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DNA methylation and childhood maltreatment: From animal models to human studies
Open accessAbstract
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 [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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“The contribution of DNA methylation has been extensively investigated especially in the context of pathologies related to exposure to stressful life events (especially those occurring early in life, ELS) including depression or post-traumatic stress disorder (73, 95, 98, 100, 101).”
BackgroundEarly 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 159
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BackgroundBarker, E. D., Walton, E., & Cecil, C. A. M. (2018) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12782 · Cited by 134
“Another severe form of adversity, childhood maltreatment (e.g. abuse, neglect), has also been found to associate with DNAm alterations in genes important for stress-response, immune function and neurodevelopment (see Lutz & Turecki, 2014, for a review).”
Brain derived neurotrophic factor: Epigenetic regulation in psychiatric disorders
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“This dynamic regulation is not captured in postmortem samples but blood samples can potentially clarify this phenomenon (Lutz and Turecki, 2014).”
Cowan, C. S. M., Callaghan, B. L., Kan, J. M., & Richardson, R. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12263 · Cited by 130
“Adversity-induced epigenetic regulation has been reviewed in detail elsewhere (e.g. Lutz & Turecki 2014), so for the purposes of this article we will limit our discussion to one potential epigenetic pathway of particular relevance for the specific behavioral effects focused on herein, that being…”
BackgroundTyrka, A. R., Ridout, K. K., & Parade, S. H. (2016) · Development and Psychopathology · doi:10.1017/s0954579416000870 · Cited by 119
“This work is complemented by animal models demonstrating that methylation of NR3C1 is linked with increased anxiety-like behaviors in rodents (Kosten, Huang, & Nielsen, 2014; Lutz & Turecki, 2014; Pan, Fleming, Lawson, Jenkind, & McGowan, 2014).”
MethodAntecedents and sex/gender differences in youth suicidal behavior
Rhodes, A. E. (2014) · World Journal of Psychiatry · doi:10.5498/wjp.v4.i4.120 · Cited by 124
Epigenetic signatures of childhood abuse and neglect: Implications for psychiatric vulnerability
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“Similarly, a small number of human studies have documented a link between childhood maltreatment and aberrant DNAm in genes important for stress-response, immune function and neurodevelopment (Lutz and Turecki, 2014).”
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Tyrka, A. R., Ridout, K. K., Parade, S. H., Paquette, A., Marsit, C. J., & Seifer, R. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000991 · Cited by 118
“Accumulating evidence indicates that childhood maltreatment may exert long-lasting effects through epigenetic changes (Lutz & Turecki, 2014; Szyf, 2011; Tyrka, Parade, Eslinger, et al., 2015).”
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“Studies of humans and non-human mammals are likely to be mutually informative, as epigenetic mechanisms are largely conserved across these species [130, 131].”
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Epigenetics for the social sciences: justice, embodiment, and inheritance in the postgenomic age
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Lutz, P.-E., Gross, J. A., Dhir, S. K., Maussion, G., Yang, J., Bramoulle, A., Meaney, M. J., & Turecki, G. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.07.012 · Cited by 96
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Barnett-Burns, S., Szyszkowicz, J. K., Luheshi, G. N., Lutz, P.-É., & Turecki, G. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.033 · Cited by 97
Exposure to childhood abuse is associated with human sperm DNA methylation
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Maternal adversities during pregnancy and cord blood oxytocin receptor (OXTR) DNA methylation
Unternaehrer, E., Bolten, M., Nast, I., Staehli, S., Meyer, A. H., Dempster, E., Hellhammer, D. H., Lieb, R., & Meinlschmidt, G. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw051 · Cited by 75
“, 2012) and maternal mood and stress experience (Lutz and Turecki, 2014).”
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Schneider, E., Hajj, N. E., Müller, F., Navarro, B., & Haaf, T. (2015) · Cytogenetic and Genome Research · doi:10.1159/000435778 · Cited by 77
“…suggests that adverse, in particular stress-related experiences, can lead to persistent epigenetic changes in the brain that can influence metabolism, behavior, cognition, mood, and neuroendocrine functions [Murgatroyd et al., 2009; Szyf, 2011; Hoffmann and Spengler, 2012; Lutz and Turecki, 2014].”
