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Associations of prenatal depressive symptoms with DNA methylation of HPA axis-related genes and diurnal cortisol profiles in primary school-aged children

Published online by Cambridge University Press:  02 April 2018

Valeska Stonawski ,
Stefan Frey ,
Yulia Golub ,
Nicolas Rohleder ,
Jennifer Kriebel ,
Tamme W. Goecke ,
Peter A. Fasching ,
Matthias W. Beckmann ,
Johannes Kornhuber  and
Oliver Kratz
...Show all authors
Valeska Stonawski*
Affiliation:
University Hospital Erlangen Friedrich-Alexander University Erlangen-Nürnberg
Stefan Frey
Affiliation:
University Hospital Erlangen
Yulia Golub
Affiliation:
University Hospital Erlangen
Nicolas Rohleder
Affiliation:
Friedrich-Alexander University Erlangen-Nürnberg
Jennifer Kriebel
Affiliation:
Helmholtz Zentrum München German Center for Diabetes Research
Tamme W. Goecke
Affiliation:
University Hospital Erlangen RoMed Hospital Rosenheim
Peter A. Fasching
Affiliation:
University Hospital Erlangen
Matthias W. Beckmann
Affiliation:
University Hospital Erlangen
Johannes Kornhuber
Affiliation:
University Hospital Erlangen
Oliver Kratz
Affiliation:
University Hospital Erlangen
Gunther H. Moll
Affiliation:
University Hospital Erlangen
Hartmut Heinrich
Affiliation:
University Hospital Erlangen kbo-Heckscher-Klinikum
Anna Eichler
Affiliation:
University Hospital Erlangen
*
Address correspondence and reprint requests to: Valeska Stonawski, Department of Child and Adolescent Mental Health, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Schwabachanlage 6 & 10, D-91054 Erlangen, Germany; E-mail: [email protected].
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Abstract

Epigenetic DNA modifications in genes related to the hypothalamic–pituitary–adrenal (HPA) axis are discussed as a mechanism underlying the association between prenatal depression and altered child HPA activity. In a longitudinal study, DNA methylation changes related to prenatal depressive symptoms were investigated in 167 children aged 6 to 9 years. At six candidate genes, 126 cytosine–guanine dinucleotides were considered without correcting for multiple testing due to the exploratory nature of the study. Further associations with the basal child HPA activity were examined. Children exposed to prenatal depressive symptoms exhibited lower bedtime cortisol (p = .003, ηp2 = 0.07) and a steeper diurnal slope (p = .023, ηp2 = 0.06). For total cortisol release, prenatal exposure was related to lower cortisol release in boys, and higher release in girls. Furthermore, prenatal depressive symptoms were associated with altered methylation in the glucocorticoid receptor gene (NR3C1), the mineralocorticoid receptor gene (NR3C2), and the serotonin receptor gene (SLC6A4), with some sex-specific effects (p = .012–.040, ηp2 = 0.03–0.04). In boys, prenatal depressive symptoms predicted bedtime cortisol mediated by NR3C2 methylation, indirect effect = –0.07, 95% confidence interval [–0.16, –0.02]. Results indicate relations of prenatal depressive symptoms to both child basal HPA activity and DNA methylation, partially fitting a mediation model, with exposed boys and girls being affected differently.

Keywords

cortisolDNA methylationepigeneticspregnancyprenatal depression
Type
Regular Articles
Information
Development and Psychopathology , Volume 31 , Issue 2 , May 2019 , pp. 419 - 431
Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

The project was supported by the ELAN Fonds of the University Hospital of Erlangen, Germany (to A.E.). The Staedtler-Stifung (Nürnberg, Germany) grant covered the costs for the DNA methylation analysis (to G.H.M.). The authors thank all families who participated in FRANCES, as well as all colleagues and student assistants who contributed to this study. Special thanks to Jörg Distler and Ruth Steigleder for their technical support. The present work was performed in partial fulfillment of the requirements for obtaining the PhD degree of Valeska Stonawski.

