Glucocorticoid programming of the fetal male hippocampal epigenome

Endocrinology

Volumn 154, Issue 3, 2013, Pages 1168-1180

  Crudo, Ariann ^a   Suderman, Matthew ^a,b   Moisiadis, Vasilis G ^c   Petropoulos, Sophie ^a   Kostaki, Alisa ^c   Hallett, Michael ^b   Szyf, Moshe ^a   Matthews, Stephen G ^c,d  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETAMETHASONE; GLUCOCORTICOID; HISTONE H3; HYDROCORTISONE; SYNTHETIC GLUCOCORTICOID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FEMALE; FETUS; FETUS DEVELOPMENT; GENETIC ASSOCIATION; GESTATION PERIOD; GUINEA PIG; HIPPOCAMPUS; HISTONE ACETYLATION; HYDROCORTISONE BLOOD LEVEL; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROMOTER REGION;

ANIMALS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FETAL DEVELOPMENT; FETUS; GLUCOCORTICOIDS; GUINEA PIGS; HIPPOCAMPUS; HISTONES; HYDROCORTISONE; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; PROMOTER REGIONS, GENETIC; RNA, MESSENGER;

EID: 84874584901     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1980     Document Type: Article

References (65)

1. Liggins GC, Howie RN. A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics. 1972;50:515-525.
2. Kapoor A, Petropoulos S, Matthews SG. Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain Res Rev. 2008;57:586-595.
3. Owen D, Matthews SG. Glucocorticoids and sex-dependent development of brain glucocorticoid and mineralocorticoid receptors. Endocrinology. 2003;144:2775-2784.
4. Owen D, Banjanin S, Gidrewicz D, McCabe L, Matthews SG. Central regulation of the hypothalamic-pituitary-adrenal axis during fetal development in the Guinea-pig. J Neuroendocrinol. 2005;17: 220-226.
5. Andrews MH, Matthews SG. Regulation of glucocorticoid receptor mRNA and heat shock protein 70 mRNA in the developing sheep brain. Brain Res. 2000;878:174-182.
6. Sloboda DM, Moss TJ, Gurrin LC, Newnham JP, Challis Jr. The effect of prenatal betamethasone administration on postnatal ovine hypothalamic-pituitary- adrenal function. J. Endocrinol. 2002;172: 71-81.
7. Uno H, Eisele S, Sakai A, et al. Neurotoxicity of glucocorticoids in the primate brain. Horm Behav. 1994;28:336-348.
8. Liu L, Li A, Matthews SG. Maternal glucocorticoid treatment programs HPA regulation in adult offspring: Sex-specific effects. Am J Physiol Endocrinol Metab. 2001;280:E729-E739.
9. Levitt NS, Lindsay RS, HolmesMC,Seckl Jr. 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. 1996;64:412-418.
10. 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;190:588-595.
11. Glover V. Annual research review: Prenatal stress and the origins of psychopathology: An evolutionary perspective. J Child Psychol Psychiatry. 2011;52:356-367.
12. SzyfM,Weaver IC, Champagne FA, Diorio J, Meaney MJ. Maternal programming of steroid receptor expression and phenotype through DNAmethylation in the rat. Front Neuroendocrinol. 2005;26:139-162.
13. Weaver IC, Champagne FA, Brown SE, et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: Altering epigenetic marking later in life. J Neurosci. 2005;25:11045-11054.
14. Weaver IC, Cervoni N, Champagne FA, et al. 2004 Epigenetic programming by maternal behavior. Nat Neurosci 7:847-854.
15. Weaver IC, Diorio J, Seckl JR, Szyf M, Meaney MJ. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: Characterization of intracellular mediators and potential genomic target sites. Ann NY Acad Sci. 2004;1024:182-212.
16. McGowan PO, Sasaki A, D'Alessio AC, et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009;12:342-348.
17. Wade PA, Pruss D, Wolffe AP. Histone acetylation: Chromatin in action. Trends Biochem Sci. 1997;22:128-132.
18. Jenuwein T. Re-SET-ting heterochromatin by histone methyltransferases. Trends Cell Biol. 2001;11:266-273.
19. Razin A, Riggs AD. DNA methylation and gene function. Science. 1980;210:604-610.
