DNA methylation, early life environment, and health outcomes
Open accessAbstract
Epigenetics, and especially DNA methylation, have recently become provocative biological explanations for early-life environmental effects on later health. Despite the large increase in papers on the topic over the last few years, many questions remain with regards to the biological feasibility of this mechanism and the strength of the evidence to date. In this review, we examine the literature on early-life effects on epigenetic patterns, with special emphasis on social environmental influences. First, we review the basic biology of epigenetic modification of DNA and debate the role of early-life stressful, protective, and positive environments on gene-specific, system-specific, and whole-genome epigenetic patterns later in life. Second, we compare the epigenetic literatures of both humans and other animals and review the research linking epigenetic patterns to health in order to complete the mechanistic pathway. Third, we discuss physical environmental and social environmental effects, which have to date, generally not been jointly considered. Finally, we close with a discussion of the current state of the area's research, its future direction, and its potential use in pediatric health.
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NR3C1 is the most studied gene to date related to abuse and neglect.
“Notwithstanding, NR3C1 has been linked to prenatal stress [140] and is the most studied gene to date related to abuse and neglect [141].”
From Food Addiction and Psychosocial Adversity: Biological Embedding, Contextual Factors, and Public Health Implications (2020) · cites this paper as [141]
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DNA methylation age of human tissues and cell types
Horvath, S. (2013) · Genome Biology · doi:10.1186/gb-2013-14-10-r115 · Cited by 7,075 · see citing works
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 · see citing works
Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1
Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L. M., Liu, D. R., Aravind, L., et al. (2009) · Science · doi:10.1126/science.1170116 · Cited by 5,836 · see citing works
Human DNA methylomes at base resolution show widespread epigenomic differences
Lister, R., Pelizzola, M., Dowen, R. H., Hawkins, R. D., Hon, G., Tonti-Filippini, J., Nery, J. R., Lee, L., Ye, Z., Ngo, Q.-M., et al. (2009) · Nature · doi:10.1038/nature08514 · Cited by 4,673 · see citing works
CpG-rich islands and the function of DNA methylation
Bird, A. P. (1986) · Nature · doi:10.1038/321209a0 · Cited by 3,777 · see citing works
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 · see citing works
Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine
Ito, S., Shen, L., Dai, Q., Wu, S. C., Collins, L. B., Swenberg, J. A., He, C., & Zhang, Y. (2011) · Science · doi:10.1126/science.1210597 · Cited by 3,451 · see citing works
DNA methylation arrays as surrogate measures of cell mixture distribution
Houseman, E. A., Accomando, W. P., Koestler, D. C., Christensen, B. C., Marsit, C. J., Nelson, H. H., Wiencke, J. K., & Kelsey, K. T. (2012) · BMC Bioinformatics · doi:10.1186/1471-2105-13-86 · Cited by 3,175 · see citing works
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 · see citing works
Tet-Mediated Formation of 5-Carboxylcytosine and Its Excision by TDG in Mammalian DNA
He, Y., Li, B.-Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L., et al. (2011) · Science · doi:10.1126/science.1210944 · Cited by 2,776 · see citing works
The Nuclear DNA Base 5-Hydroxymethylcytosine Is Present in Purkinje Neurons and the Brain
Kriaucionis, S., & Heintz, N. (2009) · Science · doi:10.1126/science.1169786 · Cited by 2,700 · see citing works
Ito, S., D’Alessio, A. C., Taranova, O., Hong, K., Sowers, L. C., & Zhang, Y. (2010) · Nature · doi:10.1038/nature09303 · Cited by 2,542 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Carone, B. R., Fauquier, L., Habib, N., Shea, J. M., Hart, C. E., Li, R., Bock, C., Li, C., Gu, H., Zamore, P. D., et al. (2010) · Cell · doi:10.1016/j.cell.2010.12.008 · Cited by 1,157 · see citing works
Sex-specific, male-line transgenerational responses in humans
The ALSPAC Study Team, Pembrey, M. E., Bygren, L. O., Kaati, G., Edvinsson, S., Northstone, K., Sjöström, M., & Golding, J. (2006) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201538 · Cited by 1,150 · see citing works
Epigenetic transmission of the impact of early stress across generations
Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., Vizi, S., & Mansuy, I. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.036 · Cited by 1,125 · cited 2× · see citing works
“As a specific example, mice that were exposed to chronic and unpredictable maternal separation from postnatal day 1 to 14 were differentially methylated in several candidate genes, including: MeCP2, CB1, and CRFR2 (44).”