References

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, 1363–1369. doi:10.1093/bioinformatics/btu049.Google Scholar
Bale, T. L. (2011). Sex differences in prenatal epigenetic programming of stress pathways. Stress, 14, 348–356. doi:10.3109/10253890.2011.586447.Google Scholar
Bangasser, D. A. (2013). Sex differences in stress-related receptors: “Micro” differences with “macro” implications for mood and anxiety disorders. Biology of Sex Differences, 4, 2. doi:10.1186/2042-6410-4-2.Google Scholar
Behrendt, H. F., Konrad, K., Goecke, T. W., Fakhrabadi, R., Herpertz-Dahlmann, B., & Firk, C. (2016). Postnatal mother-to-infant attachment in subclinically depressed mothers: Dyads at risk? Psychopathology, 49, 269–276. doi:10.1159/000447597.Google Scholar
Berardelli, R., Karamouzis, I., D'Angelo, V., Zichi, C., Fussotto, B., Giordano, R., … Arvat, E. (2013). Role of mineralocorticoid receptors on the hypothalamus-pituitary-adrenal axis in humans. Endocrine, 43, 51–58. doi:10.1007/s12020-012-9750-8.Google Scholar
Braithwaite, E. C., Kundakovic, M., Ramchandani, P. G., Murphy, S. E., & Champagne, F. A. (2015). Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation. Epigenetics, 10, 408–417. doi:10.1080/15592294.2015.1039221.Google Scholar
Buckley, T. M., Mullen, B. C., & Schatzberg, A. F. (2007). The acute effects of a mineralocorticoid receptor (MR) agonist on nocturnal hypothalamic-adrenal-pituitary (HPA) axis activity in healthy controls. Psychoneuroendocrinology, 32, 859–864. doi:10.1016/j.psyneuen.2007.05.016.Google Scholar
Carpenter, T., Grecian, S. M., & Reynolds, R. M. (2017). Sex differences in early-life programming of the hypothalamic-pituitary-adrenal axis in humans suggest increased vulnerability in females: A systematic review. Journal of Developmental Origins of Health and Disease. Advance online publication. doi:10.1017/s204017441600074x.Google Scholar
Clifton, V. L. (2010). Review: Sex and the human placenta: Mediating differential strategies of fetal growth and survival. Placenta, 31(Suppl.), S33–S39. doi:10.1016/j.placenta.2009.11.010.Google Scholar
Cohen, J. (1988). Statistical power analysis for the behavioral sciences. Hillsdale, NJ: Erlbaum.Google Scholar
Cox, J. L., Holden, J. M., & Sagovsky, R. (1987). Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale. British Journal of Psychiatry, 150, 782–786.Google Scholar
de Kloet, E. R. (2016). Corticosteroid receptor balance hypothesis: Implications for stress-adaption. In Fink, G. (Ed.), Stress: Concepts, cognition, emotion, and behavior (pp. 21–31). Amsterdam: Elsevier Academic Press.Google Scholar
de Kloet, E. R., Otte, C., Kumsta, R., Kok, L., Hillegers, M. H., Hasselmann, H., … Joels, M. (2016). Stress and depression: A crucial role of the mineralocorticoid receptor. Journal of Neuroendocrinology, 28. doi:10.1111/jne.12379.Google Scholar
Devlin, A. M., Brain, U., Austin, J., & Oberlander, T. F. (2010). Prenatal exposure to maternal depressed mood and the MTHFR C677T variant affect SLC6A4 methylation in infants at birth. PLOS ONE, 5, e12201. doi:10.1371/journal.pone.0012201.Google Scholar
Diego, M. A., Field, T., Hernandez-Reif, M., Cullen, C., Schanberg, S., & Kuhn, C. (2004). Prepartum, postpartum, and chronic depression effects on newborns. Psychiatry, 67, 63–80.Google Scholar
Eichler, A., Grunitz, J., Grimm, J., Walz, L., Raabe, E., Goecke, T. W., … Kornhuber, J. (2016). Did you drink alcohol during pregnancy? Inaccuracy and discontinuity of women's self-reports: On the way to establish meconium ethyl glucuronide (EtG) as a biomarker for alcohol consumption during pregnancy. Alcohol, 54, 39–44. doi:10.1016/j.alcohol.2016.07.002.Google Scholar
