Does maternal mental well-being in pregnancy impact the early human epigenome?

Epigenomics

Volumn 9, Issue 3, 2017, Pages 313-322

  Ryan, Joanne ^a,b,c   Mansell, Toby ^a   Fransquet, Peter ^a   Saffery, Richard ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIV MONTPELLIER   (France)

Author keywords

anxiety; biomarkers; depression; DNA methylation; epigenetics; humans; mental health; perinatal; pregnancy; stress

Indexed keywords

NEUROTRANSMITTER;

ANXIETY DISORDER; BDNF GENE; BRAIN FUNCTION; CPG ISLAND; CRHR1 GENE; DEPRESSION; DNA METHYLATION; EPIGENETICS; EXON; FEMALE; FKBP5 GENE; GENE; GENETIC CODE; GENOME IMPRINTING; GENOME-WIDE ASSOCIATION STUDY; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MATERNAL STRESS; MATERNAL WELFARE; META ANALYSIS (TOPIC); NONHUMAN; NR3C1 GENE; OXTR GENE; PREGNANCY; PRIORITY JOURNAL; PROGENY; PSYCHOLOGICAL WELL-BEING; REVIEW; SLC6A4 GENE; SYSTEMATIC REVIEW; EMBRYO DEVELOPMENT; GENETIC EPIGENESIS; GENETICS; MENTAL HEALTH; MENTAL STRESS; PRENATAL EXPOSURE; PSYCHOLOGY;

DNA METHYLATION; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; FEMALE; HUMANS; MENTAL HEALTH; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STRESS, PSYCHOLOGICAL;

EID: 85014052892     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi-2016-0118     Document Type: Review

References (125)

1. Wiegner L, Hange D, Bjorkelund C, Ahlborg G Jr. Prevalence of perceived stress and associations to symptoms of exhaustion, depression and anxiety in a working age population seeking primary care-an observational study. BMC Fam. Pract. 16, 38 (2015).
2. Woods SM, Melville JL, Guo Y, Fan MY, Gavin A. Psychosocial stress during pregnancy. Am. J. Obstet. Gynecol. 202(1), 61.e61-67.e61 (2010).
3. Lee AM, Lam SK, Sze Mun Lau SM, Chong CS, Chui HW, Fong DY. Prevalence, course, and risk factors for antenatal anxiety and depression. Obstet. Gynecol. 110(5), 1102-1112 (2007).
4. Melville JL, Gavin A, Guo Y, Fan MY, Katon WJ. Depressive disorders during pregnancy: prevalence and risk factors in a large urban sample. Obstet. Gynecol. 116(5), 1064-1070 (2010).
5. Staneva A, Bogossian F, Pritchard M, Wittkowski A. The effects of maternal depression, anxiety, and perceived stress during pregnancy on preterm birth: a systematic review. Women Birth 28(3), 179-193 (2015).
6. Grigoriadis S, Vonderporten EH, Mamisashvili L et al. The impact of maternal depression during pregnancy on perinatal outcomes: a systematic review and meta-analysis. J. Clin. Psychiatry 74(4), e321-e341 (2013).
7. Jarde A, Morais M, Kingston D et al. Neonatal outcomes in women with untreated antenatal depression compared with women without depression: a systematic review and metaanalysis. JAMA Psychiatry 73(8), 826-837 (2016).
8. Buss C, Davis EP, Muftuler LT, Head K, Sandman CA. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology 35(1), 141-153 (2010).
9. Lewis AJ, Austin E, Galbally M. Prenatal maternal mental health and fetal growth restriction: a systematic review. J. Dev. Orig. Health Dis. 7(4), 416-428 (2016).
10. Kingston D, Mcdonald S, Austin MP, Tough S. Association between prenatal and postnatal psychological distress and toddler cognitive development: a systematic review. PLoS ONE 10(5), e0126929 (2015).