BackgroundReversing DNA Methylation: Mechanisms, Genomics, and Biological Functions
Wu, H., & Zhang, Y. (2014) · Cell · doi:10.1016/j.cell.2013.12.019 · Cited by 1,065 · see citing works
Heim, C., & Binder, E. B. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2011.10.032 · Cited by 986 · see citing works
The Biological Effects of Childhood Trauma
De Bellis, M. D., & Zisk, A. (2014) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2014.01.002 · Cited by 892 · see citing works
Miller, G. E., Chen, E., Fok, A. K., Walker, H., Lim, A., Nicholls, E. F., Cole, S., & Kobor, M. S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902971106 · Cited by 822 · see citing works
Turecki, G., & Meaney, M. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.11.022 · Cited by 796 · see citing works
CpG methylation, chromatin structure and gene silencing—a three‐way connection
Razin, A. (1998) · The EMBO Journal · doi:10.1093/emboj/17.17.4905 · Cited by 791 · see citing works
Neuronal activity modifies the DNA methylation landscape in the adult brain
Guo, J. U., Ma, D. K., Mo, H., Ball, M. P., Jang, M.-H., Bonaguidi, M. A., Balazer, J. A., Eaves, H. L., Xie, B., Ford, E., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2900 · Cited by 669 · see citing works
Prenatal environmental exposures, epigenetics, and disease
Perera, F. P., & Herbstman, J. B. (2011) · Reproductive Toxicology · doi:10.1016/j.reprotox.2010.12.055 · Cited by 642 · see citing works
Epigenetic mechanisms that underpin metabolic and cardiovascular diseases
Gluckman, P. D., Hanson, M. A., Buklijas, T., Low, F. M., & Beedle, A. S. (2009) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2009.102 · Cited by 627 · see citing works
Genome-scale analysis of aberrant DNA methylation in colorectal cancerPreprint
Hinoue, T., Weisenberger, D. J., Lange, C., Shen, H., Byun, H., Van, D., Malik, S., Pan, F., Noushmehr, H., van, C., et al. (2011) · Genome Research · doi:10.1101/gr.117523.110 · Cited by 604 · see citing works
Genome-scale analysis of DNA methylation in lung adenocarcinoma and integration with mRNA expressionPreprint
Selamat, S. A., Chung, B. S. I., Girard, L., Zhang, W., Zhang, Y., Campan, M., Siegmund, K. D., Koss, M. N., Hagen, J. A., Lam, W. L., et al. (2012) · Genome Research · doi:10.1101/gr.132662.111 · Cited by 524 · see citing works
Perroud, N., Paoloni-Giacobino, A., Prada, P., Olié, E., Salzmann, A., Nicastro, R., Guillaume, S., Mouthon, D., Stouder, C., Dieben, K., et al. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.60 · Cited by 516 · see citing works
DNMT1-interacting RNAs block gene-specific DNA methylation
Ruscio, A. D., Ebralidze, A. K., Benoukraf, T., Amabile, G., Goff, L. A., Terragni, J., Figueroa, M. E., de Figueiredo‐Pontes, L. L., Alberich-Jordà, M., Zhang, P., et al. (2013) · Nature · doi:10.1038/nature12598 · Cited by 508 · see citing works
Schmitz, K., Mayer, C., Postepska, A., & Grummt, I. (2010) · Genes & Development · doi:10.1101/gad.590910 · Cited by 505 · see citing works
