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Review

Does Maternal Mental Well-Being in Pregnancy Impact The Early Human Epigenome?

, , &
Pages 313-332 | Received 07 Sep 2016, Accepted 23 Oct 2016, Published online: 31 Jan 2017

References

  • Wiegner L , HangeD , BjorkelundC , AhlborgGJr . 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 ).
  • Woods SM , MelvilleJL , GuoY , FanMY , GavinA . Psychosocial stress during pregnancy . Am. J. Obstet. Gynecol.202 ( 1 ), 61.e61 – 67.e61 ( 2010 ).
  • Lee AM , LamSK , Sze Mun LauSM , ChongCS , ChuiHW , FongDY . Prevalence, course, and risk factors for antenatal anxiety and depression . Obstet. Gynecol.110 ( 5 ), 1102 – 1112 ( 2007 ).
  • Melville JL , GavinA , GuoY , FanMY , KatonWJ . Depressive disorders during pregnancy: prevalence and risk factors in a large urban sample . Obstet. Gynecol.116 ( 5 ), 1064 – 1070 ( 2010 ).
  • Staneva A , BogossianF , PritchardM , WittkowskiA . The effects of maternal depression, anxiety, and perceived stress during pregnancy on preterm birth: a systematic review . Women Birth28 ( 3 ), 179 – 193 ( 2015 ).
  • Grigoriadis S , VonderportenEH , MamisashviliLet al. The impact of maternal depression during pregnancy on perinatal outcomes: a systematic review and meta-analysis . J. Clin. Psychiatry74 ( 4 ), e321 – e341 ( 2013 ).
  • Jarde A , MoraisM , KingstonDet al. Neonatal outcomes in women with untreated antenatal depression compared with women without depression: a systematic review and meta-analysis . JAMA Psychiatry73 ( 8 ), 826 – 837 ( 2016 ).
  • Buss C , DavisEP , MuftulerLT , HeadK , SandmanCA . High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9-year-old children . Psychoneuroendocrinology35 ( 1 ), 141 – 153 ( 2010 ).
  • Lewis AJ , AustinE , GalballyM . Prenatal maternal mental health and fetal growth restriction: a systematic review . J. Dev. Orig. Health Dis.7 ( 4 ), 416 – 428 ( 2016 ).
  • Kingston D , McdonaldS , AustinMP , ToughS . Association between prenatal and postnatal psychological distress and toddler cognitive development: a systematic review . PLoS ONE10 ( 5 ), e0126929 ( 2015 ).
  • Weikum WM , OberlanderTF , HenschTK , WerkerJF . Prenatal exposure to antidepressants and depressed maternal mood alter trajectory of infant speech perception . Proc. Natl Acad. Sci. USA109 ( Suppl. 2 ), 17221 – 17227 ( 2012 ).
  • Laplante DP , BarrRG , BrunetAet al. Stress during pregnancy affects general intellectual and language functioning in human toddlers . Pediatr. Res.56 ( 3 ), 400 – 410 ( 2004 ).
  • Gutteling BM , De WeerthC , ZandbeltN , MulderEJ , VisserGH , BuitelaarJK . Does maternal prenatal stress adversely affect the child’s learning and memory at age six?J. Abnorm. Child Psychol.34 ( 6 ), 789 – 798 ( 2006 ).
  • Mennes M , Van Den BerghB , LagaeL , StiersP . Developmental brain alterations in 17 year old boys are related to antenatal maternal anxiety . Clin. Neurophysiol.120 ( 6 ), 1116 – 1122 ( 2009 ).
  • Sharp H , HillJ , HellierJ , PicklesA . 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 ).
  • Nulman I , KorenG , RovetJet al. Neurodevelopment of children following prenatal exposure to venlafaxine, selective serotonin reuptake inhibitors, or untreated maternal depression . Am. J. Psychiatry169 ( 11 ), 1165 – 1174 ( 2012 ).
  • Gutteling BM , De WeerthC , Willemsen-SwinkelsSHet al. The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers . Eur. Child Adolesc. Psychiatry14 ( 1 ), 41 – 51 ( 2005 ).
  • Hay DF , PawlbyS , WatersCS , PerraO , SharpD . Mothers’ antenatal depression and their children’s antisocial outcomes . Child Dev.81 ( 1 ), 149 – 165 ( 2010 ).
