Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health

Trends in Molecular Medicine

Volumn 13, Issue 7, 2007, Pages 269-277

  Meaney, Michael J ^a   Szyf, Moshe ^a   Seckl, Jonathan R ^b  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR;

ARTICLE; CARDIOVASCULAR RISK; ENVIRONMENTAL FACTOR; EPIGENETICS; FETOPLACENTAL UNIT; FETUS GROWTH; GENE EXPRESSION; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; HYPERGLYCEMIA; HYPERLIPIDEMIA; HYPERTENSION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LOW BIRTH WEIGHT; MATERNAL BEHAVIOR; MATERNAL NUTRITION; MATERNAL STRESS; METABOLIC DISORDER; NONHUMAN; PERINATAL DEVELOPMENT; PERINATAL PROGRAMMING; PRENATAL EXPOSURE; PROGENY; SIDE EFFECT;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; ADRENAL GLANDS; ANIMALS; CHROMATIN; DISEASE; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FETAL DEVELOPMENT; FETUS; GLUCOCORTICOIDS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INFANT, LOW BIRTH WEIGHT; INFANT, NEWBORN; MATERNAL-FETAL EXCHANGE; PHENOTYPE; PITUITARY-ADRENAL SYSTEM; PREGNANCY; STRESS;

EID: 34347346105     PISSN: 14714914     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmed.2007.05.003     Document Type: Article

References (90)