11. Weikum WM, Oberlander TF, Hensch TK, Werker JF. Prenatal exposure to antidepressants and depressed maternal mood alter trajectory of infant speech perception. Proc. Natl Acad. Sci. USA 109(Suppl. 2), 17221-17227 (2012).
12. Laplante DP, Barr RG, Brunet A et al. Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr. Res. 56(3), 400-410 (2004).
13. Gutteling BM, De Weerth C, Zandbelt N, Mulder EJ, Visser GH, Buitelaar JK. Does maternal prenatal stress adversely affect the child's learning and memory at age six? J. Abnorm. Child Psychol. 34(6), 789-798 (2006).
14. Mennes M, Van Den Bergh B, Lagae L, Stiers P. Developmental brain alterations in 17 year old boys are related to antenatal maternal anxiety. Clin. Neurophysiol. 120(6), 1116-1122 (2009).
15. Sharp H, Hill J, Hellier J, Pickles A. Maternal antenatal anxiety, postnatal stroking and emotional problems in children: outcomes predicted from pre-and postnatal programming hypotheses. Psychol. Med. 45(2), 269-283 (2015).
16. Nulman I, Koren G, Rovet J et al. Neurodevelopment of children following prenatal exposure to venlafaxine, selective serotonin reuptake inhibitors, or untreated maternal depression. Am. J. Psychiatry 169(11), 1165-1174 (2012).
17. Gutteling BM, De Weerth C, Willemsen-Swinkels SH et al. The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. Eur. Child Adolesc. Psychiatry 14(1), 41-51 (2005).
18. Hay DF, Pawlby S, Waters CS, Perra O, Sharp D. Mothers' antenatal depression and their children's antisocial outcomes. Child Dev. 81(1), 149-165 (2010).
19. Rodriguez A, Bohlin G. Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J. Child Psychol. Psychiatry 46(3), 246-254 (2005).
20. Van Den Bergh BR, Marcoen A. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8-and 9-year-olds. Child Dev. 75(4), 1085-1097 (2004).
21. Khashan AS, Abel KM, Mcnamee R et al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch. Gen. Psychiatry 65(2), 146-152 (2008).
22. Kinney DK, Miller AM, Crowley DJ, Huang E, Gerber E. Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. J. Autism Dev. Disord. 38(3), 481-488 (2008).
23. Talge NM, Neal C, Glover V. Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J. Child Psychol. Psychiatry 48(3-4), 245-261 (2007).
24. Pawlby S, Hay DF, Sharp D, Waters CS, O'Keane V. Antenatal depression predicts depression in adolescent offspring: prospective longitudinal community-based study. J. Affect. Disord. 113(3), 236-243 (2009).
25. Slykerman RF, Thompson J, Waldie K, Murphy R, Wall C, Mitchell EA. Maternal stress during pregnancy is associated with moderate to severe depression in 11-year-old children. Acta Paediatr. 104(1), 68-74 (2015).
26. Lester BM, Conradt E, Marsit CJ. Epigenetic basis for the development of depression in children. Clin. Obstet. Gynecol. 56(3), 556-565 (2013).
27. Hall HG, Beattie J, Lau R, East C, Anne Biro M. Mindfulness and perinatal mental health: a systematic review. Women Birth 29(1), 62-71 (2016).
28. De Kloet ER, Joels M, Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6(6), 463-475 (2005).
29. Doom JR, Cicchetti D, Rogosch FA. Longitudinal patterns of cortisol regulation differ in maltreated and nonmaltreated children. J. Am. Acad. Child Adolesc. Psychiatry 53(11), 1206-1215 (2014).
30. Powers SI, Laurent HK, Gunlicks-Stoessel M, Balaban S, Bent E. Depression and anxiety predict sex-specific cortisol responses to interpersonal stress. Psychoneuroendocrinology 69, 172-179 (2016).
31. Belvederi Murri M, Pariante C, Mondelli V et al. HPA axis and aging in depression: systematic review and meta-analysis. Psychoneuroendocrinology 41, 46-62 (2014).