  • Rodriguez A , BohlinG . Are maternal smoking and stress during pregnancy related to ADHD symptoms in children?J. Child Psychol. Psychiatry46 ( 3 ), 246 – 254 ( 2005 ).
  • Van Den Bergh BR , MarcoenA . 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 ).
  • Khashan AS , AbelKM , McnameeRet al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events . Arch. Gen. Psychiatry65 ( 2 ), 146 – 152 ( 2008 ).
  • Kinney DK , MillerAM , CrowleyDJ , HuangE , GerberE . Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana . J. Autism Dev. Disord.38 ( 3 ), 481 – 488 ( 2008 ).
  • Talge NM , NealC , GloverV . Antenatal maternal stress and long-term effects on child neurodevelopment: how and why?J. Child Psychol. Psychiatry48 ( 3–4 ), 245 – 261 ( 2007 ).
  • Pawlby S , HayDF , SharpD , WatersCS , O’KeaneV . Antenatal depression predicts depression in adolescent offspring: prospective longitudinal community-based study . J. Affect. Disord.113 ( 3 ), 236 – 243 ( 2009 ).
  • Slykerman RF , ThompsonJ , WaldieK , MurphyR , WallC , MitchellEA . Maternal stress during pregnancy is associated with moderate to severe depression in 11-year-old children . Acta Paediatr.104 ( 1 ), 68 – 74 ( 2015 ).
  • Lester BM , ConradtE , MarsitCJ . Epigenetic basis for the development of depression in children . Clin. Obstet. Gynecol.56 ( 3 ), 556 – 565 ( 2013 ).
  • Hall HG , BeattieJ , LauR , EastC , Anne BiroM . Mindfulness and perinatal mental health: a systematic review . Women Birth29 ( 1 ), 62 – 71 ( 2016 ).
  • De Kloet ER , JoelsM , HolsboerF . Stress and the brain: from adaptation to disease . Nat. Rev. Neurosci.6 ( 6 ), 463 – 475 ( 2005 ).
  • Doom JR , CicchettiD , RogoschFA . Longitudinal patterns of cortisol regulation differ in maltreated and nonmaltreated children . J. Am. Acad. Child Adolesc. Psychiatry53 ( 11 ), 1206 – 1215 ( 2014 ).
  • Powers SI , LaurentHK , Gunlicks-StoesselM , BalabanS , BentE . Depression and anxiety predict sex-specific cortisol responses to interpersonal stress . Psychoneuroendocrinology69 , 172 – 179 ( 2016 ).
  • Belvederi Murri M , ParianteC , MondelliVet al. HPA axis and aging in depression: systematic review and meta-analysis . Psychoneuroendocrinology41 , 46 – 62 ( 2014 ).
  • Glover V , O’connorTG , O’donnellK . Prenatal stress and the programming of the HPA axis . Neurosci. Biobehav. Rev.35 ( 1 ), 17 – 22 ( 2010 ).
  • Novakovic B , SafferyR . The ever growing complexity of placental epigenetics – role in adverse pregnancy outcomes and fetal programming . Placenta33 ( 12 ), 959 – 970 ( 2012 ).
  • Cottrell EC , SecklJR . Prenatal stress, glucocorticoids and the programming of adult disease . Front. Behav. Neurosci.3 , 19 ( 2009 ).
  • Schoof E , GirstlM , FrobeniusWet 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 ).
  • Seth S , LewisAJ , SafferyR , LappasM , GalballyM . 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 ).
  • Baibazarova E , Van De BeekC , Cohen-KettenisPT , BuitelaarJ , SheltonKH , Van GoozenSH . Influence of prenatal maternal stress, maternal plasma cortisol and cortisol in the amniotic fluid on birth outcomes and child temperament at 3 months . Psychoneuroendocrinology38 ( 6 ), 907 – 915 ( 2013 ).
  • O’connor TG , BergmanK , SarkarP , GloverV . Prenatal cortisol exposure predicts infant cortisol response to acute stress . Dev. Psychobiol.55 ( 2 ), 145 – 155 ( 2013 ).
  • Smith AK , NewportDJ , AsheMPet al. Predictors of neonatal hypothalamic-pituitary-adrenal axis activity at delivery . Clin. Endocrinol. (Oxf.).75 ( 1 ), 90 – 95 ( 2011 ).
  • Huizink AC , BartelsM , RoseRJ , PulkkinenL , ErikssonCJ , KaprioJ . Chernobyl exposure as stressor during pregnancy and hormone levels in adolescent offspring . J. Epidemiol. Community Health62 ( 4 ), e5 ( 2008 ).
