Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-26T11:59:18.914Z Has data issue: false hasContentIssue false

Behavioral epigenetics and the developmental origins of child mental health disorders

Published online by Cambridge University Press:  03 July 2012

B. M. Lester*
Affiliation:
Brown Center for the Study of Children at Risk at Women and Infants Hospital of Rhode Island, Warren Alpert Medical School of Brown University, Providence, RI, USA Department of Psychiatry and Human Behavior, Warren Alpert Medical School of Brown University, Providence, RI, USA Department of Pediatrics, Warren Alpen Medical School of Brown University, Providence, RI, USA Department of Pediatrics, Women and Infants Hospital of Rhode Island, Providence, RI, USA
C. J. Marsit
Affiliation:
Departments of Pharmacology & Toxicology and Community & Family Medicine, Geisel School of Medicine at Dartmouth, Hanover, NH, USA
E. Conradt
Affiliation:
Brown Center for the Study of Children at Risk at Women and Infants Hospital of Rhode Island, Warren Alpert Medical School of Brown University, Providence, RI, USA Department of Pediatrics, Women and Infants Hospital of Rhode Island, Providence, RI, USA
C. Bromer
Affiliation:
Department of Neuroscience, Brown University, Providence, RI, USA
J. F. Padbury
Affiliation:
Department of Pediatrics, Warren Alpen Medical School of Brown University, Providence, RI, USA Department of Pediatrics, Women and Infants Hospital of Rhode Island, Providence, RI, USA
*
*Address for correspondence: Dr B. Lester, Department of Pediatrics, Brown Center for Children, Women and Infants Hospital, 101 Dudley Street, Providence, RI, 02905 USA. (E-mails [email protected]

Abstract

Advances in understanding the molecular basis of behavior through epigenetic mechanisms could help explain the developmental origins of child mental health disorders. However, the application of epigenetic principles to the study of human behavior is a relatively new endeavor. In this paper we discuss the ‘Developmental Origins of Health and Disease’ including the role of fetal programming. We then review epigenetic principles related to fetal programming and the recent application of epigenetics to behavior. We focus on the neuroendocrine system and develop a simple heuristic stress-related model to illustrate how epigenetic changes in placental genes could predispose the infant to neurobehavioral profiles that interact with postnatal environmental factors potentially leading to mental health disorders. We then discuss from an ‘Evo-Devo’ perspective how some of these behaviors could also be adaptive. We suggest how elucidation of these mechanisms can help to better define risk and protective factors and populations at risk.

Type
Review
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Barker, DJ, Osmond, C, Rodin, I, Fall, CH, Winter, PD. Low weight gain in infancy and suicide in adult life. BMJ. 1995; 311, 1203.CrossRefGoogle ScholarPubMed
2.Gluckman, PD, Hanson, MA. Living with the past: evolution, development, and patterns of disease. Science. 2004; 305, 17331736.CrossRefGoogle ScholarPubMed
3.Welberg, LA, Seckl, JR. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol. 2001; 13, 113128.CrossRefGoogle ScholarPubMed
4.Barker, DJ, Osmond, C. Low birth weight and hypertension. BMJ. 1988; 297, 134135.CrossRefGoogle ScholarPubMed
5.Barker, DJ, Winter, PD, Osmond, C, Margetts, B, Simmonds, SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 577580.CrossRefGoogle ScholarPubMed
6.Barker, D. Mothers, Babies and Health in Later Life, 1998. Churchill Livingstone: Edinburgh and New York.Google Scholar
7.Gluckman, PD, Hanson, MA. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res. 2004; 56, 311317.CrossRefGoogle ScholarPubMed
8.Barker, DJ. Fetal programming of coronary heart disease. Trends Endocrinol Metab. 2002; 13, 364368.CrossRefGoogle ScholarPubMed
9.Barker, DJ, Osmond, C, Golding, J, Kuh, D, Wadsworth, ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989; 298, 564567.CrossRefGoogle ScholarPubMed