Kundakovic, M., Gudsnuk, K., Franks, B., Madrid, J., Miller, R. L., Perera, F. P., & Champagne, F. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214056110 · Cited by 490 · see citing works
DNA methylation and memory formation
Day, J. J., & Sweatt, J. D. (2010) · Nature Neuroscience · doi:10.1038/nn.2666 · Cited by 488 · see citing works
5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells
Stroud, H., Feng, S., Kinney, S. R. M., Pradhan, S., & Jacobsen, S. E. (2011) · Genome biology · doi:10.1186/gb-2011-12-6-r54 · Cited by 466 · see citing works
Essex, M. J., Thomas Boyce, W., Hertzman, C., Lam, L. L., Armstrong, J. M., Neumann, S. M. A., & Kobor, M. S. (2013) · Child Development · doi:10.1111/j.1467-8624.2011.01641.x · Cited by 462 · see citing works
Monk, C. E., Spicer, J., & Champagne, F. A. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000764 · Cited by 458 · see citing works
Adverse Health Outcomes in Women Exposed In Utero to Diethylstilbestrol
Hoover, R. N., Hyer, M., Pfeiffer, R. M., Adam, E., Bond, B., Cheville, A. L., Colton, T., Hartge, P. A., Hatch, E. E., Herbst, A. L., et al. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1013961 · Cited by 445 · see citing works
Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice
Elliott, E., Ezra-Nevo, G., Regev, L., Neufeld-Cohen, A., & Chen, A. (2010) · Nature Neuroscience · doi:10.1038/nn.2642 · Cited by 436 · see citing works
Perera, F. P., Tang, W., Herbstman, J., Tang, D. L., Levin, L. S., Miller, R. L., & Ho, S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004488 · Cited by 393 · see citing works
Recommendations for the design and analysis of epigenome-wide association studies
Michels, K. B., Binder, A. M., Dedeurwaerder, S., Epstein, C. B., Greally, J. M., Gut, I., Houseman, E. A., Izzi, B., Kelsey, K. T., Meissner, A., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2632 · Cited by 378 · see citing works
Maternal Ethanol Consumption Alters the Epigenotype and the Phenotype of Offspring in a Mouse Model
Kaminen‐Ahola, N., Ahola, A., Maga, A. M., Mallitt, K., Fahey, P. P., Cox, T. C., Whitelaw, E., & Chong, S. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000811 · Cited by 335 · see citing works
Hypospadias in sons of women exposed to diethylstilbestrol in utero: a cohort study
Klip, H., Verloop, J., van Gool, J. D., Koster, M. E., Burger, C. W., & van Leeuwen, F. E. (2002) · The Lancet · doi:10.1016/s0140-6736(02)08152-7 · Cited by 327 · see citing works
Weder, N., Zhang, H., Jensen, K., Yang, B. Z., Simen, A., Jackowski, A., Lipschitz, D., Douglas-Palumberi, H., Ge, M., Perepletchikova, F., et al. (2014) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2013.12.025 · Cited by 324 · see citing works
Hedges, D. J., & Deininger, P. L. (2006) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2006.11.021 · Cited by 310 · see citing works
The role of DNA methylation in stress-related psychiatric disorders
Klengel, T., Pape, J., Binder, E. B., & Mehta, D. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.01.013 · Cited by 309 · see citing works
Associations Between Early Life Stress and Gene Methylation in Children