32. Glover V, O'connor TG, O'donnell K. Prenatal stress and the programming of the HPA axis. Neurosci. Biobehav. Rev. 35(1), 17-22 (2010).
33. Novakovic B, Saffery R. The ever growing complexity of placental epigenetics-role in adverse pregnancy outcomes and fetal programming. Placenta 33(12), 959-970 (2012).
34. Cottrell EC, Seckl JR. Prenatal stress, glucocorticoids and the programming of adult disease. Front. Behav. Neurosci. 3, 19 (2009).
35. Schoof E, Girstl M, Frobenius W et al. Course of placental 11beta-hydroxysteroid dehydrogenase type 2 and 15-hydroxyprostaglandin dehydrogenase mRNA expression during human gestation. Eur. J. Endocrinol. 145(2), 187-192 (2001).
36. Seth S, Lewis AJ, Saffery R, Lappas M, Galbally M. Maternal prenatal mental health and placental 11beta-HSD2 gene expression: initial findings from the mercy pregnancy and emotional wellbeing study. Int. J. Mol. Sci. 16(11), 27482-27496 (2015).
37. Baibazarova E, Van De Beek C, Cohen-Kettenis PT, Buitelaar J, Shelton KH, Van Goozen SH. Influence of prenatal maternal stress, maternal plasma cortisol and cortisol in the amniotic fluid on birth outcomes and child temperament at 3 months. Psychoneuroendocrinology 38(6), 907-915 (2013).
38. O'connor TG, Bergman K, Sarkar P, Glover V. Prenatal cortisol exposure predicts infant cortisol response to acute stress. Dev. Psychobiol. 55(2), 145-155 (2013).
39. Smith AK, Newport DJ, Ashe MP et al. Predictors of neonatal hypothalamic-pituitary-adrenal axis activity at delivery. Clin. Endocrinol. (Oxf.). 75(1), 90-95 (2011).
40. Huizink AC, Bartels M, Rose RJ, Pulkkinen L, Eriksson CJ, Kaprio J. Chernobyl exposure as stressor during pregnancy and hormone levels in adolescent offspring. J. Epidemiol. Community Health 62(4), e5 (2008).
41. Van Den Bergh BR, Van Calster B, Smits T, Van Huffel S, Lagae L. Antenatal maternal anxiety is related to HPAaxis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 33(3), 536-545 (2008).
42. Entringer S, Kumsta R, Hellhammer DH, Wadhwa PD, Wust S. Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults. Horm. Behav. 55(2), 292-298 (2009).
43. Stewart CP, Oaks BM, Laugero KD et al. Maternal cortisol and stress are associated with birth outcomes, but are not affected by lipid-based nutrient supplements during pregnancy: an analysis of data from a randomized controlled trial in rural Malawi. BMC Pregnancy Childbirth 15, 346 (2015).
44. Glover V. Annual research review: prenatal stress and the origins of psychopathology: an evolutionary perspective. J. Child Psychol. Psychiatry 52(4), 356-367 (2011).
45. Gluckman PA, Hanson MA. Developmental Origins of Health and Disease. Cambridge University Press, London, UK (2006).
46. Saffery R, Novakovic B. Epigenetics as the mediator of fetal programming of adult onset disease: what is the evidence? Acta Obstet. Gynecol. Scand. 93(11), 1090-1098 (2014).
47. Gluckman PD, Hanson MA. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr. Res. 56(3), 311-317 (2004).
48. Petronis A. Epigenetics as a unifying principle in the aetiology of complex traits and diseases. Nature 465(7299), 721-727 (2010).
49. Januar V, Saffery R, Ryan J. Epigenetics and depressive disorders: a review of current progress and future directions. Int. J. Epidemiol. 44(4), 1364-1387 (2015).