10.Falkner, B. Birth weight as a predictor of future hypertension. Am J Hypertens. 2002; 15(Pt 2), 43S45S.CrossRefGoogle ScholarPubMed
11.Hales, CN, Barker, DJ, Clark, PM, et al.Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991; 303, 10191022.CrossRefGoogle ScholarPubMed
12.McMillen, IC, Robinson, JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005; 85, 571633.CrossRefGoogle ScholarPubMed
13.Pfister, HP, Muir, JL. Prenatal exposure to predictable and unpredictable novelty stress and oxytocin treatment affects offspring development and behavior in rats. Int J Neurosci. 1992; 62, 227241.CrossRefGoogle ScholarPubMed
14.Rich-Edwards, J, Colditz, G, Stampfer, M, et al.Birthweight and the risk for type 2 diabetes mellitus in adult women. Ann Intern Med. 1999; 130, 278284.CrossRefGoogle ScholarPubMed
15.Sallout, B, Walker, M. The fetal origin of adult diseases. J Obstet Gynaecol. 2003; 23, 555560.CrossRefGoogle ScholarPubMed
16.Stein, CE, Fall, CH, Kumaran, K, et al. Fetal growth and coronary heart disease in south India. Lancet. 1996; 348, 12691273.CrossRefGoogle ScholarPubMed
17.Allin, M, Rooney, M, Cuddy, M, et al. Personality in young adults who are born preterm. Pediatrics. 2006; 117, 309316.CrossRefGoogle ScholarPubMed
18.Gale, CR, Martyn, CN. Birth weight and later risk of depression in a national birth cohort. Br J Psychiatry. 2004; 184, 2833.CrossRefGoogle Scholar
19.Thompson, C, Syddall, H, Rodin, I, Osmond, C, Barker, DJ. Birth weight and the risk of depressive disorder in late life. Br J Psychiatry. 2001; 179, 450455.CrossRefGoogle ScholarPubMed
20.Wals, M, Reichart, CG, Hillegers, MH, et al. Impact of birth weight and genetic liability on psychopathology in children of bipolar parents. J Am Acad Child Adolesc Psychiatry. 2003; 42, 11161121.CrossRefGoogle ScholarPubMed
21.Cannon, TD, Rosso, IM. Levels of analysis in etiological research on schizophrenia. Dev Psychopathol. 2002; 14, 653666.CrossRefGoogle ScholarPubMed
22.Alati, R, Lawlor, DA, Mamun, AA, et al. Is there a fetal origin of depression? Evidence from the Mater University Study of Pregnancy and its Outcomes. Am J Epidemiol. 2007; 165, 575582.CrossRefGoogle Scholar
23.Cheung, YB. Early origins and adult correlates of psychosomatic distress. Soc Sci Med. 2002; 55, 937948.CrossRefGoogle ScholarPubMed
24.Cheung, YB, Khoo, KS, Karlberg, J, Machin, D. Association between psychological symptoms in adults and growth in early life: longitudinal follow up study. BMJ. 2002; 325, 749.CrossRefGoogle ScholarPubMed
25.Wiles, NJ, Peters, TJ, Leon, DA, Lewis, G. Birth weight and psychological distress at age 45–51 years: results from the Aberdeen Children of the 1950s cohort study. Br J Psychiatry. 2005; 187, 2128.CrossRefGoogle ScholarPubMed
26.Schlotz, W, Phillips, DI. Fetal origins of mental health: evidence and mechanisms. Brain Behav Immun. 2009; 23, 905916.CrossRefGoogle ScholarPubMed
27.Ravelli, AC, van Der Meulen, JH, Osmond, C, Barker, DJ, Bleker, OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr. 1999; 70, 811816.CrossRefGoogle ScholarPubMed
28.Ravelli, GP, Stein, ZA, Susser, MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med. 1976; 295, 349353.CrossRefGoogle ScholarPubMed
29.Van Ijzendoorn, M, Bakermans-Kranenburg, M, Ebstein, R. Methylation matters in child development: toward developmental behavioral epigenetics. Child Dev Perspect. 2011; 5, 305310.CrossRefGoogle Scholar
30.Van den Bergh, BRH. Developmental programming of early brain and behavior development and mental health: a conceptual framework. Dev Med Child Neurol. 2011; 53, 1923.CrossRefGoogle Scholar
31.Waddington, C. Organisers and Genes, 1940. Cambridge University Press: Cambridge, UK.Google Scholar
32.Van Speybroeck, L. From epigenesis to epigenetics. The case of C.H. Waddington. Ann N Y Acad Sci. 2002; 981, 6181.CrossRefGoogle ScholarPubMed
33.Bird, A. Perceptions of epigenetics. Nature. 2007; 447, 396398.CrossRefGoogle ScholarPubMed
