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The early care environment and DNA methylome variation in childhood


Prenatal adversity shapes child neurodevelopment and risk for later mental health problems. The quality of the early care environment can buffer some of the negative effects of prenatal adversity on child development. Retrospective studies, in adult samples, highlight epigenetic modifications as sentinel markers of the quality of the early care environment; however, comparable data from pediatric cohorts are lacking. Participants were drawn from the Maternal Adversity Vulnerability and Neurodevelopment (MAVAN) study, a longitudinal cohort with measures of infant attachment, infant development, and child mental health. Children provided buccal epithelial samples (mean age = 6.99, SD = 1.33 years, n = 226), which were used for analyses of genome-wide DNA methylation and genetic variation. We used a series of linear models to describe the association between infant attachment and (a) measures of child outcome and (b) DNA methylation across the genome. Paired genetic data was used to determine the genetic contribution to DNA methylation at attachment-associated sites. Infant attachment style was associated with infant cognitive development (Mental Development Index) and behavior (Behavior Rating Scale) assessed with the Bayley Scales of Infant Development at 36 months. Infant attachment style moderated the effects of prenatal adversity on Behavior Rating Scale scores at 36 months. Infant attachment was also significantly associated with a principal component that accounted for 11.9% of the variation in genome-wide DNA methylation. These effects were most apparent when comparing children with a secure versus a disorganized attachment style and most pronounced in females. The availability of paired genetic data revealed that DNA methylation at approximately half of all infant attachment-associated sites was best explained by considering both infant attachment and child genetic variation. This study provides further evidence that infant attachment can buffer some of the negative effects of early adversity on measures of infant behavior. We also highlight the interplay between infant attachment and child genotype in shaping variation in DNA methylation. Such findings provide preliminary evidence for a molecular signature of infant attachment and may help inform attachment-focused early intervention programs.

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Address correspondence and reprint requests to: Kieran J. O'Donnell, the Ludmer Centre for Neuroinformatics and Mental Health, Douglas Mental Health University Institute, McGill University, 6875 Lasalle Boulevard, Montreal, Quebec, Canada H4H 1R3; E-mail:
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We are grateful to the participants and to Katherine O'Donnell, Tie Yuan Zhang, and Josie Diorio for helpful discussions. This work was funded by a grant from Brain Canada (Canadian Neuroepigenetics Network), the Ludmer Centre for Neuroinformatics and Mental Health, and the Sackler Program for Epigenetics and Psychobiology. Kieran J. O'Donnell is an Azrieli Canadian Institute For Advanced Research (CIFAR) Global Scholar. Michael J. Meaney, Michael S Kobor, and Marla Sokolowski are Fellows of the CIFAR Child and Brain Development Program.

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Anacker, C., Cattaneo, A., Musaelyan, K., Zunszain, P. A., Horowitz, M., Molteni, R., … Pariante, C. M. (2013). Role for the kinase SGK1 in stress, depression, and glucocorticoid effects on hippocampal neurogenesis. Proceedings of the National Academy of Sciences, 110, 87088713. doi:10.1073/pnas.1300886110
Aryee, M. J., Jaffe, A. E., Corrada-Bravo, H., Ladd-Acosta, C., Feinberg, A. P., Hansen, K. D., & Irizarry, R. A. (2014). Minfi: A flexible and comprehensive bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics, 30, 13631369. doi:10.1093/bioinformatics/btu049
Bagot, R. C., Zhang, T. Y., Wen, X., Nguyen, T. T., Nguyen, H. B., Diorio, J., … Meaney, M. J. (2012). Variations in postnatal maternal care and the epigenetic regulation of metabotropic glutamate receptor 1 expression and hippocampal function in the rat. Proceedings of the National Academy of Sciences, 109(Suppl. 2), 1720017207. doi:10.1073/pnas.1204599109
Bayley, N. (1993). Bayley Scales of Infant Development (2nd ed.). San Antonio, TX: Psychological Corporation.