50. Joubert BR, Felix JF, Yousefi P et al. DNA methylation in newborns and maternal smoking in pregnancy: genomewide consortium meta-analysis. Am. J. Hum. Genet. 98(4), 680-696 (2016).
51. Joubert BR, Den Dekker HT, Felix JF et al. Maternal plasma folate impacts differential DNA methylation in an epigenome-wide meta-analysis of newborns. Nat. Commun. 7, 10577 (2016).
52. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3(2), 97-106 (2008).
53. Radtke KM, Ruf M, Gunter HM et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl. Psychiatry 1, e21 (2011).
54. Mulligan CJ, D'Errico NC, Stees J, Hughes DA. Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics 7(8), 853-857 (2012).
55. Conradt E, Lester BM, Appleton AA, Armstrong DA, Marsit CJ. The roles of DNA methylation of NR3C1 and 11beta-HSD2 and exposure to maternal mood disorder in utero on newborn neurobehavior. Epigenetics 8(12), 1321-1329 (2013).
56. Hompes T, Izzi B, Gellens E et al. 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. J. Psychiatr. Res. 47(7), 880-891 (2013).
57. Non AL, Binder AM, Kubzansky LD, Michels KB. Genomewide DNA methylation in neonates exposed to maternal depression, anxiety, or SSRI medication during pregnancy. Epigenetics 9(7), 964-972 (2014).
58. Perroud N, Rutembesa E, Paoloni-Giacobino A et al. The Tutsi genocide and transgenerational transmission of maternal stress: epigenetics and biology of the HPA axis. World J. Biol. Psychiatry 15(4), 334-345 (2014).
59. Braithwaite EC, Kundakovic M, Ramchandani PG, Murphy SE, Champagne FA. Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation. Epigenetics 10(5), 408-417 (2015).
60. Murgatroyd C, Quinn JP, Sharp HM, Pickles A, Hill J. Effects of prenatal and postnatal depression, and maternal stroking, at the glucocorticoid receptor gene. Transl. Psychiatry 5, e560 (2015).
61. Kertes DA, Kamin HS, Hughes DA, Rodney NC, Bhatt S, Mulligan CJ. Prenatal maternal stress predicts methylation of genes regulating the hypothalamic-pituitary-adrenocortical system in mothers and newborns in the Democratic Republic of Congo. Child Dev. 87(1), 61-72 (2016).
62. Mansell T, Vuillermin P, Ponsonby AL, Collier F, Saffery R, Ryan J. Maternal mental well-being during pregnancy and glucocorticoid receptor gene promoter methylation in the neonate. Dev. Psychopathol. 28(4pt2), 1421-1430 (2016).
63. Appleton AA, Armstrong DA, Lesseur C et al. Patterning in placental 11-B hydroxysteroid dehydrogenase methylation according to prenatal socioeconomic adversity. PLoS ONE 8(9), e74691 (2013).
64. Soubry A, Murphy S, Huang Z et al. The effects of depression and use of antidepressive medicines during pregnancy on the methylation status of the IGF2 imprinted control regions in the offspring. Clin. Epigenetics 3, 2 (2012).
65. Liu Y, Murphy SK, Murtha AP et al. Depression in pregnancy, infant birth weight and DNA methylation of imprint regulatory elements. Epigenetics 7(7), 735-746 (2012).
66. Chen J, Li Q, Rialdi A et al. Influences of maternal stress during pregnancy on the epi/genome: comparison of placenta and umbilical cord blood. Depress. Anxiety 3(2), 1-6 (2014).
67. Vidal AC, Benjamin Neelon SE, Liu Y et al. Maternal stress, preterm birth, and DNA methylation at imprint regulatory sequences in humans. Genet. Epigenet. 6, 37-44 (2014).
68. Vangeel EB, Izzi B, Hompes T et al. DNA methylation in imprinted genes IGF2 and GNASXL is associated with prenatal maternal stress. Genes Brain Behav. 14(8), 573-582 (2015).