20. Razin A. CpG methylation, chromatin structure and gene silencing-a three-way connection. Embo J. 1998;17:4905-4908.
21. Perry M, Chalkley R. Histone acetylation increases the solubility of chromatin and occurs sequentially over most of the chromatin. A novel model for the biological role of histone acetylation. J Biol Chem. 1982;257:7336-7347.
22. D'Alessio AC, Szyf M. Epigenetic tete-a-tete: The bilateral relationship between chromatin modifications and DNA methylation. Biochem Cell Biol. 2006;84:463-476.
23. NanX,NgHH,Johnson CA, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex [see comments]. Nature. 1998;393:386-389.
24. Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet. 2000;24:88-91.
25. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T. Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. Embo J. 2001;20:2536-2544.
26. Dobbing J, Sands J. Growth and development of the brain and spinal cord of the guinea pig. Brain Res. 1970;17:115-123.
27. Owen D, Matthews SG. Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function in juvenile guinea pigs. J Neuroendocrinol. 2007;19:172-180.
28. Dunn E, Kapoor A, Leen J, Matthews SG. Prenatal synthetic glucocorticoid exposure alters hypothalamic-pituitary-adrenal regulation and pregnancy outcomes in mature female guinea pigs. J Physiol. 2010;588:887-899.
29. Setiawan E, Jackson MF, MacDonald JF, Matthews SG. Effects of repeated prenatal glucocorticoid exposure on long-term potentiation in the juvenile guinea-pig hippocampus. J. Physiol. 2007;581:1033-1042.
30. Iqbal M, Moisiadis VG, Kostaki A, Matthews SG. Transgenerational effects of prenatal synthetic glucocorticoids on hypothalamicpituitary-adrenal function. Endocrinology. 2012;153:3295-3307.
31. Crudo A, Petropoulos S, Moisiadis VG, et al. Prenatal synthetic glucocorticoid treatment changesDNAmethylation States in male organ systems: Multigenerational effects. Endocrinology. 2012;153:3269-3283.
32. Weaver IC, Meaney MJ, Szyf M. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci USA. 2006;103:3480-3485.
33. Dean F, Matthews SG. Maternal dexamethasone treatment in late gestation alters glucocorticoid and mineralocorticoid receptor mRNA in the fetal guinea pig brain. Brain Res. 1999;846:253-259.
34. Owen D, Matthews SG. Repeated maternal glucocorticoid treatment affects activity and hippocampal NMDA receptor expression in juvenile guinea pigs. J Physiol. 2007;578:249-257.
35. Keightley MC, Fuller PJ. Cortisol resistance and the guinea pig glucocorticoid receptor. Steroids. 1995;60:87-92.
36. Brown SE, Szyf M. Dynamic epigenetic states of ribosomal RNA promoters during the cell cycle. Cell Cycle. 2008;7:382-390.
37. Crane-Robinson C, Myers FA, Hebbes TR, Clayton AL, Thorne AW. Chromatin immunoprecipitation assays in acetylation mapping of higher eukaryotes. Methods Enzymol. 1999;304:533-547.
38. Weaver IC, Cervoni N, Champagne FA, et al. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7:847-854.
39. Agilent Technologies. 2010 Agilent Mammalian ChIP-on-chip Protocol.
40. Team RDC. 2007 R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
41. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003;19:185-193.
42. Borghol N, SudermanM,McArdleW,et al. Associations with earlylife socio-economic position in adult DNA methylation. Int J Epidemiol. 2012;41:62-74.
43. Clark SJ, Harrison J, Paul CL, Frommer M. High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 1994;22:2990-2997.
44. Drake AJ, Raubenheimer PJ, Kerrigan D, McInnes KJ, Seckl JR, Walker BR. Prenatal dexamethasone programs expression of genes in liver and adipose tissue and increased hepatic lipid accumulation but not obesity on a high-fat diet. Endocrinology. 2010;151:1581-1587.
45. Challis JRG, Matthews SG, Gibb W, Lye SJ. Endocrine and paracrine regulation of birth at term and preterm. Endocr Rev. 2000; 21:514-550.