Belsky, J., & de Haan, M. (2011). Annual Research Review: Parenting and children's brain development: The end of the beginning. Journal of Child Psychology and Psychiatry, 52, 409428. doi:10.1111/j.1469-7610.2010.02281.x
Belsky, J., Pluess, M., & Widaman, K. F. (2013). Confirmatory and competitive evaluation of alternative gene-environment interaction hypotheses. Journal of Child Psychology and Psychiatry, 54, 11351143. doi:10.1111/jcpp.12075
Belsky, J., & van IJzendoorn, M. H. (2017). Genetic differential susceptibility to the effects of parenting. Current Opinion in Psychology, 15, 125130. doi:10.1016/j.copsyc.2017.02.021
Bergman, K., Sarkar, P., Glover, V., & O'Connor, T. G. (2010). Maternal prenatal cortisol and infant cognitive development: Moderation by infant-mother attachment. Biological Psychiatry, 67, 10261032. doi:10.1016/j.biopsych.2010.01.002
Berko, E. R., Suzuki, M., Beren, F., Lemetre, C., Alaimo, C. M., Calder, R. B., … Greally, J. M. (2014). Mosaic epigenetic dysregulation of ectodermal cells in autism spectrum disorder. PLOS Genetics, 10, e1004402. doi:10.1371/journal.pgen.1004402PGENETICS-D-13-02792
Bibikova, M., Barnes, B., Tsan, C., Ho, V., Klotzle, B., Le, J. M., … Shen, R. (2011). High density DNA methylation array with single CpG site resolution. Genomics, 98, 288295. doi:10.1016/j.ygeno.2011.07.007
Champagne, F. A., & Meaney, M. J. (2006). Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biological Psychiatry, 59, 12271235. doi:10.1016/j.biopsych.2005.10.016
Chen, Y. A., Lemire, M., Choufani, S., Butcher, D. T., Grafodatskaya, D., Zanke, B. W., … Weksberg, R. (2013). Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray. Epigenetics, 8, 203209. doi:10.4161/epi.23470
Chisholm, J. S. (1996). The evolutionary ecology of attachment organization. Human Nature, 7, 137. doi:10.1007/BF02733488
Edgar, R. D., Jones, M. J., Meaney, M. J., Turecki, G., & Kobor, M. S. (2017). BECon: A tool for interpreting DNA methylation findings from blood in the context of brain. Translational Psychiatry, 7, e1187. doi:10.1038/tp.2017.171
Ellis, B. J., & Essex, M. J. (2007). Family environments, adrenarche, and sexual maturation: A longitudinal test of a life history model. Child Development, 78, 17991817. doi:10.1111/j.1467-8624.2007.01092.x
Ellis, B. J., Shirtcliff, E. A., Boyce, W. T., Deardorff, J., & Essex, M. J. (2011). Quality of early family relationships and the timing and tempo of puberty: Effects depend on biological sensitivity to context. Development and Psychopathology, 23, 8599. doi:10.1017/S0954579410000660
Fearon, R. P., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Lapsley, A. M., & Roisman, G. I. (2010). The significance of insecure attachment and disorganization in the development of children's externalizing behavior: A meta-analytic study. Child Development, 81, 435456. doi:10.1111/j.1467-8624.2009.01405.x
Forest, M., O'Donnell, K. J., Voisin, G., Gaudreau, H., MacIsaac, J. L., McEwen, L. M., … Greenwood, C. M. T. (2018). Agreement in DNA methylation levels from the Illumina 450K array across batches, tissues, and time. Epigenetics, 13, 1932.
Fortin, J. P., Labbe, A., Lemire, M., Zanke, B. W., Hudson, T. J., Fertig, E. J., … Hansen, K. D. (2014). Functional normalization of 450k methylation array data improves replication in large cancer studies. Genome Biology, 15, 503. doi:10.1186/s13059-014-0503-2
Goodman, R., Ford, T., Simmons, H., Gatward, R., & Meltzer, H. (2000). Using the Strengths and Difficulties Questionnaire (SDQ) to screen for child psychiatric disorders in a community sample. British Journal of Psychiatry, 177, 534539.