Romens, S. E., McDonald, J., Svaren, J., & Pollak, S. D. (2015) · Child Development · doi:10.1111/cdev.12270 · Cited by 299 · see citing works
Integrating 5-Hydroxymethylcytosine into the Epigenomic Landscape of Human Embryonic Stem Cells
Szulwach, K. E., Li, X., Li, Y., Song, C., Han, J. W., Kim, S., Namburi, S., Hermetz, K. E., Kim, J. J., Rudd, M. K., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002154 · Cited by 288 · see citing works
DNA Methylation Biomarkers: Cancer and Beyond
Mikeska, T., & Craig, J. M. (2014) · Genes · doi:10.3390/genes5030821 · Cited by 287 · see citing works
Influence of Prenatal Lead Exposure on Genomic Methylation of Cord Blood DNA
Pilsner, J. R., Hu, H., Ettinger, A., Sánchez, B. N., Wright, R. O., Cantonwine, D., Lazarus, A., Lamadrid-Figueroa, H., Mercado-García, A., Téllez-Rojo, M. M., et al. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.0800497 · Cited by 275 · see citing works
Epigenetic influence of social experiences across the lifespan
Champagne, F. A. (2010) · Developmental Psychobiology · doi:10.1002/dev.20436 · Cited by 273 · see citing works
DNA methylation and microRNA dysregulation in cancer
Suzuki, H., Maruyama, R., Yamamoto, E., & Kai, M. (2012) · Molecular Oncology · doi:10.1016/j.molonc.2012.07.007 · Cited by 272 · see citing works
Maternal Care and DNA Methylation of a Glutamic Acid Decarboxylase 1 Promoter in Rat Hippocampus
Zhang, T., Hellstrom, I. C., Bagot, R. C., Wen, X., Diorio, J. C., & Meaney, M. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1039-10.2010 · Cited by 269 · see citing works
Advances in the profiling of DNA modifications: cytosine methylation and beyond
Plongthongkum, N., Diep, D. H., & Zhang, K. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3772 · Cited by 259 · see citing works
Child abuse and epigenetic mechanisms of disease risk
Yang, B.-Z., Zhang, H., Ge, W., Weder, N., Douglas-Palumberi, H., Perepletchikova, F., Gelernter, J., & Kaufman, J. (2013) · American Journal of Preventive Medicine · doi:10.1016/j.amepre.2012.10.012 · Cited by 256 · see citing works
The effects of early life stress on the epigenome: From the womb to adulthood and even before
Provençal, N., & Binder, E. B. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2014.09.001 · Cited by 255 · see citing works
Genomic imprinting: employing and avoiding epigenetic processesPreprint
Bartolomei, M. S. (2009) · Genes & Development · doi:10.1101/gad.1841409 · Cited by 251 · see citing works
Hoyo, C., Murtha, A. P., Schildkraut, J. M., Jirtle, R. L., Demark‐Wahnefried, W., Forman, M. R., Iversen, E. S., Kurtzberg, J., Overcash, F. M., Huang, Z., et al. (2011) · Epigenetics · doi:10.4161/epi.6.7.16263 · Cited by 241 · see citing works
Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function
Anacker, C., O'Donnell, K. J., & Meaney, M. J. (2014) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2014.16.3/canacker · Cited by 237 · cited 2× · see citing works
“Among the early life social predictors for methylation profiles, child abuse and neglect have received the largest attention in relation to epigenetic patterns (17,54).”