Eichler, A., Walz, L., Grunitz, J., Grimm, J., Van Doren, J., Raabe, E., … Moll, G. H. (2017). Children of prenatally depressed mothers: Externalizing and internalizing symptoms are accompanied by reductions in specific social-emotional competencies. Journal of Child and Family Studies. Advance online publication. doi:10.1007/s10826-017-0819-0.Google Scholar
El Marroun, H., White, T. J., van der Knaap, N. J., Homberg, J. R., Fernandez, G., Schoemaker, N. K., … Tiemeier, H. (2014). Prenatal exposure to selective serotonin reuptake inhibitors and social responsiveness symptoms of autism: Population-based study of young children. British Journal of Psychiatry, 205, 95–102. doi:10.1192/bjp.bp.113.127746.Google Scholar
Essex, M. J., Shirtcliff, E. A., Burk, L. R., Ruttle, P. L., Klein, M. H., Slattery, M. J., … Armstrong, J. M. (2011). Influence of early life stress on later hypothalamic-pituitary-adrenal axis functioning and its covariation with mental health symptoms: A study of the allostatic process from childhood into adolescence. Developmental Psychology, 23, 1039–1058. doi:10.1017/s0954579411000484.Google Scholar
Field, A. P. (2013). Discovering statistics using IBM SPSS statistics (4th ed.). London: Sage.Google Scholar
Field, T. (2011). Prenatal depression effects on early development: A review. Infant Behavior and Development, 34, 1–14. doi:10.1016/j.infbeh.2010.09.008.Google Scholar
Field, T. (2017). Prenatal depression risk factors, developmental effects and interventions: A review. Journal of Pregnancy and Child Health, 4. doi:10.4172/2376-127x.1000301.Google Scholar
Fisher, P. A. (2017). Commentary: Is there a there there in hair? A reflection on child maltreatment and hair cortisol concentrations in White et al. (2017). Journal of Child Psychology and Psychiatry, 58, 1008–1010. doi:10.1111/jcpp.12719.Google Scholar
Fries, E., Hesse, J., Hellhammer, J., & Hellhammer, D. H. (2005). A new view on hypocortisolism. Psychoneuroendocrinology, 30, 1010–1016. doi:10.1016/j.psyneuen.2005.04.006.Google Scholar
Gaillard, A., Le Strat, Y., Mandelbrot, L., Keita, H., & Dubertret, C. (2014). Predictors of postpartum depression: Prospective study of 264 women followed during pregnancy and postpartum. Psychiatry Research, 215, 341–346. doi:10.1016/j.psychres.2013.10.003.Google Scholar
Geißler, R. (1994). Soziale Schichtung und Lebenschancen in Deutschland (2nd ed.). Stuttgart: Ferdinand Enke Verlag.Google Scholar
Gentile, S. (2015). Untreated depression during pregnancy: Short- and long-term effects in offspring. A systematic review. Neuroscience. Advance online publication. doi:10.1016/j.neuroscience.2015.09.001.Google Scholar
Glover, V., & Hill, J. (2012). Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: An evolutionary perspective. Physiology & Behavior, 106, 736–740. doi:10.1016/j.physbeh.2012.02.011.Google Scholar
Goodman, R. (2001). Psychometric properties of the Strengths and Difficulties Questionnaire. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 1337–1345. doi:10.1097/00004583-200111000-00015.Google Scholar
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press.Google Scholar
Hein, A., Rauh, C., Engel, A., Haberle, L., Dammer, U., Voigt, F., … Goecke, T. W. (2013). Socioeconomic status and depression during and after pregnancy in the Franconian Maternal Health Evaluation Studies (FRAMES). Archives of Gynecology and Obstetrics, 289, 755–763. doi:10.1007/s00404-013-3046-y.Google Scholar