Goodman, R., Meltzer, H., & Bailey, V. (1998). The Strengths and Difficulties Questionnaire: A pilot study on the validity of the self-report version. European Child & Adolescent Psychiatry, 7, 125130. doi:10.1007/s007870050057
Goodman, R., Renfrew, D., & Mullick, M. (2000). Predicting type of psychiatric disorder from Strengths and Difficulties Questionnaire (SDQ) scores in child mental health clinics in London and Dhaka. European Child & Adolescent Psychiatry, 9, 129134. doi:10.1007/s007870050008
Groh, A. M., Fearon, R. P., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Steele, R. D., & Roisman, G. I. (2014). The significance of attachment security for children's social competence with peers: A meta-analytic study. Attachment & Human Development, 16, 103136. doi:10.1080/14616734.2014.883636
Groh, A. M., Roisman, G. I., van Ijzendoorn, M. H., Bakermans-Kranenburg, M. J., & Fearon, R. P. (2012). The significance of insecure and disorganized attachment for children's internalizing symptoms: A meta-analytic study. Child Development, 83, 591610. doi:10.1111/j.1467-8624.2011.01711.x
Guintivano, J., Arad, M., Gould, T. D., Payne, J. L., & Kaminsky, Z. A. (2013). Antenatal prediction of postpartum depression with blood DNA methylation biomarkers. Molecular Psychiatry, 19, 560567. doi:10.1038/mp.2013.62
Hannon, E., Spiers, H., Viana, J., Pidsley, R., Burrage, J., Murphy, T. M., … Mill, J. (2016). Methylation QTLs in the developing brain and their enrichment in schizophrenia risk loci. Nature Neuroscience, 19, 4854. doi:10.1038/nn.4182
Hartman, S., Widaman, K. F., & Belsky, J. (2015). Genetic moderation of effects of maternal sensitivity on girl's age of menarche: Replication of the Manuck et al. study. Development and Psychopathology, 27, 747756. doi:10.1017/S0954579414000856
Jaffe, A. E., Gao, Y., Deep-Soboslay, A., Tao, R., Hyde, T. M., Weinberger, D. R., & Kleinman, J. E. (2016). Mapping DNA methylation across development, genotype and schizophrenia in the human frontal cortex. Nature Neuroscience, 19, 4047. doi:10.1038/nn.4181
Johnson, W. E., Li, C., & Rabinovic, A. (2007). Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics, 8, 118127. doi:10.1093/biostatistics/kxj037
Kangaspeska, S., Stride, B., Metivier, R., Polycarpou-Schwarz, M., Ibberson, D., Carmouche, R. P., … Reid, G. (2008). Transient cyclical methylation of promoter DNA. Nature, 452, 112115.
Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J. C., Pariante, C. M., … Binder, E. B. (2013). Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nature Neuroscience, 16, 3341.
Lam, L. L., Emberly, E., Fraser, H. B., Neumann, S. M., Chen, E., Miller, G. E., & Kobor, M. S. (2012). Factors underlying variable DNA methylation in a human community cohort. Proceedings of the National Academy of Sciences, 109(Suppl. 2), 1725317260. doi:10.1073/pnas.1121249109
Lehne, B., Drong, A. W., Loh, M., Zhang, W., Scott, W. R., Tan, S. T., … Chambers, J. C. (2015). A coherent approach for analysis of the Illumina HumanMethylation450 BeadChip improves data quality and performance in epigenome-wide association studies. Genome Biology, 16, 37. doi:10.1186/s13059-015-0600-x
Lowe, R., Gemma, C., Beyan, H., Hawa, M. I., Bazeos, A., Leslie, R. D., … Ramagopalan, S. V. (2013). Buccals are likely to be a more informative surrogate tissue than blood for epigenome-wide association studies. Epigenetics, 8. doi:24362
Manuck, S. B., Craig, A. E., Flory, J. D., Halder, I., & Ferrell, R. E. (2011). Reported early family environment covaries with menarcheal age as a function of polymorphic variation in estrogen receptor-alpha. Development and Psychopathology, 23, 6983. doi:10.1017/S0954579410000659
Marr, A. K., MacIsaac, J. L., Jiang, R., Airo, A. M., Kobor, M. S., & McMaster, W. R. (2014). Leishmania donovani infection causes distinct epigenetic DNA methylation changes in host macrophages. PLOS Pathogens, 10, e1004419. doi:10.1371/journal.ppat.1004419
Maunakea, A. K., Chepelev, I., Cui, K., & Zhao, K. (2013). Intragenic DNA methylation modulates alternative splicing by recruiting MeCP2 to promote exon recognition. Cell Research, 23, 12561269. doi:10.1038/cr.2013.110
Maunakea, A. K., Nagarajan, R. P., Bilenky, M., Ballinger, T. J., D'Souza, C., Fouse, S. D., … Costello, J. F. (2010). Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature, 466, 253257.
