Effects of antenatal synthetic glucocorticoid on glucocorticoid receptor binding, DNA methylation, and genome-wide mRNA levels in the fetal male hippocampus

Endocrinology

Volumn 154, Issue 11, 2013, Pages 4170-4181

  Crudo, Ariann ^a   Petropoulos, Sophie ^a   Suderman, Matthew ^a,b   Moisiadis, Vasilis G ^c   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

DNA; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; DNA BINDING; DNA METHYLATION; FETUS; GENE EXPRESSION; GENOME; GESTATION PERIOD; GUINEA PIG; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

ANIMALS; BETAMETHASONE; DNA METHYLATION; FEMALE; FETAL DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; GLUCOCORTICOIDS; GUINEA PIGS; HIPPOCAMPUS; MALE; PREGNANCY; PROTEIN BINDING; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER; TRANSCRIPTOME;

EID: 84886454386     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1484     Document Type: Article

References (53)

1. 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.
2. 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.
3. National Institutes of Health Consensus Development Panel 2001 Antenatal corticosteroids revisited: repeat courses-National Institutes of Health Consensus Development Conference Statement, August 17-18, 2000. Obstet Gynecol 98: 144-150.
4. SlobodaDM,Moss TJ, Gurrin LC,NewnhamJP, Challis JR The effect of prenatal betamethasone administration on postnatal ovine hypothalamic- pituitary-adrenal function. J Endocrinol. 2002;172: 71-81.
5. Uno H, Eisele S, Sakai A, et al. Neurotoxicity of glucocorticoids in the primate brain. Horm Behav. 1994;28: 336-348.
6. 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.
7. Levitt NS, Lindsay RS, Holmes MC, 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.
8. 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.
9. GloverVAnnual Research Review: Prenatal stress and the origins of psychopathology: an evolutionary perspective. J Child Psychol Psychiatry. 2011;52: 356-367.
10. Alexander N, Rosenlöcher F, Stalder T, et al. Impact of antenatal synthetic glucocorticoid exposure on endocrine stress reactivity in term-born children. J Clin Endocrinol Metab. 2012;97: 3538-3544.
11. Crudo A, Suderman M, Moisiadis VG, et al. Glucocorticoid programming of the fetal male hippocampal epigenome. Endocrinology. 2013;154: 1168-1180.
12. Crudo A, Petropoulos S, Moisiadis VG, et al. Prenatal synthetic glucocorticoid treatment changes DNA methylation States in male organ systems: multigenerational effects. Endocrinology. 2012;153: 3269-3283.
13. Owen D, Matthews SG Glucocorticoids and sex-dependent development of brain glucocorticoid and mineralocorticoid receptors. Endocrinology. 2003;144: 2775-2784.
14. Meaney MJ, Sapolsky RM, McEwen BS The development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. Brain Res. 1985;350: 159-164.
15. 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.
16. Keightley MC, Fuller PJ Cortisol resistance and the guinea pig glucocorticoid receptor. Steroids. 1995;60: 87-92.
17. 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.
18. SmythGKLimma: linear models for microarray data. In: Gentleman VC, Dudoit S, Irizarry R, Huber W, eds. Bioinformatics and Computational Biology Solutions UsingRand Bioconductor.NewYork, NY: Springer; 2005: 397-420.
19. 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.
20. Crane-Robinson C, Myers FA, Hebbes TR, Clayton AL, Thorne AWChromatin immunoprecipitation assays in acetylation mapping of higher eukaryotes. Methods Enzymol. 1999;304: 533-547.
21. Weaver IC, Cervoni N, Champagne FA, et al. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7: 847-854.
22. Technologies A 2010 Agilent Mammalian ChIP-on-chip Protocol Version 10.11. http://www.genomics.agilent.com/files/Manual/ G4481-90010- MammalianProtocol-10.11.pdf.
23. 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.
24. Thomassin H, Flavin M, Espinás ML, Grange T Glucocorticoidinduced DNA demethylation and gene memory during development. EMBO J. 2001;20: 1974-1983.
25. Pankevich DE, Mueller BR, Brockel B, Bale TL Prenatal stress programming of offspring feeding behavior and energy balance begins early in pregnancy. Physiol Behav. 2009;98: 94-102.
26. Morgan CP, Bale TL Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J Neurosci. 2011;31: 11748-11755.