Heuser, I., Deuschle, M., Weber, A., Kniest, A., Ziegler, C., Weber, B., & Colla, M. (2000). The role of mineralocorticoid receptors in the circadian activity of the human hypothalamus-pituitary-adrenal system: Effect of age. Neurobiology of Aging, 21, 585–589.Google Scholar
Korhonen, M., Luoma, I., Salmelin, R., & Tamminen, T. (2012). A longitudinal study of maternal prenatal, postnatal and concurrent depressive symptoms and adolescent well-being. Journal of Affective Disorders, 136, 680–692. doi:10.1016/j.jad.2011.10.007.Google Scholar
Koss, K. J., Mliner, S. B., Donzella, B., & Gunnar, M. R. (2016). Early adversity, hypocortisolism, and behavior problems at school entry: A study of internationally adopted children. Psychoneuroendocrinology, 66, 31–38. doi:10.1016/j.psyneuen.2015.12.018.Google Scholar
Laurent, H. K., Leve, L. D., Neiderhiser, J. M., Natsuaki, M. N., Shaw, D. S., Harold, G. T., & Reiss, D. (2013). Effects of prenatal and postnatal parent depressive symptoms on adopted child HPA regulation: Independent and moderated influences. Developmental Psychology, 49, 876–886. doi:10.1037/a0028800.Google Scholar
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.Google Scholar
Levene, H., (1960). Robust tests for equality of variances. In Olkin, I. (Ed.), Contributions to probability and statistics (pp. 278–292). Palo Alto, CA: Stanford University Press.Google Scholar
Mansell, T., Vuillermin, P., Ponsonby, A. L., Collier, F., Saffery, R., & Ryan, J. (2016). Maternal mental well-being during pregnancy and glucocorticoid receptor gene promoter methylation in the neonate. Development and Psychopathology, 28(4, Pt. 2), 1421–1430. doi:10.1017/s0954579416000183.Google Scholar
Martel, M. M. (2013). Sexual selection and sex differences in the prevalence of childhood externalizing and adolescent internalizing disorders. Psychological Bulletin, 139, 1221–1259. doi:10.1037/a0032247.Google Scholar
McBurnett, K., Lahey, B. B., Rathouz, P. J., & Loeber, R. (2000). Low salivary cortisol and persistent aggression in boys referred for disruptive behavior. Archives of General Psychiatry, 57, 38–43.Google Scholar
Medina, A., Seasholtz, A. F., Sharma, V., Burke, S., Bunney, W. Jr., Myers, R. M., … Watson, S. J. (2013). Glucocorticoid and mineralocorticoid receptor expression in the human hippocampus in major depressive disorder. Journal of Psychiatric Research, 47, 307–314. doi:10.1016/j.jpsychires.2012.11.002.Google Scholar
Miller, G. E., Chen, E., & Zhou, E. S. (2007). If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bulletin, 133, 25–45. doi:10.1037/0033-2909.133.1.25.Google Scholar
Mueller, B. R., & Bale, T. L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience, 28, 9055–9065. doi:10.1523/jneurosci.1424-08.2008.Google Scholar
Murgatroyd, C., Quinn, J. P., Sharp, H. M., Pickles, A., & Hill, J. (2015). Effects of prenatal and postnatal depression, and maternal stroking, at the glucocorticoid receptor gene. Translational Psychiatry, 5, e560. doi:10.1038/tp.2014.140.Google Scholar
Non, A. L., Binder, A. M., Kubzansky, L. D., & Michels, K. B. (2014). Genome-wide DNA methylation in neonates exposed to maternal depression, anxiety, or SSRI medication during pregnancy. Epigenetics, 9, 964–972. doi:10.4161/epi.28853.Google Scholar
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics, 3, 97–106.Google Scholar
O'Donnell, K. J., Glover, V., Jenkins, J., Browne, D., Ben-Shlomo, Y., Golding, J., & O'Connor, T. G. (2013). Prenatal maternal mood is associated with altered diurnal cortisol in adolescence. Psychoneuroendocrinology, 38, 1630–1638. doi:10.1016/j.psyneuen.2013.01.008.Google Scholar