McGoron, L., Gleason, M. M., Smyke, A. T., Drury, S. S., Nelson, C. A. III, Gregas, M. C., … Zeanah, C. H. (2012). Recovering from early deprivation: Attachment mediates effects of caregiving on psychopathology. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 683693. doi:10.1016/j.jaac.2012.05.004
McLaughlin, K. A., Sheridan, M. A., Winter, W., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2014). Widespread reductions in cortical thickness following severe early-life deprivation: A neurodevelopmental pathway to attention-deficit/hyperactivity disorder. Biological Psychiatry, 76, 629638. doi:10.1016/j.biopsych.2013.08.016
Meaney, M. J., & Ferguson-Smith, A. C. (2010). Epigenetic regulation of the neural transcriptome: The meaning of the marks. Nature Neuroscience, 13, 13131318.
Mehta, D., Klengel, T., Conneely, K. N., Smith, A. K., Altmann, A., Pace, T. W., … Binder, E. B. (2013). Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Proceedings of the National Academy of Sciences, 110, 83028307. doi:10.1073/pnas.1217750110
Metivier, R., Gallais, R., Tiffoche, C., Le Peron, C., Jurkowska, R. Z., Carmouche, R. P., … Salbert, G. (2008). Cyclical DNA methylation of a transcriptionally active promoter. Nature, 452, 4550.
Moore, S. R., McEwen, L. M., Quirt, J., Morin, A., Mah, S. M., Barr, R. G., … Kobor, M. S. (2017). Epigenetic correlates of neonatal contact in humans. Development and Psychopathology, 29, 15171538. doi:10.1017/S0954579417001213
Moss, E., Bureau, J. F., Cyr, C., Mongeau, C., & St.-Laurent, D. (2004). Correlates of attachment at age 3: Construct validity of the preschool attachment classification system. Developmental Psychology, 40, 323334. doi:10.1037/0012-1649.40.3.323
Moss, E., Cyr, C., Bureau, J. F., Tarabulsy, G. M., & Dubois-Comtois, K. (2005). Stability of attachment during the preschool period. Developmental Psychology, 41, 773783. doi:10.1037/0012-1649.41.5.773
Murgatroyd, C., Patchev, A. V., Wu, Y., Micale, V., Bockmuhl, Y., Fischer, D., … Spengler, D. (2009). Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nature Neuroscience, 12, 15591566. doi:10.1038/nn.2436
Nanni, V., Uher, R., & Danese, A. (2012). Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: A meta-analysis. American Journal of Psychiatry, 169, 141151.
Nelson, C. A., Zeanah, C. H., Fox, N. A., Marshall, P. J., Smyke, A. T., & Guthrie, D. (2007). Cognitive recovery in socially deprived young children: The Bucharest Early Intervention Project. Science, 318, 19371940. doi:10.1126/science.1143921
Ng, B., White, C. C., Klein, H. U., Sieberts, S. K., McCabe, C., Patrick, E., … De Jager, P. L. (2017). An xQTL map integrates the genetic architecture of the human brain's transcriptome and epigenome. Nature Neuroscience, 20, 14181426. doi:10.1038/nn.4632
O'Donnell, K. A., Gaudreau, H., Colalillo, S., Steiner, M., Atkinson, L., Moss, E., … MARVAN Research Team. (2014). The maternal adversity, vulnerability and neurodevelopment project: Theory and methodology. Canadian Journal of Psychiatry, 59, 497508. doi:10.1177/070674371405900906
O'Donnell, K. J., Chen, L., MacIsaac, J. L., McEwen, L. M., Nguyen, T., Beckmann, K., … Meaney, M. J. (2018). DNA methylome variation in a perinatal nurse-visitation program that reduces child maltreatment: A 27-year follow-up. Translational Psychiatry, 8, 15. doi:10.1038/s41398-017-0063-9
O'Donnell, K. J., Glover, V., Barker, E. D., & O'Connor, T. G. (2014). The persisting effect of maternal mood in pregnancy on childhood psychopathology. Development and Psychopathology, 26, 393403. doi:10.1017/S0954579414000029
O'Donnell, K. J., Glover, V., Holbrook, J. D., & O'Connor, T. G. (2014). Maternal prenatal anxiety and child brain-derived neurotrophic factor (BDNF) genotype: Effects on internalizing symptoms from 4 to 15 years of age. Development and Psychopathology, 26(4, Pt 2), 12551266. doi:10.1017/S095457941400100X
O'Donnell, K. J., Glover, V., Lahti, J., Lahti, M., Edgar, R. D., Raikkonen, K., & O'Connor, T. G. (2017). Maternal prenatal anxiety and child COMT genotype predict working memory and symptoms of ADHD. PLOS ONE, 12, e0177506. doi:10.1371/journal.pone.0177506
O'Donnell, K. J., & Meaney, M. J. (2016). Fetal origins of mental health: The developmental origins of health and disease hypothesis. American Journal of Psychiatry. Advance online publication. doi:10.1176/appi.ajp.2016.16020138
Pan, H., Chen, L., Dogra, S., Ling Teh, A., Tan, J. H., Lim, Y. I., … Holbrook, J. D. (2012). Measuring the methylome in clinical samples: Improved processing of the Infinium Human Methylation450 BeadChip Array. Epigenetics, 7, 11731187.