  • Van Den Bergh BR , Van CalsterB , SmitsT , Van HuffelS , LagaeL . Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood . Neuropsychopharmacology33 ( 3 ), 536 – 545 ( 2008 ).
  • Entringer S , KumstaR , HellhammerDH , WadhwaPD , WustS . Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults . Horm. Behav.55 ( 2 ), 292 – 298 ( 2009 ).
  • Stewart CP , OaksBM , LaugeroKDet 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 Childbirth15 , 346 ( 2015 ).
  • Glover V . Annual research review: prenatal stress and the origins of psychopathology: an evolutionary perspective . J. Child Psychol. Psychiatry52 ( 4 ), 356 – 367 ( 2011 ).
  • Gluckman PA , HansonMA . Developmental Origins of Health and Disease . Cambridge University Press , London, UK ( 2006 ).
  • Saffery R , NovakovicB . Epigenetics as the mediator of fetal programming of adult onset disease: what is the evidence?Acta Obstet. Gynecol. Scand.93 ( 11 ), 1090 – 1098 ( 2014 ).
  • Gluckman PD , HansonMA . Developmental origins of disease paradigm: a mechanistic and evolutionary perspective . Pediatr. Res.56 ( 3 ), 311 – 317 ( 2004 ).
  • Petronis A . Epigenetics as a unifying principle in the aetiology of complex traits and diseases . Nature465 ( 7299 ), 721 – 727 ( 2010 ).
  • Januar V , SafferyR , RyanJ . Epigenetics and depressive disorders: a review of current progress and future directions . Int. J. Epidemiol.44 ( 4 ), 1364 – 1387 ( 2015 ).
  • Joubert BR , FelixJF , YousefiPet al. DNA methylation in newborns and maternal smoking in pregnancy: genome-wide consortium meta-analysis . Am. J. Hum. Genet.98 ( 4 ), 680 – 696 ( 2016 ).
  • Joubert BR , Den DekkerHT , FelixJFet al. Maternal plasma folate impacts differential DNA methylation in an epigenome-wide meta-analysis of newborns . Nat. Commun.7 , 10577 ( 2016 ).
  • Oberlander TF , WeinbergJ , PapsdorfM , GrunauR , MisriS , DevlinAM . Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses . Epigenetics3 ( 2 ), 97 – 106 ( 2008 ).
  • Radtke KM , RufM , GunterHMet al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor . Transl. Psychiatry1 , e21 ( 2011 ).
  • Mulligan CJ , D’ErricoNC , SteesJ , HughesDA . Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight . Epigenetics7 ( 8 ), 853 – 857 ( 2012 ).
  • Conradt E , LesterBM , AppletonAA , ArmstrongDA , MarsitCJ . The roles of DNA methylation of NR3C1 and 11beta-HSD2 and exposure to maternal mood disorder in utero on newborn neurobehavior . Epigenetics8 ( 12 ), 1321 – 1329 ( 2013 ).
  • Hompes T , IzziB , GellensEet 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 ).
  • Non AL , BinderAM , KubzanskyLD , MichelsKB . Genome-wide DNA methylation in neonates exposed to maternal depression, anxiety, or SSRI medication during pregnancy . Epigenetics9 ( 7 ), 964 – 972 ( 2014 ).
  • Perroud N , RutembesaE , Paoloni-GiacobinoAet al. The Tutsi genocide and transgenerational transmission of maternal stress: epigenetics and biology of the HPA axis . World J. Biol. Psychiatry15 ( 4 ), 334 – 345 ( 2014 ).
  • Braithwaite EC , KundakovicM , RamchandaniPG , MurphySE , ChampagneFA . Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation . Epigenetics10 ( 5 ), 408 – 417 ( 2015 ).
  • Murgatroyd C , QuinnJP , SharpHM , PicklesA , HillJ . Effects of prenatal and postnatal depression, and maternal stroking, at the glucocorticoid receptor gene . Transl. Psychiatry5 , e560 ( 2015 ).
  • Kertes DA , KaminHS , HughesDA , RodneyNC , BhattS , MulliganCJ . 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 ).
  • Mansell T , VuillerminP , PonsonbyAL , CollierF , SafferyR , RyanJ . Maternal mental well-being during pregnancy and glucocorticoid receptor gene promoter methylation in the neonate . Dev. Psychopathol.28 ( 4pt2 ), 1421 – 1430 ( 2016 ).
