DNA methylation and childhood maltreatment: From animal models to human studies

Lutz, P.-E.; Turecki, G.

doi:10.1016/j.neuroscience.2013.07.069

Cited by 236Child Abuse and TraumaEpigenetics and DNA MethylationChild Welfare and Adoption

DNA methylation and childhood maltreatment: From animal models to human studies

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Lutz, P.-E., Turecki, G.·2014·Neuroscience

DOI 10.1016/j.neuroscience.2013.07.069PMC PMC5293537

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Abstract

Childhood maltreatment (CM) has estimated prevalence among Western societies between 10% and 15%. As CM associates with increased risk of several psychiatric disorders, early age of illness onset, increased comorbidity and negative clinical outcome, it imposes a major public health, social and economic impact. Although the clinical consequences of CM are well characterized, a major challenge remains to understand how negative early-life events can affect brain function over extended periods of time. We review here both animal and human studies indicating that the epigenetic mechanism of DNA methylation is a crucial mediator of early-life experiences, thereby maintaining life-long neurobiological sequelae of CM, and strongly determining psychopathological risk.

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Both DNA methylation and demethylation mechanisms are likely recruited during early life unfavorable experiences.
“Both DNA methylation and demethylation mechanisms are likely recruited during early life unfavorable experiences [136].”
From Food Addiction and Psychosocial Adversity: Biological Embedding, Contextual Factors, and Public Health Implications (2020) · cites this paper as [136]