Ostlund, B. D., Conradt, E., Crowell, S. E., Tyrka, A. R., Marsit, C. J., & Lester, B. M. (2016). Prenatal stress, fearfulness, and the epigenome: Exploratory analysis of sex differences in DNA methylation of the glucocorticoid receptor gene. Frontiers in Behavioral Neuroscience, 10, 147. doi:10.3389/fnbeh.2016.00147.Google Scholar
Otte, C., Jahn, H., Yassouridis, A., Arlt, J., Stober, N., Maass, P., … Kellner, M. (2003). The mineralocorticoid receptor agonist, fludrocortisone, inhibits pituitary-adrenal activity in humans after pre-treatment with metyrapone. Life Sciences, 73, 1835–1845.Google Scholar
Panagiotakopoulos, L., & Neigh, G. N. (2014). Development of the HPA axis: Where and when do sex differences manifest? Frontiers in Neuroendocrinology, 35, 285–302. doi:10.1016/j.yfrne.2014.03.002.Google Scholar
Parade, S. H., Ridout, K. K., Seifer, R., Armstrong, D. A., Marsit, C. J., McWilliams, M. A., & Tyrka, A. R. (2016). Methylation of the glucocorticoid receptor gene promoter in preschoolers: Links with internalizing behavior problems. Child Development, 87, 86–97. doi:10.1111/cdev.12484.Google Scholar
Park, S., Lee, J. M., Kim, J. W., Cho, D. Y., Yun, H. J., Han, D. H., … Kim, B. N. (2015). Associations between serotonin transporter gene (SLC6A4) methylation and clinical characteristics and cortical thickness in children with ADHD. Psychological Medicine, 45, 3009–3017. doi:10.1017/s003329171500094x.Google Scholar
Perroud, N., Rutembesa, E., Paoloni-Giacobino, A., Mutabaruka, J., Mutesa, L., Stenz, L., … Karege, F. (2014). The Tutsi genocide and transgenerational transmission of maternal stress: Epigenetics and biology of the HPA axis. World Journal of Biological Psychiatry, 15, 334–345. doi:10.3109/15622975.2013.866693.Google Scholar
Plant, D. T., Pariante, C. M., Sharp, D., & Pawlby, S. (2015). Maternal depression during pregnancy and offspring depression in adulthood: Role of child maltreatment. British Journal of Psychiatry. Advance online publication. doi:10.1192/bjp.bp.114.156620.Google Scholar
Provenzi, L., Giorda, R., Beri, S., & Montirosso, R. (2016). SLC6A4 methylation as an epigenetic marker of life adversity exposures in humans: A systematic review of literature. Neuroscience and Biobehavioral Reviews, 71, 7–20. doi:10.1016/j.neubiorev.2016.08.021.Google Scholar
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28, 916–931. doi:10.1016/s0306-4530(02)00108-7.Google Scholar
Quarini, C., Pearson, R. M., Stein, A., Ramchandani, P. G., Lewis, G., & Evans, J. (2016). Are female children more vulnerable to the long-term effects of maternal depression during pregnancy? Journal of Affective Disorders, 189, 329–335. doi:10.1016/j.jad.2015.09.039.Google Scholar
Reulbach, U., Bleich, S., Knorr, J., Burger, P., Fasching, P. A., Kornhuber, J., … Goecke, T. W. (2009). [Pre-, peri- and postpartal depression]. Fortschritte der Neurologie— Psychiatrie, 77, 708–713. doi:10.1055/s-0028-1109822.Google Scholar
Reynolds, R. M., Pesonen, A.-K., O'Reilly, J. R., Tuovinen, S., Lahti, M., Kajantie, E., … Räikkönen, K. (2015). Maternal depressive symptoms throughout pregnancy are associated with increased placental glucocorticoid sensitivity. Psychological Medicine, 45, 2023–2030. doi:10.1017/S003329171400316X.Google Scholar
Schore, A. N. (2017). All our sons: The developmental neurobiology and neuroendocrinology of boys at risk. Infant Mental Health Journal, 38, 15–52. doi:10.1002/imhj.21616.Google Scholar
Shirtcliff, E. A., Allison, A. L., Armstrong, J. M., Slattery, M. J., Kalin, N. H., & Essex, M. J. (2012). Longitudinal stability and developmental properties of salivary cortisol levels and circadian rhythms from childhood to adolescence. Developmental Psychobiology, 54, 493–502. doi:10.1002/dev.20607.Google Scholar
