., Manor, O., & Hertzman, C. (2006) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2005.07.028 · Cited by 54
Histone acetylation by p300 is involved in CREB-mediated transcription on chromatin
Yuan, L. W., & Gambee, J. E. (2001) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(01)00141-0 · Cited by 45
HIDden targets of microRNAs for growth control
Bergmann, A., & Lane, M. E. (2003) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(03)00175-0 · Cited by 44
EUKARYOTIC DNA METHYLTRANSFERASES
Vertino, P. M. (1999) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789812813077_0012 · Cited by 24
Histone acetylation in signal transduction by growth regulatory signals
Magnaghi-Jaulin, L., Ait‐Si‐Ali, S., & Harel‐Bellan, A. (1999) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.1999.0301 · Cited by 22
Eukaryotic DNA Methylase — Properties and Action on Native DNA and Chromatin
Adams, R. L. P., Davis, T., Fulton, J., Kirk, D., Qureshi, M., & Burdon, R. H. (1984) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-69370-0_10 · Cited by 16
Research works printed but not linked: 3
- Suderman, 2012, Epigenetic response to childhood abuse in the human hippocampus
- Suderman, Proceedings of the National Academy of Sciences of the United States of America
- Weaver, 2012, MBD2 mediates epigenetic programming of the glucocorticoid receptor
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Garner, A., Yogman, M., COMMITTEE ON PSYCHOSOCIAL ASPECTS OF CHILD AND FAMILY HEALTH, Lavin, A., Askew, G. L., Baum, R. A., Berger-Jenkins, E., Johnson, T. J., Jutte, D., Nasir, A. A., et al. (2021) · Pediatrics · doi:10.1542/peds.2021-052582 · Cited by 392
Dunn, E. C., Soare, T. W., Zhu, Y., Simpkin, A. J., Suderman, M. J., Klengel, T., Smith, A. D. A. C., Ressler, K. J., & Relton, C. L. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.12.023 · Cited by 315
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Ho, S., Johnson, A. D., Tarapore, P., Janakiram, V., Zhang, X., & Leung, Y. (2012) · ILAR Journal · doi:10.1093/ilar.53.3-4.289 · Cited by 327
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Metadata
- Authors
- Szyf, M., & Bick, J.
- Affiliations
- McGill University
- Yale University (US)
- ORCID
- Bick, Johanna
- Venue
- Child Development
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-01-01
- Volume
- 84
- Issue
- 1
- Pages
- 49-57
- ISSN
- 0009-3920 (ISSN-L)
- 1467-8624
- PMC
- PMC4039199
- OpenAlex
- W2115460495
- Cited by
- 251
- References
- 60
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 21 · 2023: 11 · 2022: 23 · 2021: 23 · 2020: 19 · 2019: 17 · 2018: 25 · 2017: 23 · 2016: 23 · 2015: 24 · 2014: 25 · 2013: 6
- FWCI
- 1.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Child Development (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Canadian Institutes of Health Research
- National Institute of Mental Health (T32MH018268)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Keywords
- DNA methylation, epigenetics, early life experience, genome adaptation, gene expression regulation, developmental origins of health and disease, resilience, central and peripheral nervous system
- MeSH terms
- Adaptation, Physiological, Humans, Life Change Events, Phenotype, Stress, Psychological, Signal Transduction, Genome, Human, DNA Methylation, Epigenesis, Genetic
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