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Developmental antecedents of partner abuse: A prospective-longitudinal study.
Magdol, L., Moffitt, T. E., Caspi, A., & Silva, P. A. (1998) · Journal of Abnormal Psychology · doi:10.1037//0021-843x.107.3.375 · Cited by 387 · see citing works
Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function
Zhao, X., Ueba, T., Christie, B. R., Barkho, B. Z., McConnell, M. J., Nakashima, K., Lein, E. S., Eadie, B. D., Willhoite, A. R., Muotri, A. R., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1131928100 · Cited by 376 · see citing works
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., & Moshe Szyf, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002085 · Cited by 372 · see citing works
Methylation-Dependent and -Independent Genomic Targeting Principles of the MBD Protein Family
Baubec, T., Ivánek, R., Lienert, F., & Schübeler, D. (2013) · Cell · doi:10.1016/j.cell.2013.03.011 · Cited by 365 · see citing works
Differential immune system DNA methylation and cytokine regulation in post-traumatic stress disorder
Smith, A. K., Conneely, K. N., Kilaru, V., Mercer, K. B., Weiss, T. E., Bradley, B., Tang, Y., Gillespie, C. F., Cubells, J. F., & Ressler, K. J. (2011) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.31212 · Cited by 355 · see citing works
Paternal Transmission of Stress-Induced Pathologies
Dietz, D. M., LaPlant, Q., Watts, E. L., Hodes, G. E., Russo, S. J., Feng, J., Oosting, R. S., Vialou, V., & Nestler, E. J. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.005 · Cited by 346 · see citing works
MeCP2 binds to 5hmc enriched within active genes and accessible chromatin in the nervous system
Mellén, M., Ayata, P., Dewell, S. B., Kriaučionis, S., & Heintz, N. (2013) · Epigenetics & Chromatin · doi:10.1186/1756-8935-6-s1-p52 · Cited by 345 · see citing works
Differential Glucocorticoid Receptor Exon 1B, 1C, and 1H Expression and Methylation in Suicide Completers with a History of Childhood Abuse
Labonte, B., Yerko, V., Gross, J., Mechawar, N., Meaney, M. J., Szyf, M., & Turecki, G. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.01.034 · Cited by 345 · see citing works
Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight
Mulligan, C., D'Errico, N., Stees, J., & Hughes, D. (2012) · Epigenetics · doi:10.4161/epi.21180 · Cited by 342 · see citing works
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 · see citing works
Response to psychotherapy in borderline personality disorder and methylation status of the BDNF gene
Perroud, N., Salzmann, A., Prada, P., Nicastro, R., Hoeppli, M.-E., Furrer, S., Ardu, S., Krejci, I., Karege, F., & Malafosse, A. (2013) · Translational Psychiatry · doi:10.1038/tp.2012.140 · Cited by 320 · see citing works
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 · see citing works
Analysis of DNA Methylation in a Three-Generation Family Reveals Widespread Genetic Influence on Epigenetic Regulation
Gertz, J., Varley, K. E., Reddy, T. E., Bowling, K. M., Pauli, F., Parker, S. L., Kucera, K. S., Willard, H. F., & Myers, R. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002228 · Cited by 304 · see citing works
Experience-Dependent Epigenetic Modifications in the Central Nervous System
Sweatt, J. D. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.09.002 · Cited by 302 · see citing works
The neurodevelopmental origins of suicidal behavior
Turecki, G., Ernst, C., Jollant, F., Labonté, B., & Mechawar, N. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.11.008 · Cited by 299 · cited 1× · see citing works
“Epigenetic processes are now emerging as crucial mediators of such long-term biological embedding of CM (Turecki et al., 2011, Hertzman, 2012).”
Background
Developmental antecedents of partner abuse: A prospective-longitudinal study.
Magdol, L., Moffitt, T. E., Caspi, A., et al. (1998) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.107.3.375 · Cited by 288 · see citing works
The Prediction of Violence and Homicide in Young Men.
Loeber, R., Pardini, D. A., Homish, D. L., Wei, E. H., Crawford, A. M., Farrington, D. P., Stouthamer‐Loeber, M., Creemers, J., Koehler, S. A., & Rosenfeld, R. (2005) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.73.6.1074 · Cited by 286 · see citing works
Interaction of FKBP5, a Stress-Related Gene, with Childhood Trauma Increases the Risk for Attempting Suicide
Roy, A., Gorodetsky, E., Yuan, Q., Goldman, D., & Enoch, M.-A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.236 · Cited by 282 · 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
CHILD MALTREATMENT AND YOUTHFUL PROBLEM BEHAVIOR*
Zingraff, M. T., Leiter, J., MYERS, K. A., & Johnsen, M. (1993) · Criminology · doi:10.1111/j.1745-9125.1993.tb01127.x · Cited by 264 · see citing works
Investigating the influence of maternal cortisol and emotional state during pregnancy on the DNA methylation status of the glucocorticoid receptor gene (NR3C1) promoter region in cord blood