Stalder, T., Kirschbaum, C., Kudielka, B. M., Adam, E. K., Pruessner, J. C., Wüst, S., … Clow, A. (2016). Assessment of the cortisol awakening response: Expert consensus guidelines. Psychoneuroendocrinology, 63, 414–432. doi:10.1016/j.psyneuen.2015.10.010.Google Scholar
Stonawski, V., Frey, S., Golub, Y., Moll, G. H., Heinrich, H., & Eichler, A. (2017). [Epigenetic modifications in children associated with maternal emotional stress during pregnancy]. Zeitschrift für Kinder- und Jugendpsychiatrie und Psychotherapie. Advance online publication. doi:10.1024/1422-4917/a000515.Google Scholar
Szyf, M., & Bick, J. (2013). DNA methylation: A mechanism for embedding early life experiences in the genome. Child Development, 84, 49–57. doi:10.1111/j.1467-8624.2012.01793.x.Google Scholar
ter Heegde, F., De Rijk, R. H., & Vinkers, C. H. (2015). The brain mineralocorticoid receptor and stress resilience. Psychoneuroendocrinology, 52, 92–110. doi:10.1016/j.psyneuen.2014.10.022.Google Scholar
Trickett, P. K., Noll, J. G., Susman, E. J., Shenk, C. E., & Putnam, F. W. (2010). Attenuation of cortisol across development for victims of sexual abuse. Development and Psychopathology, 22, 165–175. doi:10.1017/s0954579409990332.Google Scholar
Tyrka, A. R., Ridout, K. K., & Parade, S. H. (2016). Childhood adversity and epigenetic regulation of glucocorticoid signaling genes: Associations in children and adults. Development and Psychopathology. Advance online publication. doi:10.1017/s0954579416000870.Google Scholar
van der Knaap, L. J., Oldehinkel, A. J., Verhulst, F. C., van Oort, F. V., & Riese, H. (2015). Glucocorticoid receptor gene methylation and HPA-axis regulation in adolescents. The TRAILS study. Psychoneuroendocrinology, 58, 46–50. doi:10.1016/j.psyneuen.2015.04.012.Google Scholar
van der Voorn, B., Hollanders, J. J., Ket, J. C., Rotteveel, J., & Finken, M. J. (2017). Gender-specific differences in hypothalamus-pituitary-adrenal axis activity during childhood: A systematic review and meta-analysis. Biology of Sex Differences, 8, 3. doi:10.1186/s13293-016-0123-5.Google Scholar
Wadhwa, P. D., Buss, C., Entringer, S., & Swanson, J. M. (2009). Developmental origins of health and disease: Brief history of the approach and current focus on epigenetic mechanisms. Seminars in Reproductive Medicine, 27, 358–368. doi:10.1055/s-0029-1237424.Google Scholar
Weder, N., Zhang, H., Jensen, K., Yang, B. Z., Simen, A., Jackowski, A., … Kaufman, J. (2014). Child abuse, depression, and methylation in genes involved with stress, neural plasticity, and brain circuitry. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 417–424. doi:10.1016/j.jaac.2013.12.025.Google Scholar
White, L. O., Ising, M., von Klitzing, K., Sierau, S., Michel, A., Klein, A. M., … Stalder, T. (2017). Reduced hair cortisol after maltreatment mediates externalizing symptoms in middle childhood and adolescence. Journal of Child Psychology and Psychiatry. Advance online publication. doi:10.1111/jcpp.12700.Google Scholar
Zahn-Waxler, C., Shirtcliff, E. A., & Marceau, K. (2008). Disorders of childhood and adolescence: Gender and psychopathology. Annual Review of Clinical Psychology, 4, 275–303. doi:10.1146/annurev.clinpsy.3.022806.091358.Google Scholar
Zeilinger, S., Kühnel, B., Klopp, N., Baurecht, H., Kleinschmidt, A., Gieger, C., … Illig, T. (2013). Tobacco smoking leads to extensive genome-wide changes in DNA methylation. PLOS ONE, 8, e63812. doi:10.1371/journal.pone.0063812.Google Scholar
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