Early deprivation, atypical brain development, and internalizing symptoms in late childhood
Bick, J. R., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.026 · Cited by 76
“Findings from animal work demonstrate that early adverse rearing conditions are associated with alterations in synaptogenesis, neuronal differentiation, and synaptic pruning, especially in circuitry involved in stress regulation, reward response and motivation (as reviewed in Cirulli et al., 2003; Pryce et al., 2005;…”
BackgroundEsposito, E. A., Jones, M. J., Doom, J. R., MacIsaac, J. L., Gunnar, M. R., & Kobor, M. S. (2016) · Development and Psychopathology · doi:10.1017/s0954579416000055 · Cited by 78
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“…methylation of several other genes, including those that regulate GR function and other components of the biological response to stress (Lutz & Turecki, 2013), and recent work demonstrates moderating influences of some of these genes on NR3C1 methylation in relation to stress exposure…”
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“Epigenetic mechanisms are considered to be the interface between genetically programmed developmental processes in the brain and early environmental influences, including stress and trauma leading to long-term behavioral adaptations [for reviews, see (Bock et al. 2014b; Champagne and Curley 2009; Fagiolini et al. 2009…”
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“induced DNA methylation model than previously described for exon 1-F.(38) In the present study, CpG4 may be a transcriptionally silent methylation site that mediated aberrant epigenetic regulation, as proposed by Lutz et al.”
InfluentialBock, J., Poeschel, J., Schindler, J., Börner, F., Shachar-Dadon, A., Ferdman, N., Gaisler‐Salomon, I., Leshem, M., Braun, K., & Poeggel, G. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0940-4 · Cited by 54
“While the precise epigenetic mechanism is unknown and may vary in a sex- and age-dependent manner, changes in DNA methylation and the expression of small non-coding RNAs (sncRNA) were suggested to underlie the transfer of information across generations (Franklin et al. 2010; Hoffmann and Spengler 2012; Szyf 2013; Lutz…”
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“Methylation of the promoter region of a gene interferes with the binding of transcription factors to the promoter region, thereby inhibiting gene expression (Lutz and Turecki, 2014; Szyf, 2011).”
Epigenomic mediation after adverse childhood experiences: a systematic review and meta-analysis
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“Moreover, the importance of infantile experience and early exposure to stress has long been established in animals [13] and evidence is rapidly growing for the role of epigenetic modifications in both animal and human models of trauma and abuse [14].”
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“This new field, referred to as ‘neuroepigenetics’ (Sweatt, 2013) or ‘neurobehavioral epigenetics, (Lutz and Turecki, 2014), indicates that a myriad of external factors including nutritional status, education and socioeconomic status, exposure to environmental toxins and drugs of abuse, withdrawal…”
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Rincel, M., & Darnaudéry, M. (2019) · Proceedings of The Nutrition Society · doi:10.1017/s0029665119000958 · Cited by 51
Caregiver maltreatment causes altered neuronal DNA methylation in female rodents
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“, 2007), and severity of the clinical course (Lutz and Turecki, 2014; Tomoda et al., 2012).”
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Cecil, C. A. M., Walton, E., Jaffee, S. R., O'Connor, T., Maughan, B., Relton, C. L., Smith, R. G., McArdle, W., Gaunt, T. R., Ouellet-Morin, I., et al. (2018) · Development and Psychopathology · doi:10.1017/s095457941700092x · Cited by 46
“…influences (McGowan & Roth, 2015), including numerous nutritional, chemical, physical, and psychosocial exposures occurring in utero (e.g. Monk, Spicer, & Champagne, 2012; Richmond et al., 2015; Tobi et al., 2014) and postnatally (Lutz & Turecki, 2014; Szyf & Bick, 2013; Tyrka et al., 2015).”
Gene-Environment Interactions and Role of Epigenetics in Anxiety Disorders
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Childhood maltreatment and stress-related psychopathology: the epigenetic memory hypothesis
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Childhood Maltreatment and Headache Disorders
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“Work in humans has largely been restricted to examining genome-wide methylation patterns in peripheral samples (i.e. whole blood, buccal cells) collected from children exposed to stress or abuse (Klengel et al., 2014; Lutz & Turecki, 2014).”
Markers as mediators: A review and synthesis of epigenetics literature
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Transcriptomic and epigenomic biomarkers of antidepressant response
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“[86] DNA methylation and demethylation are likely modified by early-life unfavorable experiences,[83] but yet there is modification that also occurs throughout life.”