Hompes, T., Izzi, B., Gellens, E., Morreels, M., Fieuws, S., Pexsters, A., Schops, G., Dom, M., Van Bree, R., Freson, K., et al. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.03.009 · Cited by 262 · see citing works
Ordinary Variations in Maternal Caregiving Influence Human Infants' Stress Reactivity
Hane, A. A., & Fox, N. A. (2006) · Psychological Science · doi:10.1111/j.1467-9280.2006.01742.x · Cited by 257 · 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
Maltreatment of boys and the development of disruptive and delinquent behavior
STOUTHAMER–LOEBER, M., LOEBER, R., HOMISH, D. L., & WEI, E. (2001) · Development and Psychopathology · doi:10.1017/s0954579401004102 · Cited by 256 · see citing works
Detection of histone modifications at specific gene loci in single cells in histological sections
Gomez, D., Shankman, L. S., Nguyen, A. T., & Owens, G. K. (2013) · Nature Methods · doi:10.1038/nmeth.2332 · Cited by 253 · see citing works
Differential patterns of whole-genome DNA methylation in institutionalized children and children raised by their biological parents
Naumova, O. Y., Lee, M., Koposov, R. A., Moshe Szyf, A., Dozier, M., & Grigorenko, E. L. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000605 · Cited by 251 · see citing works
Allelic Skewing of DNA Methylation Is Widespread across the Genome
Schalkwyk, L. C., Meaburn, E. L., Smith, R. G., Dempster, E. L., Jeffries, A. R., Davies, M. N., Plomin, R. J., & Mill, J. S. (2010) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2010.01.014 · Cited by 244 · see citing works
Putting the concept of biological embedding in historical perspective
Hertzman, C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202203109 · Cited by 242 · see citing works
Variations in Maternal Care Alter GABAA Receptor Subunit Expression in Brain Regions Associated with Fear
Caldji, C., Diorio, J. C., & Meaney, M. J. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300237 · Cited by 241 · see citing works
Emerging roles of TET proteins and 5-hydroxymethylcytosines in active DNA demethylation and beyond
Guo, J. U., Su, Y., Zhong, C., Ming, G.-L., & Song, H. (2011) · Cell Cycle · doi:10.4161/cc.10.16.17093 · Cited by 235 · see citing works
Moderation of Adult Depression by a Polymorphism in the FKBP5 Gene and Childhood Physical Abuse in the General Population
Appel, K., Schwahn, C., Mahler, J., Schulz, A., Spitzer, C., Fenske, K., Stender, J., Barnow, S., John, U., Teumer, A., et al. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.81 · Cited by 234 · see citing works
Predicting suicide attempts in young adults with histories of childhood abuse
Brezo, J., Paris, J., Vitaro, F., Hébert, M., Tremblay, R. E., & Turecki, G. (2008) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.107.037994 · Cited by 229 · see citing works
Methylation at SLC6A4 is linked to family history of child abuse: An examination of the Iowa Adoptee sample
Beach, S. R. H., Brody, G. H., Todorov, A. A., Gunter, T. D., & Philibert, R. A. (2009) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.31028 · Cited by 229 · see citing works
Activity-dependent phosphorylation of MeCP2 threonine 308 regulates interaction with NCoR
Ebert, D. H., Gabel, H. W., Robinson, N. D., Kastan, N. R., Hu, L. S., Cohen, S., Navarro, A. J., Lyst, M. J., Ekiert, R., Bird, A. P., et al. (2013) · Nature · doi:10.1038/nature12348 · Cited by 227 · see citing works
An AT-hook domain in MeCP2 determines the clinical course of Rett syndrome and related disorders
Baker, S. A., Chen, L., Wilkins, A. D., Yu, P., Lichtarge, O., & Zoghbi, H. Y. (2013) · Cell · doi:10.1016/j.cell.2013.01.038 · Cited by 225 · see citing works
Long-Term Effects of Child Abuse and Neglect on Alcohol Use and Excessive Drinking in Middle Adulthood
Widom, C. S., WHITE, H. R., Czaja, S. J., & Marmorstein, N. R. (2007) · Journal of Studies on Alcohol and Drugs · doi:10.15288/jsad.2007.68.317 · Cited by 224 · see citing works
Is there a specific relationship between childhood sexual and physical abuse and repeated suicidal behavior?
Ystgaard, M., Hestetun, I., Loeb, M. E., & Mehlum, L. I. (2004) · Child Abuse & Neglect · doi:10.1016/j.chiabu.2004.01.009 · Cited by 220 · see citing works
Disturbances in Morning Cortisol Secretion in Association with Maternal Postnatal Depression Predict Subsequent Depressive Symptomatology in Adolescents
Halligan, S. L., Herbert, J., Goodyer, I., & Murray, L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.09.011 · Cited by 217 · see citing works
Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus
Bagot, R. C., van Hasselt, F. N., Champagne, D. L., Meaney, M. J., Krugers, H. J., & Joëls, M. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.03.004 · Cited by 216 · see citing works
Genome-Wide Methylation Changes in the Brains of Suicide Completers