34.World Health Organization. Promoting optimal fetal development: report of a technical consultation. Retrieved 19 April 2012 from http://www.who.int/nutrition/topics/fetal_dev_report_EN.pdfGoogle Scholar
35.Waterland, RA, Jirtle, RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol. 2003; 23, 52935300.CrossRefGoogle ScholarPubMed
36.Lillycrop, K, Phillips, E, Jackson, A, Hanson, M, Burdge, G. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005; 135, 13821386.CrossRefGoogle ScholarPubMed
37.Deal, RB, Henikoff, JG, Henikoff, S. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science. 2010; 328, 11611164.CrossRefGoogle ScholarPubMed
38.Lester, BM, Tronick, E, Nestler, E, et al. Behavioral epigenetics. Ann N Y Acad Sci. 2011; 1226, 1433.CrossRefGoogle ScholarPubMed
39.Oberlander, TF, Weinberg, J, Papsdorf, M, et al. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics. 2008; 3, 97106.CrossRefGoogle ScholarPubMed
40.Essex, MJ, Thomas Boyce, W, Hertzman, C, et al. Epigenetic vestiges of early developmental adversity: childhood stress exposure and DNA methylation in adolescence. Child Dev. 2011. Epub, doi:10.1111/j.1467-8624.2011.01641.xGoogle ScholarPubMed
41.Lester, B, Padbury, J. The third pathophysiology of prenatal cocaine exposure. Special Issue Dev Neurosci. 2009; 31, 2335.Google ScholarPubMed
42.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. 2012; 7, e33794.CrossRefGoogle Scholar
43.Bromer, C, Marsit, C, Padbury, J, Lester, B. Genetic and epigenetic variation of the glucocorticoid receptor (NR3C1) in placenta and neurobehavior. Dev Psychobiol. 2004; 160, 854860.Google Scholar
44.Marsit, CJ, Lambertini, L, Maccani, MA, et al. Placenta-imprinted gene expression association of infant neurobehavior. J Pediatr. 2011.Google ScholarPubMed
45.Gitau, R, Cameron, A, Fisk, NM, Glover, V. Fetal exposure to maternal cortisol. Lancet. 1998; 352, 707708.CrossRefGoogle ScholarPubMed
46.Matthews, S. Early programming of the hypothalamo–pituitary–adrenal axis. Trends Endocrinol Metab. 2002; 13, 373380.CrossRefGoogle ScholarPubMed
47.Padbury, JF, Martinez, AM. Sympathoadrenal system activity at birth: integration of postnatal adaptation. Semin Perinatol. 1988; 12, 163172.Google ScholarPubMed
48.Matthews, S. Antenatal glucocorticoids and the developing brain: mechanisms of action. Semin Neonatal. 2001; 6, 309317.CrossRefGoogle ScholarPubMed
49.Slone-Wilcoxon, J, Redei, EE. Maternal-fetal glucocorticoid milieu programs hypothalamic–pituitary–thyroid function of adult offspring. Endocrinology. 2004; 145, 40684072.CrossRefGoogle ScholarPubMed
50.Slotkin, TA, Orband-Miller, L, Queen, KL, Whitmore, WL, Seidler, FJ. Effects of prenatal nicotine exposure on biochemical development of rat brain regions: maternal drug infusions via osmotic minipumps. J Pharmacol Exp Ther. 1987; 240, 602611.Google ScholarPubMed
51.Williams, MT, Hennessy, MB, Davis, HN. Stress during pregnancy alters rat offspring morphology and ultrasonic vocalizations. Physiol Behav. 1998; 63, 337343.CrossRefGoogle ScholarPubMed
52.Haussmann, MF, Carroll, JA, Weesner, GD, et al. Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamic–pituitary–adrenal (HPA) axis. J Anim Sci. 2000; 78, 23992411.CrossRefGoogle ScholarPubMed
53.Griffin, WC, Skinner, HD, Salm, AK, Birkle, DL. Mild prenatal stress in rats is associated with enhanced conditioned fear. Physiol Behav. 2003; 79, 209215.CrossRefGoogle ScholarPubMed
54.French, NP, Hagan, R, Evans, SF, Mullan, A, Newnham, JP. Repeated antenatal corticosteroids: effects on cerebral palsy and childhood behavior. Am J Obstet Gynecol. 2004; 190, 588595.CrossRefGoogle ScholarPubMed
55.Lou, H, Hansen, C, Nordentoft, M, et al.Prenatal stressors of human life affect fetal brain development. Dev Med Child Neurol. 1994; 36, 826832.CrossRefGoogle ScholarPubMed
56.Rieger, M, Pirke, KM, Buske-Kirschbaum, A, et al. Influence of stress during pregnancy on HPA activity and neonatal behavior. Ann N Y Acad Sci. 2004; 1032, 228230.CrossRefGoogle ScholarPubMed