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Barnett-Burns, S., Almeida, D. M., & Turecki, G. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.01.008 · Cited by 35
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“Accumulating evidence indicates that CT may exert long-lasting effects through epigenetic changes (Lutz & Turecki 2014; Szyf 2011).”
BackgroundA Slice of the Suicidal Brain: What Have Postmortem Molecular Studies Taught Us?
Almeida, D. M., & Turecki, G. (2016) · Current Psychiatry Reports · doi:10.1007/s11920-016-0736-8 · Cited by 33
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Haller, J. (2018) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2018.00026 · Cited by 33
Keller, S. M., Doherty, T. S., & Roth, T. L. (2019) · Scientific Reports · doi:10.1038/s41598-019-46539-4 · Cited by 29
Quevedo, Y., Booij, L., Herrera, L., Hernández, C., & Jiménez, J. P. (2022) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2022.955005 · Cited by 28
“For instance, in rats, the effect of maternal care behavior like licking, grooming (LG), and back arch-nursing (ABN) on behavior of the offspring and DNA methylation in the glucocorticoid receptor gene (NR3C1) have been reported (Lutz and Turecki, 2014).”
BackgroundThe role of epigenetics in cognitive ageing
Mather, K. A., Kwok, J. B., Armstrong, N. J., & Sachdev, P. S. (2014) · International Journal of Geriatric Psychiatry · doi:10.1002/gps.4183 · Cited by 27
“Epigenetic marks may be influenced by environmental factors such as early-life adversity, diet, smoking, exposure to pollution and exercise (Wu et al., 2008; Alegria-Torres et al., 2011; Chouliaras et al., 2012; Lee and Pausova, 2013; Lovatel et al., 2013; Lutz and Turecki, 2013; Perroud et al., 2014) although our und…”
BackgroundEpigenetics Prematurely Born(e): Social Work and the Malleable Gene
White, S. J., & Wastell, D. G. (2016) · The British Journal of Social Work · doi:10.1093/bjsw/bcw157 · Cited by 23
“Whether such changes may share some relationships, and through which molecular mechanisms, remains fully unknown (Lutz and Turecki, 2014: 151-152) The uncritical enthusiasm for the use of biomarkers, however questionable their accuracy, to make normative judgements about social adversity and…”
BackgroundThe Neuroscience of Suicidal Behavior
van Heeringen, K. (2018) · Cambridge University Press eBooks · doi:10.1017/9781316563205 · Cited by 22
Social Environment and Epigenetics
Merrill, S. M., Gladish, N., & Kobor, M. S. (2019) · Current topics in behavioral neurosciences · doi:10.1007/7854_2019_114 · Cited by 24
Benedetti, F., Ambrée, O., Locatelli, C., Lorenzi, C., Poletti, S., Colombo, C., & Arolt, V. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.07.043 · Cited by 18
“DNA methylation are crucial mediators of the effect of early stress on adult brain function [34].”
BackgroundKeller, S. M., Doherty, T. S., & Roth, T. L. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00126 · Cited by 22
“Caregiver maltreatment is a form of early-life adversity incurred by 10%–15% of the population in the United States (Gilbert et al., 2009; Lutz and Turecki, 2014).”
Backgroundvan Calker, D., & Serchov, T. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.019 · Cited by 19
Meloni, M., & Reynolds, J. (2020) · Synthese · doi:10.1007/s11229-020-02748-3 · Cited by 19
Bearer, E. L., & Mulligan, B. S. (2018) · Current Genomics · doi:10.2174/1389202919666180307150508 · Cited by 19
“…is now being realized for cancer diagnosis and treatment [79, 80], and technology is being developed for that application that can be re-directed for studies of other disorders where epigenetic dynamics are suspected, such as brain development and the impact of early life experience [81].”
Dissociative Amnesia – A Challenge to Therapy
Staniloiu, A., & Markowitsch, H. J. (2018) · International Journal of Psychotherapy Practice and Research · doi:10.14302/issn.2574-612x.ijpr-18-2246 · Cited by 20
“Genetic predispositions and epigenetic constellations may intensify adverse effects, leading, for example, to stress-related clinical conditions.(35-39) Adverse life conditions during childhood have direct consequences on brain development.”
