The impact of maternal synthetic glucocorticoid administration in late pregnancy on fetal and early neonatal hypothalamic-pituitary-adrenal axes regulatory genes is dependent upon dose and gestational age at exposure

Journal of Developmental Origins of Health and Disease

Volumn 4, Issue 1, 2013, Pages 77-89

  Li, S ^a,b   Moss, T J M ^a,c   Nitsos, I ^a,c   Matthews, S G ^d   Challis, J R G ^a,d   Newnham, J P ^a,b   Sloboda, D M ^e  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b Women and Infants Research Foundation of Western Australia   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF TORONTO   (Canada)

^e MCMASTER UNIVERSITY   (Canada)

Author keywords

adrenal; fetus; glucocorticoid; hypothalamic pituitary adrenal axis; programming

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; BETAMETHASONE; GLUCOCORTICOID; HYDROCORTISONE; MELANOCORTIN 2 RECEPTOR; PHOSPHOPROTEIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

AGE; ANIMAL; BLOOD; DOSE RESPONSE; DRUG EFFECTS; FEMALE; FETUS; GENE EXPRESSION REGULATION; GENETICS; GESTATIONAL AGE; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM; NEWBORN; PREGNANCY; PRENATAL EXPOSURE; SHEEP;

3-HYDROXYSTEROID DEHYDROGENASES; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BETAMETHASONE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FETUS; GENE EXPRESSION REGULATION; GESTATIONAL AGE; GLUCOCORTICOIDS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; PHOSPHOPROTEINS; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RECEPTORS, CORTICOTROPIN; SHEEP;

EID: 84872087391     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S2040174412000591     Document Type: Article

References (55)