57.Van den Bergh, BRH. The influence of maternal emotions during pregnancy on fetal and neonatal behavior. J Prenat Perinat Psychol Health. 1990; 5, 119130.Google Scholar
58.Van den Bergh, BRH. Maternal emotions during pregnancy and fetal and neonatal behavior. In Fetal Behavior: Developmental and Perinatal Aspects (ed. Nijhuis J), 1992; pp. 157178. Oxford University Press: Oxford, UK.Google Scholar
59.Van den Bergh, BRH, Mulder, EJH, Mennesa, M, Glover, V. Antenatal maternal anxiety and stress and neurobehavioral development of the fetus and child: links and possible mechanisms: a review. Neurosci Biobehav Rev. 2005; 29, 237258.CrossRefGoogle ScholarPubMed
60.Van den Bergh, BRH, Van Calster, B, Smits, T, Van Huffel, S, Lagae, L. 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. Neuropsychopharmacology. 2008; 33, 536545.CrossRefGoogle ScholarPubMed
61.Lester, BM, Lagasse, LL, Shankaran, S, et al. Prenatal cocaine exposure related to cortisol stress reactivity in 11-year-old children. J Pediatr. 2010; 157, 288295 e1.CrossRefGoogle ScholarPubMed
62.Bauer, CR, Lambert, BL, Bann, CM, et al. Long-term impact of maternal substance use during pregnancy and extrauterine environmental adversity: stress hormone levels of preadolescent children. Pediatr Res. 2011; 70, 213219.CrossRefGoogle ScholarPubMed
63.Fisher, P, Kim, H, Bruce, J, Pears, K. Cumulative effects of prenatal substance exposure and early adversity on foster children's HPA axis reactivity during a psychosocial stressor. Int J Behav Dev. 2011; 36, 2935.CrossRefGoogle ScholarPubMed
64.Barbazanges, A, Piazza, PV, Le Moal, M, Maccari, S. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci. 1996; 16, 39433949.CrossRefGoogle ScholarPubMed
65.Henry, C, Kabbaj, M, Simon, H, Le Moal, M, Maccari, S. Prenatal stress increases the hypothalamo–pituitary–adrenal axis response in young and adult rats. J Neuroendocrinol. 1994; 6, 341345.CrossRefGoogle ScholarPubMed
66.Henry, C, Kabbaj, M, Simon, H, LeMoal, M, Maccari, S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress induced corticosterone secretion. J Neuroendocrinol. 1994; 6, 341345.CrossRefGoogle Scholar
67.Maccari, S, Piazza, PV, Kabbaj, M, et al.Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci. 1995; 15(Pt 1), 110116.CrossRefGoogle ScholarPubMed
68.Vallee, M, Mayo, W, Dellu, F, et al.Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci. 1997; 17, 26262636.CrossRefGoogle ScholarPubMed
69.Fride, E, Dan, Y, Feldon, J, Halevy, G, Weinstock, M. Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav. 1986; 37, 681687.CrossRefGoogle ScholarPubMed
70.Poltyrev, T, Keshet, GI, Kay, G, Weinstock, M. Role of experimental conditions in determining differences in exploratory behavior of prenatally stressed rats. Dev Psychobiol. 1996; 29, 453462.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
71.Wakshlak, A, Weinstock, M. Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol Behav. 1990; 48, 289292.CrossRefGoogle ScholarPubMed
72.Takahashi, LK, Haglin, C, Kalin, NH. Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats. Physiol Behav. 1992; 51, 319323.CrossRefGoogle ScholarPubMed
73.Takahashi, LK, Turner, JG, Kalin, NH. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Res. 1992; 574, 131137.CrossRefGoogle ScholarPubMed
74.Lambert, KG, Kinsley, CH, Jones, HE, et al.Prenatal stress attenuates ulceration in the activity stress paradigm. Physiol Behav. 1995; 57, 989994.CrossRefGoogle ScholarPubMed
75.Weller, A, Glaubman, H, Yehuda, S, Caspy, T, Ben-Uria, Y. Acute and repeated gestational stress affect offspring learning and activity in rats. Physiol Behav. 1988; 43, 139143.CrossRefGoogle ScholarPubMed
76.Hayashi, A, Nagaoka, M, Yamada, K, et al. Maternal stress induces synaptic loss and developmental disabilities of offspring. Int J Dev Neurosci. 1998; 16, 209216.CrossRefGoogle ScholarPubMed