1. Barker D.J.P., et al. Foetal nutrition and cardiovascular disease in adult life. Lancet 341 (1993) 938-941
2. Barker D.J.P., et al. Type 2 (non-insulin dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced foetal growth. Diabetologia 36 (1993) 62-67
3. Rich-Edwards J.W., et al. Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ 315 (1997) 396-400
4. Gluckman P.D., and Hansen M.A. The developmental origins of the metabolic syndrome. Trends Endocrinol. Metab. 15 (2004) 183-187
5. Edwards C.R.W., et al. Dysfunction of the placental glucocorticoid barrier: a link between the foetal environment and adult hypertension?. Lancet 341 (1993) 355-357
6. Seckl J.R. Physiologic programming of the foetus. Clin. Perinatol. 25 (1998) 939-964
7. Matthews S.G., and Meaney M.J. Maternal adversity, vulernability and disease. In: Riecher-Rössler A., and Steiner M. (Eds). Perinatal Stress, Mood and Anxiety Disorders (2005), Karger 28-49
8. Langley-Evans S.C. Hypertension induced by foetal exposure to a maternal low-protein diet, in the rat, is prevented by pharmacological blockade of maternal glucocorticoid synthesis. J. Hypertens. 15 (1997) 537-544
9. Tangalakis K., et al. Effect of cortisol on blood pressure and vascular reactivity in the ovine foetus. Exp. Physiol. 77 (1992) 709-717
10. Berry L.M., et al. Preterm newborn lamb renal and cardiovascular responses after foetal or maternal antenatal betamethasone. Am. J. Physiol. 272 (1997) R1972-R1979
11. Reinisch J.M., et al. Prenatal exposure to prednisone in humans and animals retards intra-uterine growth. Science 202 (1978) 436-438
12. Nyirenda M.J., et al. Glucocorticoid exposure in late gestation permanently programmes rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J. Clin. Invest. 101 (1998) 2174-2181
13. French N.P., et al. Repeated antenatal corticosteroids: size at birth and subsequent development. Am. J. Obstet. Gynecol. 180 (1999) 114-121
14. Newnham J.P., and Moss T.J. Antenatal glucocorticoids and growth: single versus multiple doses in animal and human studies. Semin. Neonatol. 6 (2001) 285-292
15. Matthews S.G. Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol. Metab. 13 (2002) 373-380
16. Goland R.S., et al. Elevated levels of umbilical cord plasma corticotropin-releasing hormone in growth-retarded foetuses. J. Clin. Endocrinol. Metab. 77 (1993) 1174-1179
17. Speirs H.J., et al. Ontogeny of glucocorticoid receptor and 11 hydroxysteroid dehydrogenase type 1 gene expression identifies potential critical periods of glucocorticoid susceptibility during development. J. Endocrinol. 181 (2004) 105-116
18. Brown R.W., et al. The ontogeny of 11ßhydroxysteroid dehydrogenase type 2 and mineralocorticoid receptor gene expression reveal intricate control of glucocorticoid action in development. Endocrinology 137 (1996) 794-797
19. Sun K., et al. Differential expression of 11betahydroxysteroid dehydrogenase types 1 and 2 in human placenta and foetal membranes. J. Clin. Endocrinol. Metab. 82 (1997) 300-305
20. White P.C., et al. 11beta-Hydroxysteroid dehydrogenase and the syndrome of apparent mineralocorticoid excess. Endocr. Rev. 18 (1997) 135-156
21. Benediktsson R., et al. Placental 11β-hydroxysteroid dehydrogenase type 2 is the placental barrier to maternal glucocorticoids: ex vivo studies. Clin. Endocrinol. (Oxf.) 46 (1997) 161-166
22. Waddell B.J., et al. Tissue-specific mRNA expression of 11B-hydroxysteroid dehydrogenase types 1 and 2 and the glucocorticoid receptor within rat placenta suggest exquisite local control of glucocorticoid action. Endocrinology 139 (1998) 1517-1523
23. Venihaki M., et al. Circadian rise in maternal glucocorticoid prevents pulmonary dysplasia in foetal mice with adrenal insufficiency. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 7336-7341
24. Murphy V.E., 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. 87 (2002) 1660-1668
25. Stewart P.M., et al. Type 2 11β-hydroxysteroid dehydrogenase messenger RNA and activity in human placenta and foetal membranes: its relationship to birth weight and putative role in foetal steroidogenesis. J. Clin. Endocrinol. Metab. 80 (1995) 885-890
26. McTernan C.L., et al. Reduced placental 11 beta-hydroxysteroid dehydrogenase type 2 mRNA levels in human pregnancies complicated by intrauterine growth restriction: an analysis of possible mechanisms. J. Clin. Endocrinol. Metab. 86 (2001) 4979-4983
27. Rogerson F.M., et al. Variation in placental type 2 11beta-hydroxysteroid dehydrogenase activity is not related to birth weight or placental weight. Mol. Cell. Endocrinol. 128 (1997) 103-109