BackgroundDNA methylation and childhood maltreatment: From animal models to human studies
Lutz, P.-E., & Turecki, G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.069 · Cited by 236 · see citing works
Epigenetics of stress adaptations in the brain
Stankiewicz, A. M., Swiergiel, A. H., & Lisowski, P. (2013) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2013.07.003 · Cited by 220 · see citing works
Toyokawa, S., Uddin, M., Koenen, K. C., & Galea, S. (2011) · Social Science & Medicine · doi:10.1016/j.socscimed.2011.09.036 · Cited by 219 · see citing works
BDNF promoter methylation and suicidal behavior in depressive patients
Kang, H.-J., Kim, J.-M., Lee, J.-Y., Kim, S.-Y., Bae, K.-Y., Kim, S.-W., Shin, I.-S., Kim, H.-R., Shin, M.-G., & Yoon, J.-S. (2013) · Journal of Affective Disorders · doi:10.1016/j.jad.2013.08.001 · Cited by 218 · see citing works
Epigenetics and the regulation of stress vulnerability and resilience
Zannas, A. S., & West, A. E. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.003 · Cited by 211 · see citing works
Influence of Early Stress on Social Abilities and Serotonergic Functions across Generations in Mice
Franklin, T. B., Linder, N., Russig, H., Thöny, B., & Mansuy, I. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021842 · Cited by 207 · see citing works
Ouellet-Morin, I., Wong, C. C. Y., Danese, A., Pariante, C. M., Papadopoulos, A. S., Mill, J., & Arseneault, L. (2013) · Psychological Medicine · doi:10.1017/s0033291712002784 · Cited by 207 · see citing works
Cecil, C. A. M., Lysenko, L., Jaffee, S. R., Pingault, J., Smith, R. G., Relton, C. L., Woodward, G., McArdle, W. L., Mill, J. S., & Barker, E. D. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.95 · Cited by 187 · see citing works
Li, X., Wei, W., Zhao, Q., Widagdo, J., Baker‐Andresen, D., Flavell, C. R., D’Alessio, A. C., Zhang, Y., & Bredy, T. W. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318906111 · Cited by 187 · see citing works
Scrutinizing the epigenetics revolution
Meloni, M., & Testa, G. (2014) · BioSocieties · doi:10.1057/biosoc.2014.22 · Cited by 185 · see citing works
Epigenetic Influence of Stress and the Social Environment
Gudsnuk, K. M., & Champagne, F. A. (2012) · ILAR Journal · doi:10.1093/ilar.53.3-4.279 · Cited by 185 · see citing works
Epigenetic marking of sperm by post-translational modification of histones and protamines
Brunner, A. M., Nanni, P., & Mansuy, I. M. (2014) · Epigenetics & Chromatin · doi:10.1186/1756-8935-7-2 · Cited by 181 · see citing works
Guo, L., Choufani, S., Ferreira, J. C., Smith, A. C., Chitayat, D. A., Shuman, C. T., Uxa, R., Keating, S. J., Kingdom, J. C., & Weksberg, R. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.04.025 · Cited by 164 · see citing works
Epigenetic Signaling in Psychiatric Disorders
Peña, C. J., Bagot, R. C., Labonté, B., & Nestler, E. J. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.03.016 · Cited by 163 · see citing works
Influence of Prenatal Arsenic Exposure and Newborn Sex on Global Methylation of Cord Blood DNA
Pilsner, J. R., Hall, M. N., Liu, X., Ilievski, V., Slavkovich, V. N., Levy, D., Factor-Litvak, P. R., Yunus, M., Rahman, M., Graziano, J. H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037147 · Cited by 160 · see citing works
Paternal Influences on Offspring Development: Behavioural and Epigenetic Pathways
Braun, K., & Champagne, F. A. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12174 · Cited by 157 · see citing works
Hypospadias: a transgenerational effect of diethylstilbestrol?