77.Szuran, T, Zimmermann, E, Welzl, H. Water maze performance and hippocampal weight of prenatally stressed rats. Behav Brain Res. 1994; 65, 153155.CrossRefGoogle ScholarPubMed
78.Vallee, M, MacCari, S, Dellu, F, et al.Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat. Eur J Neurosci. 1999; 11, 29062916.CrossRefGoogle ScholarPubMed
79.Meaney, M, Seckl, J. Glucocorticoid programming. Ann N Y Acad Sci. 2004; 1032, 6384.Google Scholar
80.Roughton, EC, Schneider, ML, Bromley, LJ, Coe, CL. Maternal endocrine activation during pregnancy alters neurobehavioral state in primate infants. Am J Occup Ther. 1998; 52, 9098.CrossRefGoogle Scholar
81.Schneider, ML, Moore, CF, Kraemer, GW. Moderate level alcohol during pregnancy, prenatal stress, or both and limbic–hypothalamic–pituitary–adrenocortical axis response to stress in rhesus monkeys. Child Dev. 2004; 75, 96109.CrossRefGoogle ScholarPubMed
82.Schneider, ML. Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Dev Psychobiol. 1992; 25, 529540.CrossRefGoogle ScholarPubMed
83.McEwen, BS. Glucocorticoid–biogenic amine interactions in relation to mood and behavior. Biochem Pharmacol. 1987; 36, 17551763.CrossRefGoogle ScholarPubMed
84.Maes, M, Meltzer, HY, D'Hondt, P, Cosyns, P, Blockx, P. Effects of serotonin precursors on the negative feedback effects of glucocorticoids on hypothalamic–pituitary–adrenal axis function in depression. Psychoneuroendocrinology. 1995; 20, 149167.CrossRefGoogle ScholarPubMed
85.Meador-Woodruff, JH, Greden, JF, Grunhaus, L, Haskett, RF. Severity of depression and hypothalamic–pituitary–adrenal axis dysregulation: identification of contributing factors. Acta Psychiatr Scand. 1990; 81, 364371.CrossRefGoogle ScholarPubMed
86.Nemeroff, CB, Widerlov, E, Bissette, G, et al. Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science. 1984; 226, 13421344.CrossRefGoogle ScholarPubMed
87.van Praag, H. Depression. Lancet. 1982; 8310, 12591264.CrossRefGoogle Scholar
88.Wadhwa, PD, Garite, TJ, Porto, M, et al. Placental corticotropin-releasing hormone (CRH), spontaneous preterm birth, and fetal growth restriction: a prospective investigation. Am J Obstet Gynecol. 2004; 191, 10631069.CrossRefGoogle ScholarPubMed
89.Wadhwa, PD, Sandman, CA, Garite, TJ. The neurobiology of stress in human pregnancy: implications for prematurity and development of the fetal central nervous system. Prog Brain Res. 2001; 133, 131142.CrossRefGoogle ScholarPubMed
90.Kajantie, E, Raikkonen, K. Early life predictors of the physiological stress response later in life. Neurosci Biobehav Rev. 2010; 35, 2332.CrossRefGoogle ScholarPubMed
91.van Os, J, Selten, J. Prenatal exposure to maternal stress and subsequent schizophrenia. Br J Psychiatry. 1998; 172, 324326.CrossRefGoogle ScholarPubMed
92.Field, T. Stress and coping from pregnancy through the postnatal period. In Life-Span Developmental Psychology: Perspectives on Stress and Coping (ed. Cummings E), 1991; pp. 4559. Lawrence Erlbaum Associates: Hillsdale, NJ, USA.Google Scholar
93.Huizink, AC, Robles de Medina, PG, Mulder, EJ, Visser, GH, Buitelaar, JK. Stress during pregnancy is associated with developmental outcome in infancy. J Child Psychol Psychiatry. 2003; 44, 810818.CrossRefGoogle ScholarPubMed
94.Levy-Shiff, R, Dimitrovsky, L, Shulman, S, Har-Even, D. Cognitive appraisals, coping strategies, and support resources as correlates of parenting and infant development. Dev Psychol. 1998; 34, 14171427.CrossRefGoogle ScholarPubMed
95.Meijer, A. Child psychiatric sequelae of maternal war stress. Acta Psychiatr Scand. 1985; 72, 505511.CrossRefGoogle ScholarPubMed
96.Stott, DH. Follow-up study from birth of the effects of prenatal stresses. Dev Med Child Neurol. 1973; 15, 770787.CrossRefGoogle ScholarPubMed
97.Ward, AJ. Prenatal stress and childhood psychopathology. Child Psychiatry Hum Dev. 1991; 22, 97110.CrossRefGoogle ScholarPubMed
98.DePietro, J. The role of prenatal maternal stress in child development. Curr Dir Psychol Sci. 2004; 13, 7174.CrossRefGoogle Scholar
