Home LiteratureArticle Details
PMID: 24863383 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Glucocorticoids and fetal programming part 2: Mechanisms.

Nature reviews. Endocrinology ·Vol. 10 ·No. 7 ·2014-07-00 ·Pages 403-11

Moisiadis VG, Matthews SG

Abstract

The lifelong health of an individual is shaped during critical periods of development. The fetus is particularly susceptible to internal and external stimuli, many of which can alter developmental trajectories and subsequent susceptibility to disease. Glucocorticoids are critical in normal development of the fetus, as they are involved in the growth and maturation of many organ systems. The surge in fetal glucocorticoid levels that occurs in most mammalian species over the last few days of pregnancy is an important developmental switch leading to fundamental changes in gene regulation in many organs, including the brain. These changes are important for the transition to postnatal life. Exposure of the fetus to increased levels of glucocorticoids, resulting from maternal stress or treatment with synthetic glucocorticoids, can lead to long-term 'programming' of hypothalamic-pituitary-adrenal function and behaviours. Glucocorticoids act at multiple levels within the fetal brain. Growing evidence indicates that they can exert powerful effects on the epigenome, including on DNA methylation, histone acetylation and microRNA, to influence gene expression. Such influences probably represent a critical component of the 'programming' process, and might be partly responsible for the transgenerational effects of antenatal glucocorticoid exposure on neurologic, cardiovascular and metabolic function.

MeSH Terms
Animals Brain/embryology DNA Methylation/drug effects Epigenesis, Genetic Female Fetal Development/drug effects Gene Expression Regulation, Developmental/drug effects Glucocorticoids/physiology Humans Hypothalamo-Hypophyseal System/embryology Maternal-Fetal Exchange Pituitary-Adrenal System/drug effects,embryology Pregnancy Prenatal Exposure Delayed Effects/physiopathology Receptors, Glucocorticoid/metabolism Stress, Psychological/complications
Chemicals
Glucocorticoids Receptors, Glucocorticoid
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Moisiadis Vasilis G
Department of Physiology, University of Toronto, Medical Sciences Building, 1 King's College Circle, Toronto, ON M5S 1A8, Canada.
Matthews Stephen G
Departments of Obstetrics and Gynaecology, Medicine and Physiology, University of Toronto, Medical Sciences Building, 1 King's College Circle, Toronto, ON M5S 1A8, Canada.
References (83)
83 references, click to expand
  1. Glucocorticoid programming of the fetal male hippocampal epigenome.
    Endocrinology. 2013 Mar;154(3):1168-80 PMID: 23389956
  2. Neonatal exposure to low dose corticosterone persistently modulates hippocampal mineralocorticoid receptor expression and improves locomotor/exploratory behaviour in a mouse model of Rett syndrome.
    Neuropharmacology. 2013 May;68:174-83 PMID: 22709945
  3. Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects.
    Endocrinology. 2012 Jul;153(7):3269-83 PMID: 22564977
  4. Genomic DNA methylation: the mark and its mediators.
    Trends Biochem Sci. 2006 Feb;31(2):89-97 PMID: 16403636
  5. Structural determinants of P-glycoprotein-mediated transport of glucocorticoids.
    Pharm Res. 2003 Nov;20(11):1794-803 PMID: 14661924
  6. Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis.
    J Androl. 2006 Nov-Dec;27(6):868-79 PMID: 16837734
  7. Effects of antenatal synthetic glucocorticoid on glucocorticoid receptor binding, DNA methylation, and genome-wide mRNA levels in the fetal male hippocampus.
    Endocrinology. 2013 Nov;154(11):4170-81 PMID: 24029241
  8. Endocrine and paracrine regulation of birth at term and preterm.
    Endocr Rev. 2000 Oct;21(5):514-50 PMID: 11041447
  9. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation.
    J Neurosci. 2013 May 22;33(21):9003-12 PMID: 23699511
  10. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse.
    Nat Neurosci. 2009 Mar;12(3):342-8 PMID: 19234457
  11. Glucocorticoids and fetal programming part 1: Outcomes.
    Nat Rev Endocrinol. 2014 Jul;10(7):391-402 PMID: 24863382
  12. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring.
    J Nutr. 2005 Jun;135(6):1382-6 PMID: 15930441
  13. Epigenetic effects of prenatal stress on 11β-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain.
    PLoS One. 2012;7(6):e39791 PMID: 22761903
  14. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses.