Brouwers, M. M., Feitz, W. F. J., Roelofs, L. A. J., Kiemeney, L. A. L. M., de Gier, R. P. E., & Roeleveld, N. (2005) · Human Reproduction · doi:10.1093/humrep/dei398 · Cited by 150 · see citing works
Early life adversity, genomic plasticity, and psychopathology
Turecki, G., Ota, V., Belangero, S. I., Jackowski, A. P., & Kaufman, J. (2014) · The Lancet Psychiatry · doi:10.1016/s2215-0366(14)00022-4 · Cited by 149 · see citing works
Epigenetic inheritance: histone bookmarks across generations
Campos, E. I., Stafford, J. M., & Reinberg, D. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.08.004 · Cited by 145 · see citing works
Waters, C. S., Hay, D. F., Simmonds, J. R., & van Goozen, S. H. M. (2014) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-014-0582-3 · Cited by 143 · see citing works
DNA Methylation, Behavior and Early Life Adversity
Moshe Szyf, A. (2013) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2013.06.004 · Cited by 142 · see citing works
Epigenetic memory of environmental organisms: A reflection of lifetime stressor exposures
Mirbahai, L., & Chipman, J. K. (2013) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2013.10.003 · Cited by 138 · see citing works
Epigenetics and depression: return of the repressed
Dalton, V. S., Kolshus, E., & McLoughlin, D. M. (2013) · Journal of Affective Disorders · doi:10.1016/j.jad.2013.10.028 · Cited by 134 · see citing works
Epigenetic mechanisms underlying learning and the inheritance of learned behaviors
Dias, B. G., Maddox, S. A., Klengel, T., & Ressler, K. J. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2014.12.003 · Cited by 125 · see citing works
Okada, S., Morinobu, S., Fuchikami, M., Segawa, M., Yokomaku, K., Kataoka, T., Okamoto, Y., Yamawaki, S., Inoue, T., Kusumi, I., et al. (2014) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2014.02.002 · Cited by 125 · see citing works
Parenting and Beyond: Common Neurocircuits Underlying Parental and Altruistic Caregiving
Swain, J. E., Konrath, S., Brown, S. L., Finegood, E. D., Akce, L., Dayton, C. J., & Ho, S.-H. S. (2012) · Parenting · doi:10.1080/15295192.2012.680409 · Cited by 117 · see citing works
Griffiths, B. B., & Hunter, R. G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.041 · Cited by 111 · see citing works
Titus-Ernstoff, L. T., Troisi, R. J., Hatch, E. E., Wise, L. A., Palmer, J. R., Hyer, M., Kaufman, R. H., Adam, E., Strohsnitter, W. C., Noller, K. L., et al. (2006) · International Journal of Epidemiology · doi:10.1093/ije/dyl106 · Cited by 101 · see citing works
Branchi, I., Karpova, N. N., D’Andrea, I., Castrén, E., & Alleva, E. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.03.038 · Cited by 87 · see citing works
Social environmental effects on gene regulation
Tung, J., & Gilad, Y. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1357-6 · Cited by 81 · see citing works
Epigenetic Effects of Early Developmental Experiences
Gudsnuk, K. M., & Champagne, F. A. (2011) · Clinics in Perinatology · doi:10.1016/j.clp.2011.08.005 · Cited by 80 · see citing works
Interplay Between Social Experiences and the Genome: Epigenetic Consequences for Behavior
Champagne, F. A. (2012) · Advances in genetics · doi:10.1016/b978-0-12-387687-4.00002-7 · Cited by 72 · see citing works
Altobelli, G., Bogdarina, I. G., Stupka, E., Clark, A., & Langley‐Evans, S. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082989 · Cited by 68 · see citing works
Commentary: The epidemiology of epigenetics: Figure 1
Haig, D. (2011) · International Journal of Epidemiology · doi:10.1093/ije/dyr183 · Cited by 66 · see citing works
Ignácio, Z. M., Réus, G. Z., Abelaira, H. M., & Quevedo, J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.036 · Cited by 65 · see citing works
The neurobiological effects of stress as contributors to psychiatric disorders: focus on epigenetics
Provencal, N., & Binder, E. B. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.08.007 · Cited by 64 · see citing works
Early environments, glucocorticoid receptors, and behavioral epigenetics.