Labonté, B., Suderman, M., Maussion, G., Lopez, J. P., Navarro-Sánchez, L., Yerko, V., Mechawar, N., Szyf, M., Meaney, M. J., & Turecki, G. (2013) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2012.12050627 · Cited by 212 · see citing works
Memory of early maltreatment: neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning
Roth, T. L., & Sullivan, R. M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.01.032 · Cited by 204 · see citing works
Early-life experience decreases drug-induced reinstatement of morphine CPP in adulthood via microglial-specific epigenetic programming of anti-inflammatory IL-10 expression
Schwarz, J. M., Hutchinson, M. R., & Bilbo, S. D. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3297-11.2011 · Cited by 203 · see citing works
Epigenetic Signatures of Autism: Trimethylated H3K4 Landscapes in Prefrontal Neurons
Shulha, H. P. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.151 · Cited by 196 · see citing works
Methylation at 5htt mediates the impact of child sex abuse on women’s antisocial behavior: an examination of the iowa adoptee sample
Beach, S. R. H., Brody, G. H., Todorov, A. A., Gunter, T. D., & Philibert, R. A. (2011) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3181fdd074 · Cited by 195 · see citing works
The Relationship Between Adolescent Physical Abuse and Criminal Offending: Support for an Enduring and Generalized Cycle of Violence
Fagan, A. A. (2005) · Journal of Family Violence · doi:10.1007/s10896-005-6604-7 · Cited by 194 · see citing works
Suicidal phenomena and abuse in adolescents: a review of epidemiological studies
Evans, E., Hawton, K. E., & Rodham, K. (2005) · Child Abuse & Neglect · doi:10.1016/j.chiabu.2004.06.014 · Cited by 189 · see citing works
Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice
Curley, J. P. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.025.2009 · Cited by 184 · see citing works
Maternal separation with early weaning: A novel mouse model of early life neglect
George, E. D., Bordner, K. A., Elwafi, H. M., & Simen, A. A. (2010) · BMC Neuroscience · doi:10.1186/1471-2202-11-123 · Cited by 163 · see citing works
Rearing environment and hypothalamic-pituitary-adrenal regulation in young rhesus monkeys (Macaca mulatta)
Capitanio, J. P., Mendoza, S. P., Mason, W. A., & Maninger, N. (2005) · Developmental Psychobiology · doi:10.1002/dev.20067 · Cited by 153 · see citing works
Dynamic DNA methylation: a prime candidate for genomic metaplasticity and behavioral adaptation
Baker‐Andresen, D., Ratnu, V. S., & Bredy, T. W. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.09.003 · Cited by 151 · see citing works
Epigenetic regulation of BDNF expression according to antidepressant response
Lopez, J. P., Mamdani, F., Labonte, B., Beaulieu, M.-M., Yang, J. P., Berlim, M. T., Ernst, C., & Turecki, G. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.38 · Cited by 146 · see citing works
Variations in postnatal maternal care and the epigenetic regulation of metabotropic glutamate receptor 1 expression and hippocampal function in the rat
Bagot, R. C., Zhang, T.-Y., Wen, X., Nguyen, T. T. T., Nguyen, H.-B., Diorio, J., Wong, T. P., & Meaney, M. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204599109 · Cited by 141 · see citing works
Paternal social enrichment effects on maternal behavior and offspring growth
Rahia Mashoodh, A., Franks, B., Curley, J. P., & Champagne, F. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121083109 · Cited by 140 · see citing works
Maternal separation is associated with strain‐specific responses to stress and epigenetic alterations to Nr3c1, Avp, and Nr4a1 in mouse
Kember, R. L., Dempster, E. L., Lee, T. H. A., Schalkwyk, L. C., Mill, J., & Fernandes, C. (2012) · Brain and Behavior · doi:10.1002/brb3.69 · Cited by 133 · see citing works
Is Domestic Violence Learned? The Contribution of Five Forms of Child Maltreatment to Men's Violence and Adjustment
Bevan, E., & Higgins, D. J. (2002) · Journal of Family Violence · doi:10.1023/a:1016053228021 · Cited by 130 · see citing works
Effects of Genotype and Child Abuse on DNA Methylation and Gene Expression at the Serotonin Transporter
Vijayendran, M., Beach, S. R. H., Plume, J. M., Brody, G. H., & Philibert, R. A. (2012) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2012.00055 · Cited by 126 · see citing works
Genetic–epigenetic interaction modulates µ-opioid receptor regulation
Oertel, B. G., Doehring, A., Roskam, B., Kettner, M., Hackmann, N., Ferreirós, N., Schmidt, P. H., & Lötsch, J. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds314 · Cited by 124 · see citing works
Brain-Penetrant LSD1 Inhibitors Can Block Memory Consolidation
Neelamegam, R., Ricq, E. L., Malvaez, M., Patnaik, D., Norton, S., Carlin, S. M., Hill, I. T., Wood, M. A., Haggarty, S. J., & Hooker, J. M. (2011) · ACS Chemical Neuroscience · doi:10.1021/cn200104y · Cited by 122 · see citing works
Instruments for the Assessment of Childhood Trauma in Adults