    Epigenetics. 2008 Mar-Apr;3(2):97-106 PMID: 18536531
  15. Developmental regulation of the 5-HT7 serotonin receptor and transcription factor NGFI-A in the fetal guinea-pig limbic system: influence of GCs.
    J Physiol. 2004 Mar 16;555(Pt 3):659-70 PMID: 14724213
  16. Transgenerational epigenetic effects on brain functions.
    Biol Psychiatry. 2013 Feb 15;73(4):313-20 PMID: 23062885
  17. An unbalanced maternal diet in pregnancy associates with offspring epigenetic changes in genes controlling glucocorticoid action and foetal growth.
    Clin Endocrinol (Oxf). 2012 Dec;77(6):808-15 PMID: 22642564
  18. Hypomethylation of the serotonin receptor type-2A Gene (HTR2A) at T102C polymorphic site in DNA derived from the saliva of patients with schizophrenia and bipolar disorder.
    Am J Med Genet B Neuropsychiatr Genet. 2011 Jul;156B(5):536-45 PMID: 21598376
  19. Hyperhomocysteinemia in patients with Cushing's syndrome.
    J Clin Endocrinol Metab. 2004 Aug;89(8):3745-51 PMID: 15292300
  20. 11β-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action.
    Physiol Rev. 2013 Jul;93(3):1139-206 PMID: 23899562
  21. Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: the effects of thyroid hormones and serotonin.
    J Neurosci. 2000 May 15;20(10):3926-35 PMID: 10804232
  22. DNA hypomethylation of MB-COMT promoter in the DNA derived from saliva in schizophrenia and bipolar disorder.
    J Psychiatr Res. 2011 Nov;45(11):1432-8 PMID: 21820670
  23. Neuroprotection provided by dietary restriction in rats is further enhanced by reducing glucocortocoids.
    Neurobiol Aging. 2012 Oct;33(10):2398-410 PMID: 22226488
  24. Proopiomelanocortin gene expression and DNA methylation: implications for Cushing's syndrome and beyond.
    J Endocrinol. 2003 Jun;177(3):365-72 PMID: 12773116
  25. Corticosteroid regulation of P-glycoprotein in the developing blood-brain barrier.
    Endocrinology. 2011 Mar;152(3):1067-79 PMID: 21239442
  26. Short periods of prenatal stress affect growth, behaviour and hypothalamo-pituitary-adrenal axis activity in male guinea pig offspring.
    J Physiol. 2005 Aug 1;566(Pt 3):967-77 PMID: 15932885
  27. Understanding transgenerational epigenetic inheritance via the gametes in mammals.
    Nat Rev Genet. 2012 Jan 31;13(3):153-62 PMID: 22290458
  28. Differential glucocorticoid receptor exon 1(B), 1(C), and 1(H) expression and methylation in suicide completers with a history of childhood abuse.
    Biol Psychiatry. 2012 Jul 1;72(1):41-8 PMID: 22444201
  29. Epigenetic regulation of 11 beta-hydroxysteroid dehydrogenase type 2 expression.
    J Clin Invest. 2004 Oct;114(8):1146-57 PMID: 15489962
  30. Changes in placental CRH, urocortins, and CRH-receptor mRNA expression associated with preterm delivery and chorioamnionitis.
    J Clin Endocrinol Metab. 2011 Feb;96(2):534-40 PMID: 21106714
  31. Regulation of glucocorticoid receptor mRNA and heat shock protein 70 mRNA in the developing sheep brain.
    Brain Res. 2000 Sep 29;878(1-2):174-82 PMID: 10996148
  32. Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans.
    Neuropsychopharmacology. 2013 Jan;38(1):111-23 PMID: 22968814
  33. Repeated antenatal glucocorticoid treatment decreases hypothalamic corticotropin releasing hormone mRNA but not corticosteroid receptor mRNA expression in the fetal guinea-pig brain.
    J Neuroendocrinol. 2001 May;13(5):425-31 PMID: 11328452
  34. Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance?
    Proc Nutr Soc. 1998 Feb;57(1):113-22 PMID: 9571716
  35. What obesity research tells us about epigenetic mechanisms.
    Philos Trans R Soc Lond B Biol Sci. 2013 Jan 5;368(1609):20110337 PMID: 23166398
  36. Transient cyclical methylation of promoter DNA.
    Nature. 2008 Mar 6;452(7183):112-5 PMID: 18322535
  37. Elevation in S-adenosylhomocysteine and DNA hypomethylation: potential epigenetic mechanism for homocysteine-related pathology.