69. Mansell T, Novakovic B, Meyer B et al. The effects of maternal anxiety during pregnancy on IGF2/H19 methylation in cord blood. Transl. Psychiatry 6, e765 (2016).
70. Devlin AM, Brain U, Austin J, Oberlander TF. Prenatal exposure to maternal depressed mood and the MTHFR C677T variant affect SLC6A4 methylation in infants at birth. PLoS ONE 5(8), e12201 (2010).
71. Alexander N, Wankerl M, Hennig J et al. DNA methylation profiles within the serotonin transporter gene moderate the association of 5-HTTLPR and cortisol stress reactivity. Transl. Psychiatry 4, e443 (2014).
72. Cecil CA, Lysenko LJ, Jaffee SR et al. Environmental risk, Oxytocin Receptor Gene (OXTR) methylation and youth callous-unemotional traits: a 13-year longitudinal study. Mol. Psychiatry 19(10), 1071-1077 (2014).
73. Ciesielski TH, Marsit CJ, Williams SM. Maternal psychiatric disease and epigenetic evidence suggest a common biology for poor fetal growth. BMC Pregnancy Childbirth 15, 192 (2015).
74. Unternaehrer E, Bolten M, Nast I et al. Maternal adversities during pregnancy and cord blood oxytocin receptor (OXTR) DNA methylation. Soc. Cogn. Affect. Neurosci. 11(9), 1460-1470 (2016).
75. Schroeder JW, Smith AK, Brennan PA et al. DNA methylation in neonates born to women receiving psychiatric care. Epigenetics 7(4), 409-414 (2012).
76. Rodney NC, Mulligan CJ. A biocultural study of the effects of maternal stress on mother and newborn health in the Democratic Republic of Congo. Am. J. Phys. Anthropol. 155(2), 200-209 (2014).
77. Cao-Lei L, Elgbeili G, Massart R, Laplante DP, Szyf M, King S. Pregnant women's cognitive appraisal of a natural disaster affects DNA methylation in their children 13 years later: Project Ice Storm. Transl. Psychiatry 5, e515 (2015).
78. Gurnot C, Martin-Subero I, Mah SM et al. Prenatal antidepressant exposure associated with CYP2E1 DNA methylation change in neonates. Epigenetics 10(5), 361-372 (2015).
79. Nemoda Z, Massart R, Suderman M et al. Maternal depression is associated with DNA methylation changes in cord blood T lymphocytes and adult hippocampi. Transl. Psychiatry 5, e545 (2015).
80. Rijlaarsdam J, Pappa I, Walton E et al. An epigenome-wide association meta-analysis of prenatal maternal stress in neonates: a model approach for replication. Epigenetics 11(2), 140-149 (2016).
81. Alikhani-Koopaei R, Fouladkou F, Frey FJ, Frey BM. Epigenetic regulation of 11 beta-hydroxysteroid dehydrogenase type 2 expression. J. Clin. Invest. 114(8), 1146-1157 (2004).
82. Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG. Fetal programming of hypothalamopituitary-adrenal function: prenatal stress and glucocorticoids. J. Physiol. 572(Pt 1), 31-44 (2006).
83. Weaver IC, Cervoni N, Champagne FA et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7(8), 847-854 (2004).
84. Weaver IC, D'alessio AC, Brown SE et al. The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J. Neurosci. 27(7), 1756-1768 (2007).
85. Liu D, Diorio J, Tannenbaum B et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamicpituitary-adrenal responses to stress. Science 277(5332), 1659-1662 (1997).
86. Palma-Gudiel H, Cordova-Palomera A, Eixarch E, Deuschle M, Fananas L. Maternal psychosocial stress during pregnancy alters the epigenetic signature of the glucocorticoid receptor gene promoter in their offspring: a meta-analysis. Epigenetics 10(10), 893-902 (2015).
87. Marsit CJ, Maccani MA, Padbury JF, Lester BM. Placental 11-beta hydroxysteroid dehydrogenase methylation is associated with newborn growth and a measure of neurobehavioral outcome. PLoS ONE 7(3), e33794 (2012).