Roy, C. A., & Perry, J. C. (2004) · The Journal of Nervous and Mental Disease · doi:10.1097/01.nmd.0000126701.23121.fa · Cited by 122 · see citing works
Genetic and epigenetic variation of the glucocorticoid receptor (NR3C1) in placenta and infant neurobehavior
Bromer, C., Marsit, C. J., Armstrong, D. A., Padbury, J. F., & Lester, B. M. (2012) · Developmental Psychobiology · doi:10.1002/dev.21061 · Cited by 116 · see citing works
Predicting Child Abuse Potential: An Empirical Investigation of Two Theoretical Frameworks
Begle, A. M., Dumas, J. E., & Hanson, R. F. (2010) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374410903532650 · Cited by 114 · see citing works
Risk and Resilience: Early Manipulation of Macaque Social Experience and Persistent Behavioral and Neurophysiological Outcomes
Stevens, H. E., Leckman, J. F., Coplan, J. D., & Suomi, S. J. (2009) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e318193064c · Cited by 106 · see citing works
Histone Deacetylase Inhibitor MS-275 Exhibits Poor Brain Penetration: Pharmacokinetic Studies of [11C]MS-275 using Positron Emission Tomography
Hooker, J. M., Kim, S. W., Alexoff, D. L., Xu, Y., Shea, C. E., Reid, A. E., Volkow, N. D., & Fowler, J. S. (2009) · ACS Chemical Neuroscience · doi:10.1021/cn9000268 · Cited by 91 · see citing works
The role of emotions in the development and organization of personality.
Malatesta, C. Z. (1988) · PubMed · Cited by 90 · see citing works
Early life socioeconomic factors and genomic DNA methylation in mid-life
Tehranifar, P., Wu, H., Fan, X., Flom, J. D., Ferris, J. S., Cho, Y. H., González, K., Santella, R. M., & Terry, M. B. (2012) · Epigenetics · doi:10.4161/epi.22989 · Cited by 89 · see citing works
The Methyl-CpG Binding Proteins Mecp2, Mbd2 and Kaiso Are Dispensable for Mouse Embryogenesis, but Play a Redundant Function in Neural Differentiation
Caballero, I. M., Hansen, J., Leaford, D., Pollard, S. M., & Hendrich, B. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004315 · Cited by 71 · see citing works
Maternal Care Influences Hippocampal N-Methyl-D-Aspartate Receptor Function and Dynamic Regulation by Corticosterone in Adulthood
Bagot, R. C., Tse, Y. C., Nguyen, H.-B., Wong, A. S., Meaney, M. J., & Wong, T. P. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.03.016 · Cited by 65 · see citing works
Childhood trajectories of anxiousness and disruptiveness explain the association between early-life adversity and attempted suicide
Wanner, B., Vitaro, F., Tremblay, R. E., & Turecki, G. (2012) · Psychological Medicine · doi:10.1017/s0033291712000438 · Cited by 64 · see citing works
DNA memories of early social life
Hoffmann, A. H., & Spengler, D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.003 · Cited by 62 · see citing works
Exposure to neonatal separation stress alters exploratory behavior and corticotropin releasing factor expression in neurons in the amygdala and hippocampus
Becker, K., Abraham, A., Kindler, J., Helmeke, C., & Braun, K. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20372 · Cited by 60 · see citing works
Impact of child sex abuse on adult psychopathology: A genetically and epigenetically informed investigation.
Beach, S. R. H., Brody, G. H., Lei, M., Gibbons, F. X., Gerrard, M., Simons, R. L., Cutrona, C. E., & Philibert, R. A. (2013) · Journal of Family Psychology · doi:10.1037/a0031459 · Cited by 58 · see citing works
Modeling Dad: Animal models of paternal behavior
Kentner, A. C., Abizaid, A. B., & Bielajew, C. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.08.010 · Cited by 57 · see citing works
Interaction between genetic and epigenetic variation defines gene expression patterns at the asthma-associated locus 17q12-q21 in lymphoblastoid cell lines
Berlivet, S., Moussette, S., Ouimet, M., Verlaan, D. J., Koka, V., Tuwaijri, A. A., Kwan, T., Sinnett, D., Pastinen, T., & Naumova, A. K. (2012) · Human Genetics · doi:10.1007/s00439-012-1142-x · Cited by 57 · see citing works
Paternal Deprivation Affects the Development of Corticotrophin‐Releasing Factor‐Expressing Neurones in Prefrontal Cortex, Amygdala and Hippocampus of the BiparentalOctodon degus
Seidel, K., Poeggel, G., Holetschka, R., Helmeke, C., & Braun, K. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02208.x · Cited by 51 · see citing works
Paternal deprivation alters the development of catecholaminergic innervation in the prefrontal cortex and related limbic brain regions
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Paternal Deprivation Alters Region- and Age-Specific Interneuron Expression Patterns in the Biparental Rodent, Octodon degus
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By Hook or by Crook: Multifaceted DNA-Binding Properties of MeCP2
Shin, J., Ming, G., & Song, H. (2013) · Cell · doi:10.1016/j.cell.2013.02.017 · Cited by 14 · see citing works
The Neuroepigenetics of Suicide
Akbarian, S., & Halene, T. B. (2013) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2013.13020235 · Cited by 6 · see citing works