Champagne, F. A. (2013) · Behavioral Neuroscience · doi:10.1037/a0034186 · Cited by 64 · see citing works
Epigenetic mechanisms in mood disorders: Targeting neuroplasticity
Fass, D. M., Schroeder, F. A., Perlis, R. H., & Haggarty, S. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.01.041 · Cited by 62 · see citing works
Field, S. F., Beraldi, D., Bachman, M., Stewart, S. K., Beck, S., & Balasubramanian, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0118202 · Cited by 55 · see citing works
Role of epigenetic factors in the development of mental illness throughout life
Guintivano, J., & Kaminsky, Z. A. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.08.003 · Cited by 54 · see citing works
Early-life stress interactions with the epigenome
Lewis, C. R., & Olive, M. F. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000057 · Cited by 51 · see citing works
The secret language of destiny: stress imprinting and transgenerational origins of disease
Zucchi, F. C. R., Yao, Y., & Metz, G. A. S. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00096 · Cited by 48 · see citing works
Social isolation-induced epigenetic changes in midbrain of adult mice.
Siuda, D., Wu, Z., Chen, Y., Guo, L., Linke, M., Zechner, U., Xia, N., Reifenberg, G., Kleinert, H., Förstermann, U., et al. (2014) · PubMed · Cited by 48 · see citing works
Polycomb Binding Precedes Early-Life Stress Responsive DNA Methylation at the Avp Enhancer
Murgatroyd, C., & Spengler, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090277 · Cited by 44 · see citing works
Epigenetics for anthropologists: An introduction to methods
Non, A. L., & Thayer, Z. M. (2015) · American Journal of Human Biology · doi:10.1002/ajhb.22679 · Cited by 39 · see citing works
Epigenetic and Neurodevelopmental Perspectives on Variation in Parenting Behavior
Peña, C. J., & Champagne, F. A. (2012) · Parenting · doi:10.1080/15295192.2012.683358 · Cited by 29 · see citing works
Assaying the epigenome in limited numbers of cells
Greenleaf, W. J. (2014) · Methods · doi:10.1016/j.ymeth.2014.10.010 · Cited by 16 · see citing works
Kundaković, M. (2013) · Journal of Medical Biochemistry · doi:10.2478/jomb-2013-0047 · Cited by 11 · see citing works
Epigenetic changes brought about by perinatal stressors: A brief review of the literature
Billack, B., Serio, R. N., Silva, I., & Kinsley, C. H. (2012) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/j.vascn.2012.08.169 · Cited by 10 · see citing works
Current Approaches to Epigenetic Therapy for the Treatment of Mantle Cell Lymphoma
Ghai, V., Sharma, K., Abbi, K. K. S., et al. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-6176-0_11 · Cited by 8 · see citing works
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Yeshurun, S., & Hannan, A. J. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0039-z · Cited by 121 · see citing works
Pohl, T. T., Young, L. J., & Bosch, O. J. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2017.12.011 · Cited by 83 · see citing works
Wiss, D. A., Avena, N., & Gold, M. (2020) · Nutrients · doi:10.3390/nu12113521 · Cited by 66 · see citing works
- Authors
- Mitchell, C., Schneper, L. M., & Notterman, D. A.
- Affiliations
- University of Michigan (US)
- Princeton University (US)
- Venue
- Pediatric Research
- Published
- 2015-10-14
- Volume
- 79
- Issue
- 1-2
- Pages
- 212-219
- ISSN
- 0031-3998 (ISSN-L)
- 1530-0447
- PMC
- PMC4798238
- OpenAlex
- W2270848678
- Cited by
- 146
- References
- 109
- Citations by year
- 2026: 12 · 2025: 21 · 2024: 15 · 2023: 11 · 2022: 12 · 2021: 20 · 2020: 17 · 2019: 10 · 2018: 15 · 2017: 9 · 2016: 4
- FWCI
- 0.90
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Pediatric Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Child Health and Human Development
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD076592, P2CHD047879, P2CHD041028)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Keywords
- DNA methylation, epigenetics, early life environment, early life stress, social environment, physical environment, health outcomes, gene-environment interaction, child health, developmental origins of health and disease
- MeSH terms
- Child Health, Child, Humans, Infant, Social Environment, DNA Methylation, Epigenesis, Genetic
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