27. BaleTLSex differences in prenatal epigenetic programming of stress pathways. Stress. 2011;14: 348-356.
28. Fowden AL, Li J, Forhead AJ Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance? Proc Nutr Soc. 1998;57: 113-122.
29. Bloomfield FH Epigenetic modifications may play a role in the developmental consequences of early life events. J Neurodev Disord. 2011;3: 348-355.
30. Hochberg Z, Feil R, Constancia M, et al. Child health, developmental plasticity, and epigenetic programming. Endocr Rev. 2011;32: 159-224.
31. Bian XP, Seidler FJ, SlotkinTAPromotional role for glucocorticoids in the development of intracellular signalling: enhanced cardiac and renal adenylate cyclase reactivity to β-adrenergic and non-adrenergic stimuli after low-dose fetal dexamethasone exposure. J Dev Physiol. 1991;16: 331-339.
32. Bian XP, Seidler FJ, SlotkinTAPromotional role for glucocorticoids in the development of intracellular signalling: enhanced cardiac and renal adenylate cyclase reactivity to β-adrenergic and non-adrenergic stimuli after low-dose fetal dexamethasone exposure. J Dev Physiol. 1992;17: 289-297.
33. Owen D, Matthews SG Prenatal glucocorticoid exposure alters hypothalamic- pituitary-adrenal function in juvenile guinea pigs. J Neuroendocrinol. 2007;19: 172-180.
34. Welberg LA, Seckl JR, Holmes MC Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience. 2001;104: 71-79.
35. Drake AJ, Walker BR, Seckl JR Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol. 2005;288:R34-R38.
36. Drake RR, Cazares LH, Jones EE, Fuller TW, Semmes OJ, Laronga C Challenges to developing proteomic-based breast cancer diagnostics. OMICS. 2011;15: 251-259.
37. Fisher DA, KleinAHThyroid development and disorders of thyroid function in the newborn. N Engl J Med. 1981;304: 702-712.
38. 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.
39. Martin CR, Van Marter LJ, Allred EN, Leviton A, Developmental Epidemiology Network Antenatal glucocorticoids increase early total thyroxine levels in premature infants. Biol Neonate. 2005;87: 273-280.
40. Truss M, BeatoMSteroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors. Endocr Rev. 1993; 14: 459-479.
41. Kassel O, Herrlich P Crosstalk between the glucocorticoid receptor and other transcription factors: molecular aspects. Mol Cell Endocrinol. 2007;275: 13-29.
42. Torres A, Tucker DC Glucocorticoid stimulation interacts with sympathetic innervation to affect cardiac development in oculo. Pediat Res. 1995;38: 479-484.
43. Wintour EM Cortisol: a growth hormone for the fetal heart? Endocrinology. 2006;147: 3641-3642.
44. Bolt RJ, van Weissenbruch MM, Lafeber HN, Delemarre-van de Waal HA 2001 Glucocorticoids and lung development in the fetus and preterm infant. Pediatr Pulmonol. 32: 76-91.
45. Edwards CR, Benediktsson R, Lindsay RS, Seckl JR 11 β-Hydroxysteroid dehydrogenases: key enzymes in determining tissue-specific glucocorticoid effects. Steroids. 1996;61: 263-269.
46. Dy J, Guan H, Sampath-Kumar R, Richardson BS, YangKPlacental 11β-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.
47. Seckl JR Glucocorticoids, feto-placental 11 β-hydroxysteroid dehydrogenase type 2, and the early life origins of adult disease. Steroids. 1997;62: 89-94.
48. Kalabis GM, Kostaki A, Andrews MH, Petropoulos S, Gibb W, Matthews SG Multidrug resistance phosphoglycoprotein (ABCB1) in the mouse placenta: fetal protection. Biol Reprod. 2005;73: 591-597.
49. McCabe L, Marash D, Li A, Matthews SG Repeated antenatal glucocorticoid treatment decreases hypothalamic corticotropin releasing hormonemRNAbut not corticosteroid receptormRNAexpression in the fetal guinea-pig brain. J Neuroendocrinol. 2001;13: 425-431.
50. Burnstein KL, Bellingham DL, Jewell CM, Powell-Oliver FE, Cidlowski JA Autoregulation of glucocorticoid receptor gene expression. Steroids. 1991;56: 52-58.
51. Mulatero P, Panarelli M, Schiavone D, et al. Impaired cortisol binding to glucocorticoid receptors in hypertensive patients. Hypertension. 1997;30: 1274-1278.
52. Reul JM, de Kloet ER, van Sluijs FJ, Rijnberk A, Rothuizen J Binding characteristics of mineralocorticoid and glucocorticoid receptors in dog brain and pituitary. Endocrinology. 1990;127: 907-915.
53. 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.