99.Bremner, JD, Randall, P, Vermetten, E, et al.Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse – a preliminary report. Biol Psychiatry. 1997; 41, 2332.CrossRefGoogle ScholarPubMed
100.McEwen, BS. Protective and damaging effects of stress mediators. N Engl J Med. 1998; 338, 171179.CrossRefGoogle ScholarPubMed
101.McEwen, BS. Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev. 2003; 9, 149154.CrossRefGoogle ScholarPubMed
102.Felitti, V, Anda, R, Nordenberg, D, et al.The relationship of adult health status to childhood abuse and household dysfunction. J Prev Med. 1998; 14, 42454258.Google ScholarPubMed
103.Meyer, JS. Biochemical effects of corticosteroids on neural tissues. Physiol Rev. 1985; 65, 9461020.CrossRefGoogle ScholarPubMed
104.Lopez Bernal, A, Craft, IL. Corticosteroid metabolism in vitro by human placenta, fetal membranes and decidua in early and late gestation. Placenta. 1981; 2, 279285.CrossRefGoogle ScholarPubMed
105.Benediktsson, R, Lindsay, RS, Noble, J, Seckl, JR, Edwards, CR. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet. 1993; 341, 339341.CrossRefGoogle ScholarPubMed
106.McTernan, CL, Draper, N, Nicholson, H, et al.Reduced placental 11beta-hydroxysteroid dehydrogenase type 2 mRNA levels in human pregnancies complicated by intrauterine growth restriction: an analysis of possible mechanisms. J Clin Endocrinol Metab. 2001; 86, 49794983.Google Scholar
107.Murphy, VE, Zakar, T, Smith, R, et al.Reduced 11beta-hydroxysteroid dehydrogenase type 2 activity is associated with decreased birth weight centile in pregnancies complicated by asthma. J Clin Endocrinol Metab. 2002; 87, 16601668.Google ScholarPubMed
108.Shams, M, Kilby, MD, Somerset, DA, et al.11beta-hydroxysteroid dehydrogenase type 2 in human pregnancy and reduced expression in intrauterine growth restriction. Hum Reprod. 1998; 13, 799804.CrossRefGoogle Scholar
109.Stewart, P, Roberson, F, Mason, J. Type 2 11-hydroxysteroid dehydrogenase messenger RNA and activity in human placenta and fetal membranes: its relationship to birth weight and putative role in fetal steroidogenesis. J Clin Endocrinol Metab. 1995; 80, 885890.Google Scholar
110.Holmes, MC, Abrahamsen, CT, French, KL, et al.The mother or the fetus? 11beta-hydroxysteroid dehydrogenase type 2 null mice provide evidence for direct fetal programming of behavior by endogenous glucocorticoids. J Neurosci. 2006; 26, 38403844.CrossRefGoogle ScholarPubMed
111.Dave-Sharma, S, Wilson, R, Harbison, M. Extensive personal experience: examination of genotype and phenotype relationships in 14 patients with apparent mineralocorticoid excess. J Clin Endocrinol Metab. 1998; 83, 22442254.Google Scholar
112.Seckl, JR, Cleasby, M, Nyirenda, MJ. Glucocorticoids, 11beta-hydroxysteroid dehydrogenase, and fetal programming. Kidney Int. 2000; 57, 14121417.CrossRefGoogle ScholarPubMed
113.Edwards, CR, Benediktsson, R, Lindsay, RS, Seckl, JR. Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet. 1993; 341, 355357.CrossRefGoogle ScholarPubMed
114.Seckl, JR. Glucocorticoids, feto-placental 11 beta-hydroxysteroid dehydrogenase type 2, and the early life origins of adult disease. Steroids. 1997; 62, 8994.CrossRefGoogle Scholar
115.Bohn, MC. Granule cell genesis in the hippocampus of rats treated neonatally with hydrocortisone. Neuroscience. 1980; 5, 20032012.CrossRefGoogle ScholarPubMed
116.Gould, E, Woolley, CS, Cameron, HA, Daniels, DC, McEwen, BS. Adrenal steroids regulate postnatal development of the rat dentate gyrus: II. Effects of glucocorticoids and mineralocorticoids on cell birth. J Comp Neurol. 1991; 313, 486493.CrossRefGoogle ScholarPubMed
117.Gould, E, Woolley, CS, McEwen, BS. Adrenal steroids regulate postnatal development of the rat dentate gyrus: I. Effects of glucocorticoids on cell death. J Comp Neurol. 1991; 313, 479485.CrossRefGoogle ScholarPubMed
118.Sarkar, S, Tsai, S, Nguyen, T, Plevyak, M, Padbury, J. Inhibition of placental 11β-hydroxysteroid dehydrogenase type 2 by catecholamines via α-adrenergic signaling. Am J Physiol Regul Integr Comp Physiol. 2001; 281, R1966R1974.CrossRefGoogle Scholar