46. Thomassin H, Flavin M, Espinas ML, Grange T. Glucocorticoidinduced DNA demethylation and gene memory during development. EMBO J. 2001;20:1974-1983.
47. Dalle M, Delost P. Plasma and adrenal cortisol concentrations in foetal, newborn and mother guinea-pigs during the perinatal period. J Endocrinol. 1976;70:207-214.
48. Dy J, Guan H, Sampath-Kumar R, Richardson BS, Yang K. Placental 11α-hydroxysteroid dehydrogenase type 2 is reduced in pregnancies complicated with idiopathic intrauterine growth restriction: Evidence that this is associated with an attenuated ratio of cortisone to cortisol in the umbilical artery. Placenta. 2008;29:193-200.
49. 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;80:1209-1215.
50. Borzsonyi B, Demendi C, Pajor A, et al. Gene expression patterns of the 11beta-hydroxysteroid dehydrogenase 2 enzyme in human placenta from intrauterine growth restriction: The role of impaired fetomaternal glucocorticoid metabolism. Eur J Obstet Gynecol Reprod Biol. 2012;161:12-17.
51. Fisher DA, Klein AH. Thyroid development and disorders of thyroid function in the newborn. N Engl J Med. 1981;304:702-712.
52. De Vries LS, Heckmatt JZ, Burrin JM, Dubowitz LM, Dubowitz V. Low serum thyroxine concentrations and neural maturation in preterm infants. Arch Dis Child. 1986;61:862-866.
53. Martin CR, Van Marter LJ, Allred EN, Leviton A. Antenatal glucocorticoids increase early total thyroxine levels in premature infants. Biol Neonate. 2005;87:273-280.
54. Krozowski ZS, Funder JW. Renal mineralocorticoid receptors and hippocampal corticosterone-binding species have identical intrinsic steroid specificity. Proc Natl Acad Sci USA. 1983;80:6056-6060.
55. Kliewer SA, Lehmann JM, Milburn MV, Willson TM. The PPARs and PXRs: Nuclear xenobiotic receptors that define novel hormone signaling pathways. Recent Prog Horm Res. 1999;54:345-367; discussion 367-348.
56. Langdown ML, Smith ND, Sugden MC, Holness MJ. Excessive glucocorticoid exposure during late intrauterine development modulates the expression of cardiac uncoupling proteins in adult hypertensive male offspring. Pflugers Arch. 2001;442:248-255.
57. Bian X, Seidler FJ, Slotkin TA. Fetal dexamethasone exposure interferes with establishment of cardiac noradrenergic innervation and sympathetic activity. Teratology. 1993;47:109-117.
58. Bian XP, Seidler FJ, Slotkin TA. Promotional role for glucocorticoids in the development of intracellular signalling: Enhanced cardiac and renal adenylate cyclase reactivity to beta-adrenergic and non-adrenergic stimuli after low-dose fetal dexamethasone exposure. J Dev Physiol. 1992;17:289-297.
59. Koenen SV, Mecenas CA, Smith GS, Jenkins S, Nathanielsz PW. Effects of maternal betamethasone administration on fetal and maternal blood pressure and heart rate in the baboon at 0.7 of gestation. Am J Obstet Gynecol. 2002;186:812-817.
60. Langdown ML, Holness MJ, Sugden MC. 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. 2001;169:11-22.
61. Sugden MC, Langdown ML, Munns MJ, Holness MJ. Maternal glucocorticoid treatment modulates placental leptin and leptin receptor expression and materno-fetal leptin physiology during late pregnancy, and elicits hypertension associated with hyperleptinaemia in the early-growth-retarded adult offspring. Eur J Endocrinol. 2001;145:529-539.
62. Matthews SG. Antenatal glucocorticoids and programming of the developing CNS. Pediatr Res. 2000;47:291-300.
63. Meaney MJ, Diorio J, Francis D, et al. Early environmental regulation of forebrain glucocorticoid receptor gene expression: Implications for adrenocortical responses to stress. Dev Neurosci. 1996;18:49-72.
64. Truss M, Beato M. Steroid hormone receptors: Interaction with deoxyribonucleic acid and transcription factors. Endocr Rev. 1993; 14:459-479.
65. Kassel O, Herrlich P. Crosstalk between the glucocorticoid receptor and other transcription factors: Molecular aspects. Mol Cell Endocrinol. 2007;275:13-29.