88. Plasschaert RN, Bartolomei MS. Genomic imprinting in development, growth, behavior and stem cells. Development 141(9), 1805-1813 (2014).
89. Li E, Beard C, Jaenisch R. Role for DNA methylation in genomic imprinting. Nature 366(6453), 362-365 (1993).
90. Delaval K, Feil R. Epigenetic regulation of mammalian genomic imprinting. Curr. Opin. Genet. Dev. 14(2), 188-195 (2004).
91. Boissonnas CC, Abdalaoui HE, Haelewyn V et al. Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur. J. Hum. Genet. 18(1), 73-80 (2010).
92. Chao W, D'amore PA. IGF2: epigenetic regulation and role in development and disease. Cytokine Growth Factor Rev. 19(2), 111-120 (2008).
93. Heijmans BT, Tobi EW, Stein AD et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl Acad. Sci. USA 105(44), 17046-17049 (2008).
94. Bouwland-Both MI, Van Mil NH, Tolhoek CP et al. Prenatal parental tobacco smoking, gene specific DNA methylation, and newborns size: the Generation R study. Clin. Epigenetics 7(1), 83 (2015).
95. Bell AC, Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405(6785), 482-485 (2000).
96. Olivier JD, Akerud H, Sundstrom Poromaa I. Antenatal depression and antidepressants during pregnancy: unraveling the complex interactions for the offspring. Eur. J. Pharmacol. 753, 257-262 (2015).
97. Whitaker-Azmitia PM, Druse M, Walker P, Lauder JM. Serotonin as a developmental signal. Behav. Brain Res. 73(1-2), 19-29 (1996).
98. Ponder KL, Salisbury A, Mcgonnigal B, Laliberte A, Lester B, Padbury JF. Maternal depression and anxiety are associated with altered gene expression in the human placenta without modification by antidepressant use: implications for fetal programming. Dev. Psychobiol. 53(7), 711-723 (2011).
99. Hempstead BL. Brain-derived neurotrophic factor: three ligands, many actions. Trans. Am. Clin. Climatol. Assoc. 126, 9-19 (2015).
100. Bocchio-Chiavetto L, Bagnardi V, Zanardini R et al. Serum and plasma BDNF levels in major depression: a replication study and meta-analyses. World J. Biol. Psychiatry 11(6), 763-773 (2010).
101. Lanfumey L, Mongeau R, Cohen-Salmon C, Hamon M. Corticosteroid-serotonin interactions in the neurobiological mechanisms of stress-related disorders. Neurosci. Biobehav. Rev. 32(6), 1174-1184 (2008).
102. Kumsta R, Hummel E, Chen FS, Heinrichs M. Epigenetic regulation of the oxytocin receptor gene: implications for behavioral neuroscience. Front. Neurosci. 7, 83 (2013).
103. Kusui C, Kimura T, Ogita K et al. DNA methylation of the human oxytocin receptor gene promoter regulates tissue-specific gene suppression. Biochem. Biophys. Res. Commun. 289(3), 681-686 (2001).
104. Lawson EA, Miller KK, Blum JI et al. Leptin levels are associated with decreased depressive symptoms in women across the weight spectrum, independent of body fat. Clin. Endocrinol. (Oxf.). 76(4), 520-525 (2012).
105. Mcgowan PO, Sasaki A, D'Alessio AC et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12(3), 342-348 (2009).
106. Van Der Knaap LJ, Riese H, Hudziak JJ et al. Glucocorticoid receptor gene (NR3C1) methylation following stressful events between birth and adolescence. the TRAILS study. Transl. Psychiatry 4, e381 (2014).
107. Novakovic B, Ryan J, Pereira N, Boughton B, Craig JM, Saffery R. Postnatal stability, tissue, and time specific effects of AHRR methylation change in response to maternal smoking in pregnancy. Epigenetics 9(3), 377-386 (2014).