28. Benediktsson R., et al. Foetal osteocalcin levels are related to placental 11β-hydroxysteroid dehydrogenase activity. Clin. Endocrinol. (Oxf.) 42 (1995) 551-555
29. Dave-Sharma S., et al. Extensive personal experience: examination of genotype and phenotype relationships in 14 patients with apparent mineralocorticoid excess. J. Clin. Endocrinol. Metab. 83 (1998) 2244-2254
30. Holmes M.C., et al. The mother or the foetus? 11beta-hydroxysteroid dehydrogenase type 2 null mice provide evidence for direct foetal programming of behavior by endogenous glucocorticoids. J. Neurosci. 26 (2006) 3840-3844
31. Benediktsson R., et al. Glucocorticoid exposure in utero: a new model for adult hypertension. Lancet 341 (1993) 339-341
32. Dodic M., et al. Programmed hypertension: kidney, brain or both?. Trends Endocrinol. Metab. 13 (2002) 403-408
33. Lindsay R.S., et al. Inhibition of 11β-hydroxysteroid dehydrogenase in pregnant rats and the programming of blood pressure in the offspring. Hypertension 27 (1996) 1200-1204
34. Lindsay R.S., et al. Programming of glucose tolerance in the rat: role of placental 11β-hydroxysteroid dehydrogenase. Diabetologia 39 (1996) 1299-1305
35. Ortiz L.A., et al. Effect of prenatal dexamethasone on rat renal development. Kidney Int. 59 (2001) 1663-1669
36. Wintour E.M., et al. Reduced nephron number in adult sheep, hypertensive as a result of prenatal glucocorticoid treatment. J. Physiol. 549 (2003) 929-935
37. Molnar J., et al. Prenatal dexamethasone leads to both endothelial dysfunction and vasodilatory compensation in sheep. J. Physiol. 547 (2003) 61-66
38. Bian X., et al. Foetal dexamethasone exposure interferes with establishment of cardiac noradrenergic innervation and sympathetic activity. Teratology 47 (1993) 109-117
39. Langdown M.L., et al. Early growth retardation induced by excessive exposure to glucocorticoids in utero selectively increases cardiac GLUT1 protein expression and Akt/protein kinase B activity in adulthood. J. Endocrinol. 169 (2001) 11-22
40. Langdown M.L., et al. Effects of prenatal glucocorticoid exposure on cardiac calreticulin and calsequestrin protein expression during early development and in adulthood. Biochem. J. 371 (2003) 61-69
41. Lesage J., et al. Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J. Endocrinol. 181 (2004) 291-296
42. Sloboda D.M., et al. Repeated maternal glucocorticoid administration and the developing liver in foetal sheep. J. Endocrinol. 175 (2002) 535-543
43. Moss T.J., et al. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281 (2001) R960-R970
44. Rosella G., et al. Impaired suppression of gluconeogenesis induced by overexpression of a noninsulin-responsive phosphoenolpyruvate carboxykinase gene. Mol. Endocrinol. 7 (1993) 1456-1462
45. Valera A., et al. Transgenic mice overexpressing phosphoenolpyruvate carboxykinase develop non-insulin-dependent diabetes mellitus. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 9151-9154
46. Whorwood C.B., et al. Maternal undernutrition during early to midgestation programs tissue-specific alterations in the expression of the glucocorticoid receptor, 11 beta-hydroxysteroid dehydrogenase isoforms, and type 1 angiotensin II receptor in neonatal sheep. Endocrinology 142 (2001) 2854-2864
47. Cleasby M.E., et al. Programming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids. Endocrinology 144 (2003) 999-1007
48. Schubring C., et al. Levels of leptin in maternal serum, amniotic fluid, and arterial and venous cord blood: relation to neonatal and placental weight. J. Clin. Endocrinol. Metab. 82 (1997) 1480-1483
49. Koistinen H.A., et al. Leptin concentration in cord blood correlates with intrauterine growth. J. Clin. Endocrinol. Metab. 82 (1997) 3328-3330
50. Ong K.K., et al. Cord blood leptin is associated with size at birth and predicts infancy weight gain in humans. ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. J. Clin. Endocrinol. Metab. 84 (1999) 1145-1148
51. Sugden M.C., et al. Maternal glucocorticoid treatment modulates placental leptin and leptin receptor expression and materno-foetal leptin physiology during late pregnancy, and elicits hypertension associated with hyperleptinaemia in the early-growth-retarded adult offspring. Eur. J. Endocrinol. 145 (2001) 529-539
52. Smith J.T., and Waddell B.J. Leptin receptor expression in the rat placenta: changes in Ob-Ra, Ob-Rb, and Ob-Re with gestational age and suppression by glucocorticoids. Biol. Reprod. 67 (2002) 1204-1210
53. Stocker C., et al. Modulation of susceptibility to weight gain and insulin resistance in low birth weight rats by treatment of their mothers with leptin during pregnancy and lactation. Int. J. Obes. Relat. Metab. Disord. 28 (2004) 129-136