  • Appleton AA , ArmstrongDA , LesseurCet al. Patterning in placental 11-B hydroxysteroid dehydrogenase methylation according to prenatal socioeconomic adversity . PLoS ONE8 ( 9 ), e74691 ( 2013 ).
  • Soubry A , MurphyS , HuangZet 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. Epigenetics3 , 2 ( 2012 ).
  • Liu Y , MurphySK , MurthaAPet al. Depression in pregnancy, infant birth weight and DNA methylation of imprint regulatory elements . Epigenetics7 ( 7 ), 735 – 746 ( 2012 ).
  • Chen J , LiQ , RialdiAet al. Influences of maternal stress during pregnancy on the epi/genome: comparison of placenta and umbilical cord blood . Depress. Anxiety3 ( 2 ), 1 – 6 ( 2014 ).
  • Vidal AC , Benjamin NeelonSE , LiuYet al. Maternal stress, preterm birth, and DNA methylation at imprint regulatory sequences in humans . Genet. Epigenet.6 , 37 – 44 ( 2014 ).
  • Vangeel EB , IzziB , HompesTet al. DNA methylation in imprinted genes IGF2 and GNASXL is associated with prenatal maternal stress . Genes Brain Behav.14 ( 8 ), 573 – 582 ( 2015 ).
  • Mansell T , NovakovicB , MeyerBet al. The effects of maternal anxiety during pregnancy on IGF2/H19 methylation in cord blood . Transl. Psychiatry6 , e765 ( 2016 ).
  • Devlin AM , BrainU , AustinJ , OberlanderTF . Prenatal exposure to maternal depressed mood and the MTHFR C677T variant affect SLC6A4 methylation in infants at birth . PLoS ONE5 ( 8 ), e12201 ( 2010 ).
  • Alexander N , WankerlM , HennigJet al. DNA methylation profiles within the serotonin transporter gene moderate the association of 5-HTTLPR and cortisol stress reactivity . Transl. Psychiatry4 , e443 ( 2014 ).
  • Cecil CA , LysenkoLJ , JaffeeSRet al. Environmental risk, Oxytocin Receptor Gene (OXTR) methylation and youth callous-unemotional traits: a 13-year longitudinal study . Mol. Psychiatry19 ( 10 ), 1071 – 1077 ( 2014 ).
  • Ciesielski TH , MarsitCJ , WilliamsSM . Maternal psychiatric disease and epigenetic evidence suggest a common biology for poor fetal growth . BMC Pregnancy Childbirth15 , 192 ( 2015 ).
  • Unternaehrer E , BoltenM , NastIet al. Maternal adversities during pregnancy and cord blood oxytocin receptor (OXTR) DNA methylation . Soc. Cogn. Affect. Neurosci.11 ( 9 ), 1460 – 1470 ( 2016 ).
  • Schroeder JW , SmithAK , BrennanPAet al. DNA methylation in neonates born to women receiving psychiatric care . Epigenetics7 ( 4 ), 409 – 414 ( 2012 ).
  • Rodney NC , MulliganCJ . 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 ).
  • Cao-Lei L , ElgbeiliG , MassartR , LaplanteDP , SzyfM , KingS . Pregnant women’s cognitive appraisal of a natural disaster affects DNA methylation in their children 13 years later: Project Ice Storm . Transl. Psychiatry5 , e515 ( 2015 ).
  • Gurnot C , Martin-SuberoI , MahSMet al. Prenatal antidepressant exposure associated with CYP2E1 DNA methylation change in neonates . Epigenetics10 ( 5 ), 361 – 372 ( 2015 ).
  • Nemoda Z , MassartR , SudermanMet al. Maternal depression is associated with DNA methylation changes in cord blood T lymphocytes and adult hippocampi . Transl. Psychiatry5 , e545 ( 2015 ).
  • Rijlaarsdam J , PappaI , WaltonEet al. An epigenome-wide association meta-analysis of prenatal maternal stress in neonates: a model approach for replication . Epigenetics11 ( 2 ), 140 – 149 ( 2016 ).
  • Alikhani-Koopaei R , FouladkouF , FreyFJ , FreyBM . Epigenetic regulation of 11 beta-hydroxysteroid dehydrogenase type 2 expression . J. Clin. Invest.114 ( 8 ), 1146 – 1157 ( 2004 ).