108. Braig S, Grabher F, Ntomchukwu C et al. Determinants of maternal hair cortisol concentrations at delivery reflecting the last trimester of pregnancy. Psychoneuroendocrinology 52, 289-296 (2015).
109. Teh AL, Pan H, Chen L et al. The effect of genotype and in utero environment on interindividual variation in neonate DNA methylomes. Genome Res. 24(7), 1064-1074 (2014).
110. De Bruijn AT, Van Bakel HJ, Van Baar AL. Sex differences in the relation between prenatal maternal emotional complaints and child outcome. Early Hum. Dev. 85(5), 319-324 (2009).
111. Grace T, Bulsara M, Robinson M, Hands B. Early life events and motor development in childhood and adolescence: a longitudinal study. Acta Paediatr. 105(5), e219-e227 (2016).
112. Zijlmans MA, Riksen-Walraven JM, De Weerth C. Associations between maternal prenatal cortisol concentrations and child outcomes: a systematic review. Neurosci. Biobehav. Rev. 53, 1-24 (2015).
113. Huang H, Coleman S, Bridge JA, Yonkers K, Katon W. A meta-analysis of the relationship between antidepressant use in pregnancy and the risk of preterm birth and low birth weight. Gen. Hosp. Psychiatry 36(1), 13-18 (2014).
114. O'connor TG, Heron J, Glover V. Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression. J. Am. Acad. Child Adolesc. Psychiatry 41(12), 1470-1477 (2002).
115. Gentile S. SSRIs in pregnancy and lactation: emphasis on neurodevelopmental outcome. CNS Drugs 19(7), 623-633 (2005).
116. Kim J, Riggs KW, Misri S et al. Stereoselective disposition of fluoxetine and norfluoxetine during pregnancy and breastfeeding. Br. J. Clin. Pharmacol. 61(2), 155-163 (2006).
117. Pawluski JL, Brain UM, Underhill CM, Hammond GL, Oberlander TF. Prenatal SSRI exposure alters neonatal corticosteroid binding globulin, infant cortisol levels, and emerging HPA function. Psychoneuroendocrinology 37(7), 1019-1028 (2012).
118. Chiarella J, Tremblay RE, Szyf M, Provencal N, Booij L. Impact of early environment on children's mental health: lessons from DNA methylation studies with monozygotic twins. Twin Res. Hum. Genet. 18(6), 623-634 (2015).
119. Van Mil NH, Steegers-Theunissen RP, Bouwland-Both MI et al. DNA methylation profiles at birth and child ADHD symptoms. J. Psychiatr. Res. 49, 51-59 (2014).
120. Kupers LK, Xu X, Jankipersadsing SA et al. DNA methylation mediates the effect of maternal smoking during pregnancy on birthweight of the offspring. Int. J. Epidemiol. 44(4), 1224-1237 (2015).
121. Houtepen LC, Vinkers CH, Carrillo-Roa T et al. Genomewide DNA methylation levels and altered cortisol stress reactivity following childhood trauma in humans. Nat. Commun. 7, 10967 (2016).
122. Blaze J, Roth TL. Evidence from clinical and animal model studies of the long-term and transgenerational impact of stress on DNA methylation. Semin. Cell Dev. Biol. 43, 76-84 (2015).
123. Pembrey M, Saffery R, Bygren LO. Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research. J. Med. Genet. 51(9), 563-572 (2014).
124. Bergman K, Sarkar P, Glover V, O'Connor TG. Quality of child-parent attachment moderates the impact of antenatal stress on child fearfulness. J. Child Psychol. Psychiatry 49(10), 1089-1098 (2008).
125. Brotnow L, Reiss D, Stover CS et al. Expectant mothers maximizing opportunities: maternal characteristics moderate multifactorial prenatal stress in the prediction of birth weight in a sample of children adopted at birth. PLoS ONE (2015). https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4636431/