119.Bottalico, B, Larsson, I, Brodszki, J, et al.Norepinephrine transporter (NET), serotonin transporter (SERT), vesicular monoamine transporter (VMAT2) and organic cation transporters (OCT1, 2 and EMT) in human placenta from pre-eclamptic and normotensive pregnancies. Placenta. 2004; 25, 518529.CrossRefGoogle ScholarPubMed
120.Bzoskie, L, Yen, J, Tseng, YT, et al.Human placental norepinephrine transporter mRNA: expression and correlation with fetal condition at birth. Placenta. 1997; 18, 205210.CrossRefGoogle ScholarPubMed
121.Alikhani-Koopaei, R, Fouladkou, F, Frey, FJ, Frey, BM. Epigenetic regulation of 11 beta-hydroxysteroid dehydrogenase type 2 expression. J Clin Invest. 2004; 114, 11461157.CrossRefGoogle ScholarPubMed
122.Friso, S, Pizzolo, F, Choi, SW, et al.Epigenetic control of 11 beta-hydroxysteroid dehydrogenase 2 gene promoter is related to human hypertension. Atherosclerosis. 2008; 199, 323327.CrossRefGoogle ScholarPubMed
123.Alikhani-Koupaei, R, Fouladkou, F, Fustier, P, et al.Identification of polymorphisms in the human 11beta hydroxysteroid dehydrogenase type 2 gene promoter: functional characterization and relevance for salt sensitivity. FASEB J. 2007; 21, 111.CrossRefGoogle ScholarPubMed
124.Zanchi, N, Filho, M, Felitti, V, et al.Glucocorticoids: extensive physiological actions modulated through multiple mechanisms of gene regulation. J Cell Physiol. 2010; 224, 311315.CrossRefGoogle ScholarPubMed
125.Yudt, MR, Cidlowski, JA. The glucocorticoid receptor: coding a diversity of proteins and responses through a single gene. Mol Endocrinol. 2002; 16, 17191726.CrossRefGoogle ScholarPubMed
126.Johnson, RF, Rennie, N, Murphy, V, et al.Expression of glucocorticoid receptor messenger ribonucleic acid transcripts in the human placenta at term. J Clin Endocrinol Metab. 2008; 93, 48874893.CrossRefGoogle ScholarPubMed
127.Meaney, MJ, Szyf, M. Maternal care as a model for experience-dependent chromatin plasticity? Trends Neurosci. 2005; 28, 456463.CrossRefGoogle Scholar
128.Weaver, IC, Cervoni, N, Champagne, FA, et al.. Epigenetic programming by maternal behavior. Nat Neurosci. 2004; 7, 847854.CrossRefGoogle ScholarPubMed
129.Liu, D, Diorio, J, Day, JC, Francis, DD, Meaney, MJ. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci. 2000; 3, 799806.CrossRefGoogle ScholarPubMed
130.Mark, PJ, Augustus, S, Lewis, JL, Hewitt, DP, Waddell, BJ. Changes in the placental glucocorticoid barrier during rat pregnancy: impact on placental corticosterone levels and regulation by progesterone. Biol Reprod. 2009; 80, 12091215.CrossRefGoogle ScholarPubMed
131.Yiallourides, M, Sebert, SP, Wilson, V, et al.The differential effects of the timing of maternal nutrient restriction in the ovine placenta on glucocorticoid sensitivity, uncoupling protein 2, peroxisome proliferator-activated receptor-gamma and cell proliferation. Reproduction. 2009; 138, 601608.CrossRefGoogle ScholarPubMed
132.Filiberto, AC, Maccani, MA, Koestler, D, et al.Birthweight is associated with DNA promoter methylation of the glucocorticoid receptor in human placenta. Epigenetics. 2011; 6, 566572.CrossRefGoogle ScholarPubMed
133.Lester, BM, Tronick, EZ. The Neonatal Intensive Care Unit Network Neurobehavioral Scale (NNNS). Pediatrics (Supplement). 2004; 113, 631699.Google Scholar
134.El-Dib, M, Massaro, AN, Glass, P, Aly, H. Neurobehavioral assessment as a predictor of neurodevelopmental outcome in preterm infants. J Perinatol. 2011; 32, 299303.CrossRefGoogle ScholarPubMed
135.Stephens, BE, Liu, J, Lester, B, et al.Neurobehavioral assessment predicts motor outcome in preterm infants. J Pediatr. 2010; 156, 366371.CrossRefGoogle ScholarPubMed
136.Liu, J, Bann, C, Lester, B, et al.Neonatal neurobehavior predicts medical and behavioral outcome. Pediatrics. 2010; 125, e90e98.CrossRefGoogle ScholarPubMed