  • Kapoor A , DunnE , KostakiA , AndrewsMH , MatthewsSG . Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids . J. Physiol.572 ( Pt 1 ), 31 – 44 ( 2006 ).
  • Weaver IC , CervoniN , ChampagneFAet al. Epigenetic programming by maternal behavior . Nat. Neurosci.7 ( 8 ), 847 – 854 ( 2004 ).
  • Weaver IC , D’alessioAC , BrownSEet 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 ).
  • Liu D , DiorioJ , TannenbaumBet al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress . Science277 ( 5332 ), 1659 – 1662 ( 1997 ).
  • Palma-Gudiel H , Cordova-PalomeraA , EixarchE , DeuschleM , FananasL . Maternal psychosocial stress during pregnancy alters the epigenetic signature of the glucocorticoid receptor gene promoter in their offspring: a meta-analysis . Epigenetics10 ( 10 ), 893 – 902 ( 2015 ).
  • Marsit CJ , MaccaniMA , PadburyJF , LesterBM . Placental 11-beta hydroxysteroid dehydrogenase methylation is associated with newborn growth and a measure of neurobehavioral outcome . PLoS ONE7 ( 3 ), e33794 ( 2012 ).
  • Plasschaert RN , BartolomeiMS . Genomic imprinting in development, growth, behavior and stem cells . Development141 ( 9 ), 1805 – 1813 ( 2014 ).
  • Li E , BeardC , JaenischR . Role for DNA methylation in genomic imprinting . Nature366 ( 6453 ), 362 – 365 ( 1993 ).
  • Delaval K , FeilR . Epigenetic regulation of mammalian genomic imprinting . Curr. Opin. Genet. Dev.14 ( 2 ), 188 – 195 ( 2004 ).
  • Boissonnas CC , AbdalaouiHE , HaelewynVet al. Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men . Eur. J. Hum. Genet.18 ( 1 ), 73 – 80 ( 2010 ).
  • Chao W , D’amorePA . IGF2: epigenetic regulation and role in development and disease . Cytokine Growth Factor Rev.19 ( 2 ), 111 – 120 ( 2008 ).
  • Heijmans BT , TobiEW , SteinADet al. Persistent epigenetic differences associated with prenatal exposure to famine in humans . Proc. Natl Acad. Sci. USA105 ( 44 ), 17046 – 17049 ( 2008 ).
  • Bouwland-Both MI , Van MilNH , TolhoekCPet al. Prenatal parental tobacco smoking, gene specific DNA methylation, and newborns size: the Generation R study . Clin. Epigenetics7 ( 1 ), 83 ( 2015 ).
  • Bell AC , FelsenfeldG . Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene . Nature405 ( 6785 ), 482 – 485 ( 2000 ).
  • Olivier JD , AkerudH , Sundstrom PoromaaI . Antenatal depression and antidepressants during pregnancy: unraveling the complex interactions for the offspring . Eur. J. Pharmacol.753 , 257 – 262 ( 2015 ).
  • Whitaker-Azmitia PM , DruseM , WalkerP , LauderJM . Serotonin as a developmental signal . Behav. Brain Res.73 ( 1–2 ), 19 – 29 ( 1996 ).
  • Ponder KL , SalisburyA , McgonnigalB , LaliberteA , LesterB , PadburyJF . 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 ).
  • Hempstead BL . Brain-derived neurotrophic factor: three ligands, many actions . Trans. Am. Clin. Climatol. Assoc.126 , 9 – 19 ( 2015 ).
  • Bocchio-Chiavetto L , BagnardiV , ZanardiniRet al. Serum and plasma BDNF levels in major depression: a replication study and meta-analyses . World J. Biol. Psychiatry11 ( 6 ), 763 – 773 ( 2010 ).
  • Lanfumey L , MongeauR , Cohen-SalmonC , HamonM . Corticosteroid–serotonin interactions in the neurobiological mechanisms of stress-related disorders . Neurosci. Biobehav. Rev.32 ( 6 ), 1174 – 1184 ( 2008 ).
  • Kumsta R , HummelE , ChenFS , HeinrichsM . Epigenetic regulation of the oxytocin receptor gene: implications for behavioral neuroscience . Front. Neurosci.7 , 83 ( 2013 ).
  • Kusui C , KimuraT , OgitaKet al. DNA methylation of the human oxytocin receptor gene promoter regulates tissue-specific gene suppression . Biochem. Biophys. Res. Commun.289 ( 3 ), 681 – 686 ( 2001 ).