    J Nutr. 2002 Aug;132(8 Suppl):2361S-2366S PMID: 12163693
  38. The physiological relevance of glucocorticoid endangerment of the hippocampus.
    Ann N Y Acad Sci. 1994 Nov 30;746:294-304; discussion 304-7 PMID: 7825884
  39. Pregnant women become insensitive to cold stress.
    BMC Pregnancy Childbirth. 2002 Nov 19;2(1):8 PMID: 12437774
  40. Sex-specificity in transgenerational epigenetic programming.
    Horm Behav. 2011 Mar;59(3):290-5 PMID: 20483359
  41. Maternal undernutrition programs tissue-specific epigenetic changes in the glucocorticoid receptor in adult offspring.
    Endocrinology. 2013 Dec;154(12):4560-9 PMID: 24064364
  42. Placental drug transporters and their role in fetal protection.
    Placenta. 2012 Mar;33(3):137-42 PMID: 22265855
  43. Antenatal glucocorticoids and programming of the developing CNS.
    Pediatr Res. 2000 Mar;47(3):291-300 PMID: 10709726
  44. Infantile experience and resistance to physiological stress.
    Science. 1957 Aug 30;126(3270):405 PMID: 13467220
  45. Reduced telomerase activity in human T lymphocytes exposed to cortisol.
    Brain Behav Immun. 2008 May;22(4):600-5 PMID: 18222063
  46. Sex-specific programming of offspring emotionality after stress early in pregnancy.
    J Neurosci. 2008 Sep 3;28(36):9055-65 PMID: 18768700
  47. Sexually dimorphic effects of maternal nutrient reduction on expression of genes regulating cortisol metabolism in fetal baboon adipose and liver tissues.
    Diabetes. 2013 Apr;62(4):1175-85 PMID: 23238295
  48. Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight.
    Epigenetics. 2012 Aug;7(8):853-7 PMID: 22810058
  49. Dynamics of telomerase activity in response to acute psychological stress.
    Brain Behav Immun. 2010 May;24(4):531-9 PMID: 20018236
  50. Molecular regulation of the hypothalamic-pituitary-adrenal axis in adult male guinea pigs after prenatal stress at different stages of gestation.
    J Physiol. 2008 Sep 1;586(17):4317-26 PMID: 18635650
  51. Psychological stress and aging: role of glucocorticoids (GCs).
    Age (Dordr). 2012 Dec;34(6):1421-33 PMID: 21971999
  52. Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length.
    Proc Biol Sci. 2012 Apr 7;279(1732):1447-56 PMID: 22072607
  53. Review: Sex and the human placenta: mediating differential strategies of fetal growth and survival.
    Placenta. 2010 Mar;31 Suppl:S33-9 PMID: 20004469
  54. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model.
    Biol Psychiatry. 2006 Jun 15;59(12):1227-35 PMID: 16457784
  55. Homocysteine inhibits arterial endothelial cell growth through transcriptional downregulation of fibroblast growth factor-2 involving G protein and DNA methylation.
    Circ Res. 2008 Apr 25;102(8):933-41 PMID: 18309099
  56. Epigenetic programming by maternal behavior.
    Nat Neurosci. 2004 Aug;7(8):847-54 PMID: 15220929
  57. Epigenetic transgenerational inheritance of altered stress responses.
    Proc Natl Acad Sci U S A. 2012 Jun 5;109(23):9143-8 PMID: 22615374
  58. Maternal high-fat diet effects on third-generation female body size via the paternal lineage.
    Endocrinology. 2011 Jun;152(6):2228-36 PMID: 21447631
  59. Epigenetic effects of glucocorticoids.
    Semin Fetal Neonatal Med. 2009 Jun;14(3):143-50 PMID: 19217839
  60. A longitudinal study of plasma and urinary cortisol in pregnancy and postpartum.
    J Clin Endocrinol Metab. 2011 May;96(5):1533-40 PMID: 21367926
  61. Glucocorticoid-induced DNA demethylation and gene memory during development.
    EMBO J. 2001 Apr 17;20(8):1974-83 PMID: 11296230
  62. Epigenetic Biomarkers as Predictors and Correlates of Symptom Improvement Following Psychotherapy in Combat Veterans with PTSD.