Papavassiliou, P., York, T. P., Gursoy, N., Hill, G., Nicely, L. V., Sundaram, U., … Jackson-Cook, C. (2009). The phenotype of persons having mosaicism for trisomy 21/Down syndrome reflects the percentage of trisomic cells present in different tissues. American Journal of Medical Genetics Part A, 149A, 573583. doi:10.1002/ajmg.a.32729
Pawlby, S., Hay, D. F., Sharp, D., Waters, C. S., & O'Keane, V. (2009). Antenatal depression predicts depression in adolescent offspring: Prospective longitudinal community-based study. Journal of Affective Disorders, 113, 236243. doi:10.1016/j.jad.2008.05.018
Pena, C. J., Neugut, Y. D., & Champagne, F. A. (2013). Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats. Endocrinology, 154, 43404351. doi:10.1210/en.2013-1595
Price, A. L., Patterson, N. J., Plenge, R. M., Weinblatt, M. E., Shadick, N. A., & Reich, D. (2006). Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics, 38, 904909. doi:10.1038/ng1847
Price, M. E., Cotton, A. M., Lam, L. L., Farre, P., Emberly, E., Brown, C. J., … Kobor, M. S. (2013). Additional annotation enhances potential for biologically-relevant analysis of the Illumina Infinium HumanMethylation450 BeadChip array. Epigenetics Chromatin, 6, 4. doi:10.1186/1756-8935-6-4
Pritchard, L. E., & White, A. (2007). Neuropeptide processing and its impact on melanocortin pathways. Endocrinology, 148, 42014207. doi:10.1210/en.2006-1686
Provençal, N., Suderman, M. J., Guillemin, C., Massart, R., Ruggiero, A., Wang, D., … Szyf, M. (2012). The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells. Journal of Neuroscience, 32, 1562615642. doi:10.1523/jneurosci.1470-12.2012
R Core Team. (2014). R: A language and environment for statistical computing. Vienna, Austria: Foundation for Statistical Computing.