  • Lawson EA , MillerKK , BlumJIet 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 ).
  • Mcgowan PO , SasakiA , D’AlessioACet al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse . Nat. Neurosci.12 ( 3 ), 342 – 348 ( 2009 ).
  • Van Der Knaap LJ , RieseH , HudziakJJet al. Glucocorticoid receptor gene (NR3C1) methylation following stressful events between birth and adolescence. the TRAILS study . Transl. Psychiatry4 , e381 ( 2014 ).
  • Novakovic B , RyanJ , PereiraN , BoughtonB , CraigJM , SafferyR . Postnatal stability, tissue, and time specific effects of AHRR methylation change in response to maternal smoking in pregnancy . Epigenetics9 ( 3 ), 377 – 386 ( 2014 ).
  • Braig S , GrabherF , NtomchukwuCet al. Determinants of maternal hair cortisol concentrations at delivery reflecting the last trimester of pregnancy . Psychoneuroendocrinology52 , 289 – 296 ( 2015 ).
  • Teh AL , PanH , ChenLet al. The effect of genotype and in utero environment on interindividual variation in neonate DNA methylomes . Genome Res.24 ( 7 ), 1064 – 1074 ( 2014 ).
  • De Bruijn AT , Van BakelHJ , Van BaarAL . Sex differences in the relation between prenatal maternal emotional complaints and child outcome . Early Hum. Dev.85 ( 5 ), 319 – 324 ( 2009 ).
  • Grace T , BulsaraM , RobinsonM , HandsB . Early life events and motor development in childhood and adolescence: a longitudinal study . Acta Paediatr.105 ( 5 ), e219 – e227 ( 2016 ).
  • Zijlmans MA , Riksen-WalravenJM , De WeerthC . Associations between maternal prenatal cortisol concentrations and child outcomes: a systematic review . Neurosci. Biobehav. Rev.53 , 1 – 24 ( 2015 ).
  • Huang H , ColemanS , BridgeJA , YonkersK , KatonW . A meta-analysis of the relationship between antidepressant use in pregnancy and the risk of preterm birth and low birth weight . Gen. Hosp. Psychiatry36 ( 1 ), 13 – 18 ( 2014 ).
  • O’connor TG , HeronJ , GloverV . Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression . J. Am. Acad. Child Adolesc. Psychiatry41 ( 12 ), 1470 – 1477 ( 2002 ).
  • Gentile S . SSRIs in pregnancy and lactation: emphasis on neurodevelopmental outcome . CNS Drugs19 ( 7 ), 623 – 633 ( 2005 ).
  • Kim J , RiggsKW , MisriSet al. Stereoselective disposition of fluoxetine and norfluoxetine during pregnancy and breast-feeding . Br. J. Clin. Pharmacol.61 ( 2 ), 155 – 163 ( 2006 ).
  • Pawluski JL , BrainUM , UnderhillCM , HammondGL , OberlanderTF . Prenatal SSRI exposure alters neonatal corticosteroid binding globulin, infant cortisol levels, and emerging HPA function . Psychoneuroendocrinology37 ( 7 ), 1019 – 1028 ( 2012 ).
  • Chiarella J , TremblayRE , SzyfM , ProvencalN , BooijL . 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 ).
  • Van Mil NH , Steegers-TheunissenRP , Bouwland-BothMIet al. DNA methylation profiles at birth and child ADHD symptoms . J. Psychiatr. Res.49 , 51 – 59 ( 2014 ).
  • Kupers LK , XuX , JankipersadsingSAet al. DNA methylation mediates the effect of maternal smoking during pregnancy on birthweight of the offspring . Int. J. Epidemiol.44 ( 4 ), 1224 – 1237 ( 2015 ).
  • Houtepen LC , VinkersCH , Carrillo-RoaTet al. Genome-wide DNA methylation levels and altered cortisol stress reactivity following childhood trauma in humans . Nat. Commun.7 , 10967 ( 2016 ).
  • Blaze J , RothTL . 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 ).
  • Pembrey M , SafferyR , BygrenLO . Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research . J. Med. Genet.51 ( 9 ), 563 – 572 ( 2014 ).
  • Bergman K , SarkarP , GloverV , O’ConnorTG . Quality of child–parent attachment moderates the impact of antenatal stress on child fearfulness . J. Child Psychol. Psychiatry49 ( 10 ), 1089 – 1098 ( 2008 ).
  • Brotnow L , ReissD , StoverCSet 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/

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