    Front Psychiatry. 2013 Sep 27;4:118 PMID: 24098286
  63. Hypomethylation of MB-COMT promoter is a major risk factor for schizophrenia and bipolar disorder.
    Hum Mol Genet. 2006 Nov 1;15(21):3132-45 PMID: 16984965
  64. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life.
    J Neurosci. 2005 Nov 23;25(47):11045-54 PMID: 16306417
  65. The effects of psychosomatic stress at the end of pregnancy on maternal and fetal plasma cortisol levels and liver glycogen in guinea-pigs.
    Reprod Nutr Dev. 1984;24(1):45-51 PMID: 6709956
  66. Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids.
    Brain Res Rev. 2008 Mar;57(2):586-95 PMID: 17716742
  67. Altered placental methyl donor transport in the dexamethasone programmed rat.
    Placenta. 2012 Mar;33(3):220-3 PMID: 22226642
  68. Placental programming of chronic diseases, cancer and lifespan: a review.
    Placenta. 2013 Oct;34(10):841-5 PMID: 23916422
  69. Genomic sequencing reveals a positive correlation between the kinetics of strand-specific DNA demethylation of the overlapping estradiol/glucocorticoid-receptor binding sites and the rate of avian vitellogenin mRNA synthesis.
    Proc Natl Acad Sci U S A. 1986 Oct;83(19):7167-71 PMID: 3463957
  70. Differential effects of maternal dexamethasone treatment on circulating thyroid hormone concentrations and tissue deiodinase activity in the pregnant ewe and fetus.
    Endocrinology. 2007 Feb;148(2):800-5 PMID: 17110425
  71. Epigenetic dysregulation of HTR2A in the brain of patients with schizophrenia and bipolar disorder.
    Schizophr Res. 2011 Jul;129(2-3):183-90 PMID: 21550210
  72. Child health, developmental plasticity, and epigenetic programming.
    Endocr Rev. 2011 Apr;32(2):159-224 PMID: 20971919
  73. Maternal stress induces epigenetic signatures of psychiatric and neurological diseases in the offspring.
    PLoS One. 2013;8(2):e56967 PMID: 23451123
  74. Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development.
    Cell. 2013 Sep 26;155(1):81-93 PMID: 24074862
  75. Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk.
    Endocr Rev. 2013 Dec;34(6):885-916 PMID: 23970762
  76. Renal mineralocorticoid receptors and hippocampal corticosterone-binding species have identical intrinsic steroid specificity.
    Proc Natl Acad Sci U S A. 1983 Oct;80(19):6056-60 PMID: 6310613
  77. Maternal choline intake alters the epigenetic state of fetal cortisol-regulating genes in humans.
    FASEB J. 2012 Aug;26(8):3563-74 PMID: 22549509
  78. Prenatal stress changes the glycoprotein GPM6A gene expression and induces epigenetic changes in rat offspring brain.
    Epigenetics. 2014 Jan;9(1):152-60 PMID: 23959066
  79. 11beta-hydroxysteroid dehydrogenase type 1 deficiency prevents memory deficits with aging by switching from glucocorticoid receptor to mineralocorticoid receptor-mediated cognitive control.
    J Neurosci. 2011 Mar 16;31(11):4188-93 PMID: 21411659
  80. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage.
    J Neurosci. 2011 Aug 17;31(33):11748-55 PMID: 21849535
  81. Stress and hippocampal plasticity.
    Annu Rev Neurosci. 1999;22:105-22 PMID: 10202533
  82. Expression of the multidrug resistance P-glycoprotein, (ABCB1 glycoprotein) in the human placenta decreases with advancing gestation.
    Placenta. 2006 Jun-Jul;27(6-7):602-9 PMID: 16143395
  83. The pregnane X receptor: a promiscuous xenobiotic receptor that has diverged during evolution.
    Mol Endocrinol. 2000 Jan;14(1):27-39 PMID: 10628745
Article Info
Journal
Nature reviews. Endocrinology
Abbr.
Nat Rev Endocrinol
ISSN
1759-5037
Published
2014-07-00
Epub
2014-00-27
Pages
403-11
Language
English
Region
England
NLM ID
101500078
Subset
IM
Grants
Canadian Institutes of Health Research · 126166 · Canada
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]