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009). Lasting epigenetic influence of early-life adversity on the BDNF gene. Biological Psychiatry, 65, 760769. doi:10.1016/j.biopsych.2008.11.028
Rutter, M., Kumsta, R., Schlotz, W., & Sonuga-Barke, E. (2012). Longitudinal studies using a “natural experiment” design: The case of adoptees from Romanian institutions. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 762770. doi:10.1016/j.jaac.2012.05.011
Scholtens, S., Rydell, A.-M., Bohlin, G., & Thorell, L. (2014). ADHD symptoms and attachment representations: Considering the role of conduct problems, cognitive deficits and narrative responses in non-attachment-related story stems. Journal of Abnormal Child Psychology, 42, 10331042. doi:10.1007/s10802-014-9854-0
Sheleg, M., Yu, Q., Go, C., Wagner, G. C., Kusnecov, A. W., & Zhou, R. (2017). Decreased maternal behavior and anxiety in ephrin-A5(-/-) mice. Genes, Brain and Behavior, 16, 271284. doi:10.1111/gbb.12319
Silveira, P. P., Pokhvisneva, I., Parent, C., Cai, S., Rema, A. S. S., Broekman, B. F. P., … Meaney, M. J. (2017). Cumulative prenatal exposure to adversity reveals associations with a broad range of neurodevelopmental outcomes that are moderated by a novel, biologically informed polygenetic score based on the serotonin transporter solute carrier family C6, member 4 (SLC6A4) gene expression. Development and Psychopathology, 29, 16011617. doi:10.1017/S0954579417001262
Smith, A. K., Kilaru, V., Klengel, T., Mercer, K. B., Bradley, B., Conneely, K. N., … Binder, E. B. (2015). DNA extracted from saliva for methylation studies of psychiatric traits: Evidence tissue specificity and relatedness to brain. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 168B, 3644. doi:10.1002/ajmg.b.32278
Sonuga-Barke, E. J. S., Kennedy, M., Kumsta, R., Knights, N., Golm, D., Rutter, M., … Kreppner, J. (2017). Child-to-adult neurodevelopmental and mental health trajectories after early life deprivation: The young adult follow-up of the longitudinal English and Romanian Adoptees study. Lancet, 389, 15391548. doi:10.1016/S0140-6736(17)30045-4
Spatz Widom, C., DuMont, K., & Czaja, S. J. (2007). A prospective investigation of major depressive disorder and comorbidity in abused and neglected children grown up. Archives of General Psychiatry, 64, 4956.
Spielberger, C. D., Gorusch, R. L., & Lushene, R. E. (1970). STAI manual for the State-trait Anxiety Inventory. Pao Alto, CA: Consulting Psychologists Press.
Stadler, M. B., Murr, R., Burger, L., Ivanek, R., Lienert, F., Scholer, A., … Schubeler, D. (2011). DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature, 480, 490495. doi:10.1038/nature10716
Stocker, C. M., Masarik, A. S., Widaman, K. F., Reeb, B. T., Boardman, J. D., Smolen, A., … Conger, K. J. (2017). Parenting and adolescents' psychological adjustment: Longitudinal moderation by adolescents' genetic sensitivity. Development and Psychopathology, 29, 12891304. doi:10.1017/S0954579416001310
Suderman, M., McGowan, P. O., Sasaki, A., Huang, T. C. T., Hallett, M. T., Meaney, M. J., … Szyf, M. (2012). Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. Proceedings of the National Academy of Sciences, 109(Suppl. 2), 1726617272. doi:10.1073/pnas.1121260109
Teh, A. L., Pan, H., Chen, L., Ong, M. L., Dogra, S., Wong, J., … Holbrook, J. D. (2014). The effect of genotype and in utero environment on inter-individual variation in neonate DNA methylomes. Genome Research, 24, 10641074. doi:10.1101/gr.171439.113
Weaver, I. C., D'Alessio, A. C., Brown, S. E., Hellstrom, I. C., Dymov, S., Sharma, S., … Meaney, M. J. (2007). The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: Altering epigenetic marks by immediate-early genes. Journal of Neuroscience, 27, 17561768. doi:10.1523/JNEUROSCI.4164-06.2007
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., … Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847854.
Wu, Y., Patchev, A. V., Daniel, G., Almeida, O. F., & Spengler, D. (2014). Early-life stress reduces DNA methylation of the Pomc gene in male mice. Endocrinology, 155, 17511762. doi:10.1210/en.2013-1868
Yehuda, R., Daskalakis, N. P., Desarnaud, F., Makotkine, I., Lehrner, A. L., Koch, E., … Bierer, L. M. (2013). Epigenetic biomarkers as predictors and correlates of symptom improvement following psychotherapy in combat veterans with PTSD. Frontiers in Psychiatry, 4, 118. doi:10.3389/fpsyt.2013.00118
Zhang, T. Y., Hellstrom, I. C., Bagot, R. C., Wen, X., Diorio, J., & Meaney, M. J. (2010). Maternal care and DNA methylation of a glutamic acid decarboxylase 1 promoter in rat hippocampus. Journal of Neuroscience, 30, 1313013137. doi:10.1523/JNEUROSCI.1039-10.2010
Ziller, M. J., Gu, H., Muller, F., Donaghey, J., Tsai, L. T., Kohlbacher, O., … Meissner, A. (2013). Charting a dynamic DNA methylation landscape of the human genome. Nature, 500, 477481. doi:10.1038/nature12433
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