54. Vickers M.H., et al. Neonatal leptin treatment reverses developmental programming. Endocrinology 146 (2005) 4211-4216
55. Garofano A., et al. Beta-cell mass and proliferation following late foetal and early postnatal malnutrition in the rat. Diabetologia 41 (1998) 1114-1120
56. Blondeau B., et al. Glucocorticoids impair foetal beta-cell development in rats. Am. J. Physiol. Endocrinol. Metab. 281 (2001) E592-E599
57. Shen C.-N., et al. Glucocorticoids suppress beta cell development and induce hepatic metaplasia in embryonic pancreas. Biochem. J. 375 (2003) 41-50
58. Nyirenda M.J., et al. Prenatal programming of hepatocyte nuclear factor 4alpha in the rat: a key mechanism in the 'foetal origins of hyperglycaemia'?. Diabetologia 49 (2006) 1412-1420
59. Drake A.J., et al. Intergenerational consequences of foetal programming by in utero exposure to glucocorticoids in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288 (2005) R34-R38
60. Hales C.N., and Barker D.J.P. The thrifty phenotype hypothesis. Br. Med. Bull. 60 (2001) 5-20
61. Wells J.C. Parent-offspring conflict theory, signaling of need, and weight gain in early life. Q. Rev. Biol. 78 (2003) 169-202
62. Coall D.A., and Chisholm J.S. Evolutionary perspectives on pregnancy: maternal age at menarche and infant birth weight. Soc. Sci. Med. 57 (2003) 1771-1781
63. Levitt N.S., et al. Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. Neuroendocrinology 64 (1996) 412-418
64. Welberg L.A.M., et al. Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience 104 (2001) 71-79
65. McCormick C.M., et al. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res. Dev. Brain Res. 84 (1995) 55-61
66. Langley-Evans S.C., et al. Maternal protein restriction influences the programming of the rat hypothalamic-pituitaryadrenal axis. J. Nutr. 126 (1996) 1578-1585
67. Trautman P.D., et al. Effects of early prenatal dexamethasone on the cognitive and behavioral development of young children: results of a pilot study. Psychoneuroendocrinology 20 (1995) 439-449
68. Haapasalo J., and Tremblay R.E. Physically aggressive boys from ages 6 to 12: family background. Parenting behavior and prediction of delinquency. J. Consult. Clin. Psychol. 62 (1994) 1044-1052
69. Weaver I.C., et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J. Neurosci. 25 (2005) 11045-11054
70. Schulkin J., et al. Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology 23 (1998) 219-243
71. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24 (2001) 1161-1192
72. Liu D., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277 (1997) 1659-1662
73. Weaver I.C., et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7 (2004) 847-854
74. Caldji C., et al. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 5335-5340
75. Francis D., et al. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286 (1999) 1155-1158
76. Meaney M.J., et al. Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 50 (1989) 597-604
77. Mitchell J.B., et al. Serotonin regulates type II corticosteroid receptor binding in hippocampal cell cultures. J. Neurosci. 10 (1990) 1745-1752
78. Meaney M.J., et al. Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: the effects of thyroid hormones and serotonin. J. Neurosci. 20 (2000) 3926-3935
79. Szyf M., et al. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front. Neuroendocrinol. 26 (2005) 139-162
80. Weaver I.C., et al. The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J. Neurosci. 27 (2007) 1756-1768
81. McCormick J.A., et al. 5′-heterogeneity of glucocorticoid receptor mRNA is tissue-specific; differential regulation of variant promoters by early life events. Mol. Endocrinol. 14 (2000) 506-517
82. Champagne F.A., et al. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147 (2006) 2909-2915
83. Lillycrop K.A., et al. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J. Nutr. 135 (2005) 1382-1386
84. Waterland R.A., and Jirtle R.L. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition 20 (2004) 63-68
85. Mousseau T.A., and Fox C.W. Maternal Effects as Adaptations (1999), Oxford University Press
86. Waddington C.H. The Evolution of an Evolutionist (1975), Cornell University Press
87. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 25 (2002) 507-536
88. Herman J.P., et al. Central mechanisms of stress integration: hierarchicial circuitry controlling hypothalamic-pituitary-adrenal responsiveness. Frts. Front. Neuroendocrinol. 24 (2003) 151-180
89. De Kloet E.R., et al. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19 (1998) 269-301
90. Bird A.P., and Wolffe A.P. Methylation-induced repression - Belts, Braces, and Chromatin. Cell 99 (1999) 451-454