BackgroundAssociations of age, sex, sexual abuse, and genotype with monoamine oxidase a gene methylation
Checknita, D., Tiihonen, J., Hodgins, S., & Nilsson, K. W. (2021) · Journal of Neural Transmission · doi:10.1007/s00702-021-02403-2 · Cited by 14
Álvarez, P., Levine, J. D., & Green, P. G. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.01.066 · Cited by 14
Matas, E., Bock, J., & Braun, K. (2016) · Psychopathology · doi:10.1159/000448055 · Cited by 14
Early Enriched Environment Prevents Epigenetic p11 Gene Changes Induced by Adulthood Stress in Mice
Seo, M. K., Choi, A., Seog, D., Lee, J. G., & Park, S. W. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041928 · Cited by 14
Early life stress induces age-dependent epigenetic changes in p11 gene expression in male mice
Seo, M. K., Lee, J. G., & Park, S. W. (2021) · Scientific Reports · doi:10.1038/s41598-021-89593-7 · Cited by 14
Early Life Stress: Nature and Nurture
Dallman, M. F. (2014) · Endocrinology · doi:10.1210/en.2014-1267 · Cited by 13
“21, 22 and a very interesting opinion piece about interactions between ELS and nutrition on hippocampal epigenetic marks in Ref.”
BackgroundSuicide: Genetics and Heritability
Vaquero‐Lorenzo, C., & Vasquez, M. A. (2020) · Current topics in behavioral neurosciences · doi:10.1007/7854_2020_161 · Cited by 13
Traces cérébrales des traumatismes infantiles et devenir psychopathologique
Moureau, A., & Delvenne, V. (2016) · La psychiatrie de l enfant · doi:10.3917/psye.591.0333 · Cited by 14
Environmental influences on the female epigenome and behavior
Keller, S. M., & Roth, T. L. (2016) · Current Zoology · doi:10.1093/eep/dvw007 · Cited by 12
“Aberrant epigenetic profiles have also been linked to a host of neuropsychiatric disorders [23–26], and epigenetic modifications are increasingly being”
BackgroundFilipe, Â. M., Lloyd, S., & Larivée, A. (2021) · Frontiers in Sociology · doi:10.3389/fsoc.2021.635986 · Cited by 11
Wang, H., Moon, S., Kim, H., Kim, G., Ahn, W., Joo, Y. Y., & Cha, J. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e23345 · Cited by 11
del Re, E. C., Yassin, W., Zeng, V., Keedy, S., Alliey‐Rodriguez, N., Ivleva, E. I., Hill, S., Rychagov, N., McDowell, J. E., Bishop, J. R., et al. (2023) · Schizophrenia Research · doi:10.1016/j.schres.2023.03.029 · Cited by 9
Dissociative amnesia – A valid construct for repressed memories
Markowitsch, H. J., & Staniloiu, A. (2025) · Legal and Criminological Psychology · doi:10.1111/lcrp.12276 · Cited by 7
Tenuta, F., Bartolo, M. G., Diano, D., & Costabile, A. (2020) · MALTRATTAMENTO E ABUSO ALL INFANZIA · doi:10.3280/mal2020-002005 · Cited by 7
Ignácio, Z. M., Réus, G. Z., Quevedo, J., Kalinichev, M., & Francis, D. (2017) · Reference Module in Neuroscience and Biobehavioral Psychology · doi:10.1016/b978-0-12-809324-5.00352-7 · Cited by 7
How stress affects gene expression through epigenetic modifications
Bainomugisa, C. K., & Mehta, D. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-823039-8.00014-9 · Cited by 6
Zhang, Y., Gong, L., Feng, Q., Hu, K., Liu, C., Tian, J., & Zhang, Q. (2024) · BMC Psychiatry · doi:10.1186/s12888-024-05880-3 · Cited by 7
Narayan, E. J., Sawyer, G., Fox, D., Smith, R. S., & Tilbrook, A. J. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.830450 · Cited by 6
Monoamine Oxidase: A Potential Link in Papez Circuit to Generalized Anxiety Disorders
Sharma, R., Kumarasamy, M., Parihar, V. K., Ravichandiran, V., & Kumar, N. (2023) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527322666230412105711 · Cited by 7
West, A. E., & Orlando, V. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.02.001 · Cited by 6
Metadata
- 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)
- 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
- 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 › Sociology and Political Science › 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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