137.Houseman, EA, Christensen, BC, Yeh, RF, et al.Model-based clustering of DNA methylation array data: a recursive-partitioning algorithm for high-dimensional data arising as a mixture of beta distributions. BMC Bioinformatics. 2008; 9 365.CrossRefGoogle Scholar
138.Calkins, S, Hill, A. Caregiver influences on emerging emotion regulation: biological and environmental transactions in early development. In Handbook of Emotion Regulation (ed. Gross J), 2007; pp. 229248. The Guilford Press: New York, NY, USA.Google Scholar
139.Cohn, JF, Tronick, E. Specificity of infants’ response to mothers’ affective behavior. J Am Acad Child Adolesc Psychiatry. 1989; 28, 242248.CrossRefGoogle ScholarPubMed
140.Tronick, E. The neurobehavioral and social-emotional development of infants and children, 2007. W.W. Norton & Company: New York, NY, USA.Google Scholar
141.Fracasso, M, Lamb, M, Scholmerich, A, Leyendecker, B. The ecology of mother–infant interaction in Euroamerican and immigrant central American families living in the United States. Int J Behav Dev. 1997; 20, 207218.CrossRefGoogle Scholar
142.Chess, S, Thomas, A. Temperament and the concept of goodness of fit. In Explorations in Temperament (eds. Strelau J, Angleitner A), 1991, 15–28. Plenum: New York.Google Scholar
143.Lester, B, Boukydis, C, Garcia-Coll, C, et al.Developmental outcome as a function of the goodness of fit between the infant's cry characteristics and the mother's perception of her infant's cry. Pediatrics. 1995; 95, 516521.CrossRefGoogle ScholarPubMed
144.Maziade, M. Should adverse temperament matter to the clinician? An empirically based answer. In Temperament in Childhood (eds. Kohnstamm G, Bates JE, Rothbart M), 1989; pp. 263281. Wiley: New York, NY, USA.Google Scholar
145.Van den Boom, D. The influence of temperament and mothering on attachment and exploration: an experimental manipulation of sensitive responsiveness among lower-class mothers with irritable infants. Child Dev. 1994; 65, 14591477.Google ScholarPubMed
146.Spangler, G, Grossmann, KE. Biobehavioral organization in securely and insecurely attached infants. Child Dev. 1993; 64, 14391450.CrossRefGoogle ScholarPubMed
147.Gunnar, M. Psychoendocrine study of temperament and stress in early childhood: expanding current models. In Temperament: Individual Differences at the Interface of Biology and Behavior (eds. Bates J, Wachs TD), 1994; pp. 175198. American Psychological Association Press: New York.CrossRefGoogle Scholar
148.Haley, DW, Stansbury, K. Infant stress and parent responsiveness: regulation of physiology and behavior during still-face and reunion. Child Dev. 2003; 74, 15341546.CrossRefGoogle ScholarPubMed
149.Harwood, K, McLean, N, Durkin, K. First-time mothers’ expectations of parenthood: What happens when optimistic expectations are not matched by later experiences? Dev Psychol. 2007; 43, 112.CrossRefGoogle Scholar
150.Hofer, MA. Evolutionary basis of adaptation in resilience and vulnerability: response to Cicchetti and Blender. Ann N Y Acad Sci. 2006; 1094, 259262.CrossRefGoogle ScholarPubMed
151.Carroll, S. Endless Forms Most Beautiful: The New Science of Evo-Devo, 2005. W.W. Norton & Company: New York.Google Scholar
152.Cameron, NM, Champagne, FA, Parent, C, et al.The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev. 2005; 29, 843865.CrossRefGoogle ScholarPubMed
153.Boyce, WT, Ellis, BJ. Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol. 2005; 17, 271301.CrossRefGoogle ScholarPubMed
154.Pluess, M, Belsky, J. Prenatal programming of postnatal plasticity? Dev Psychopathol. 2011; 23, 2938.CrossRefGoogle ScholarPubMed
155.Harper, LV. Epigenetic inheritance and the intergenerational transfer of experience. Psychol Bull. 2005; 131, 340360.CrossRefGoogle ScholarPubMed
156.Whitelaw, NC, Whitelaw, E. How lifetimes shape epigenotype within and across generations. Hum Mol Genet. 2006; 15 (Spec No. 2), R131R137.CrossRefGoogle Scholar
157.Belsky, J. War, trauma and children's development: observations from a modern evolutionary perspective. Int J Behav Dev. 2008; 32, 260271.CrossRefGoogle Scholar