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McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM, Kessler RC. Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication II: associations with persistence of DSM-IV disorders. Archives of general psychiatry. 2010b;67:124–132. doi: 10.1001/archgenpsychiatry.2009.187. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
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Depression, Stress, and Anhedonia: Toward a Synthesis and Integrated Model
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Comprehending the Body in the Era of the Epigenome
Lock, M. M. (2015) · Current Anthropology · doi:10.1086/680350 · Cited by 248 · see citing works
Stress In Utero: Prenatal Programming of Brain Plasticity and Cognition
Bock, J., Wainstock, T., Braun, K., & Segal, M. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.02.036 · Cited by 232 · see citing works
Duration of early adversity and structural brain development in post-institutionalized adolescents
Hodel, A. S., Hunt, R. H., Cowell, R. A., Van Den Heuvel, S. E., Gunnar, M. R., & Thomas, K. M. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.020 · Cited by 220 · see citing works
Association of a history of child abuse with impaired myelination in the anterior cingulate cortex: convergent epigenetic, transcriptional, and morphological evidence
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Authors: Lutz, P.-E., & Turecki, G.
Affiliations: Douglas Mental Health University Institute (CA)
Corresponding author: Turecki, G.
ORCID: Turecki, G.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2014-04
Volume: 264
Pages: 142-156
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2013.07.069
PMC: PMC5293537
OpenAlex: W2014566312
Cited by: 236
References: 155
Citations by year: 2026: 2 · 2025: 5 · 2024: 3 · 2023: 27 · 2022: 10 · 2021: 34 · 2020: 28 · 2019: 12 · 2018: 31 · 2017: 24 · 2016: 24 · 2015: 17 · 2014: 19
FWCI: 2.92
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
HAL (submittedVersion, other-oa)
eScholarship@McGill (McGill) (submittedVersion)
Funders: Canadian Institutes of Health Research (119429_1)
Topics: Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Social Sciences › Safety Research › Child Welfare and Adoption
Keywords: DNA methylation, child abuse, epigenetics, childhood adversity, mental illness, animal models, psychopathological risk, comorbidities, age of onset
MeSH terms: Animals, Mental Disorders, Brain, Child, Child Abuse, Female, Humans, Male, Stress, Psychological, Age of Onset, DNA Methylation, Models, Animal, Epigenesis, Genetic, Mice, Rats

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DNA methylation and childhood maltreatment: From animal models to human studies

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