1. Polyakov A, Cohen S, Marita B, et al. Patterns of antenatal corticosteroid prescribing 1998-2004. Aust N Z J Obstet Gynaecol. 2007; 47, 42-45.
2. Crowley P. Prophylactic corticosteroids for preterm birth. Cochrane Database Syst Rev. 2000, CD000065.
3. Ikegami M, Jobe AH, Newnham J, et al. Repetitive prenatal glucocorticoids improve lung function and decrease growth in preterm lambs. Am J Respir Crit Care Med. 1997; 156, 178-184.
4. Moss TJ, Sloboda DM, Gurrin LC, et al. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am J Physiol Regul Integr Comp Physiol. 2001; 281, R960-R970.
5. Sloboda DM, Newnham JP, Challis Jr. Effects of repeated maternal betamethasone administration on growth and hypothalamic-pituitary-adrenal function of the ovine fetus at term. J Endocrinol. 2000; 165, 79-91.
6. Sloboda DM, Newnham JP. Repeated maternal glucocorticoid administration and the developing liver in fetal sheep. J Endocrinol. 2002; 175, 535-543.
7. Sloboda DM, Challis JR, Moss TJ, Newnham JP. Synthetic glucocorticoids: antenatal administration and long-term implications. Curr Pharm Des. 2005; 11, 1459-1472.
8. Newnham JP. Is prenatal glucocorticoid administration another origin of adult disease? Clin Exp Pharmacol Physiol. 2001; 28, 957-961.
9. 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.
10. Sloboda DM, Moss TJ, Li S, et al. Prenatal betamethasone exposure results in pituitary-adrenal hyporesponsiveness in adult sheep. Am J Physiol Endocrinol Metab. 2007; 292, E61-E70.
11. Benediktsson R, Lindsay RS, Noble J, Seckl JR, Edwards CR. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet. 1993; 341, 339-341.
12. Cleasby ME, Livingstone DE, Nyirenda MJ, Seckl JR, Walker BR. Is programming of glucocorticoid receptor expression by prenatal dexamethasone in the rat secondary to metabolic derangement in adulthood? Eur J Endocrinol. 2003; 148, 129-138.
13. Owen D, Matthews SG. Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function in juvenile guinea pigs. J Neuroendocrinol. 2007; 19, 172-180.
14. Banjanin S, Kapoor A, Matthews SG. Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function and blood pressure in mature male guinea pigs. J Physiol. 2004; 558, 305-318.
15. 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.
16. McDonald TJ. Hypothalamic glucocorticoid implants prevent fetal ovine adrenocorticotropin secretion in response to stress. Endocrinology. 1990; 127, 2862-2868.
17. Akagi K, Berdusco ET, Challis Jr. Cortisol inhibits ACTH but not the AVP response to hypoxaemia in fetal lambs at days 123-128 of gestation. J Dev Physiol. 1990; 14, 319-324.
18. Moss TJ, Harding R, Newnham JP. Lung function, arterial pressure and growth in sheep during early postnatal life following single and repeated prenatal corticosteroid treatments. Early Hum Dev. 2002; 66, 11-24.
19. Jobe AH, Moss TJ, Nitsos I, et al. Betamethasone for lung maturation: testing dose and formulation in fetal sheep. Am J Obstet Gynecol. 2007; 197:523 e521-526.
20. Gatford KL, Owens JA, Li S, et al. Repeated betamethasone treatment of pregnant sheep programs persistent reductions in circulating IGF-I and IGF-binding proteins in progeny. Am J Physiol Endocrinol Metab. 2008; 295, E170-E178.
21. Sloboda DM, Moss TJ, Li S, et al. Hepatic glucose regulation and metabolism in adult sheep: effects of prenatal betamethasone. Am J Physiol Endocrinol Metab. 2005; 289, E721-E728.
22. Sloboda DM, Moss TJ, Li S, et al. Expression of glucocorticoid receptor, mineralocorticoid receptor, and 11beta-hydroxysteroid dehydrogenase 1 and 2 in the fetal and postnatal ovine hippocampus: ontogeny and effects of prenatal glucocorticoid exposure. J Endocrinol. 2008; 197, 213-220.
23. Gutierrez-Adan A, Cushwa WT, Anderson GB, Medrano JF. Ovine-specific Y-chromosome RAPD-SCAR marker for embryo sexing. Anim Genet. 1997; 28, 135-138.
24. Holloway AC, Howe DC, Chan G, et al. Urocortin: a mechanism for the sustained activation of the HPA axis in the late-gestation ovine fetus? Am J Physiol Endocrinol Metab. 2002; 283, E165-E171.
25. Zarkawi M, Soukouti A. Serum progesterone levels using radioimmunoassay during oestrous cycle of indigenous Damascus does. NZ J Agric Res. 2001; 44, 165-170.
26. Bloomfield FH, Oliver MH, Hawkins P, et al. Periconceptional undernutrition in sheep accelerates maturation of the fetal hypothalamic- pituitary-adrenal axis in late gestation. Endocrinology. 2004; 145, 4278-4285.
27. McCabe L, Marash D, Li A, Matthews SG. 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; 13, 425-431.
28. Zhao HF, Simard J, Labrie C, Breton N, Rheaume E. Molecular cloning, cDNA structure and predicted amino acid sequence of bovine 3 beta-hydroxy-5-ene steroid dehydrogenase/delta 5-delta 4 isomerase. FEBS Lett. 1989; 259, 153-157.
29. Dodic M, Hantzis V, Duncan J, et al. Programming effects of short prenatal exposure to cortisol. In FASEB. 2002; 16, 1017-1026.
30. Van Harmelen V, Ariapart P, Hoffstedt J, et al. Increased adipose angiotensinogen gene expression in human obesity. In NAASO. 2000; 8, 337-341.
31. Jobe AH, Wada N, Berry LM, Ikegami M, Ervin MG. Single and repetitive maternal glucocorticoid exposures reduce fetal growth in sheep. Am J Obstet Gynecol. 1998; 178, 880-885.
32. Moss TJM, Doherty DA, Nitsos I, et al. Effects into adulthood of single or repeated antenatal corticosteroids in sheep. Am J Obstet Gynecol. 2005; 192, 146-152.
33. Matthews SG, Challis Jr. CRH and AVP-induced changes in synthesis and release of ACTH from the ovine fetal pituitary in vitro: negative influences of cortisol. Endocrine. 1997; 6, 293-300.
34. Challis JRG, Matthews SG, Gibb W, Lye SJ. Endocrine and paracrine regulation of birth at term and preterm. Endocr Rev. 2000; 21, 514-550.
35. Levidiotis ML, Wintour EM, McKinley MJ, Oldfield BJ. Hypothalamic- hypophyseal vascular connections in the fetal sheep. Neuroendocrinology. 1989; 49, 47-50.
36. Berdusco ET, Hammond GL, Jacobs RA, et al. Glucocorticoid-induced increase in plasma corticosteroid-binding globulin levels in fetal sheep is associated with increased biosynthesis and alterations in glycosylation. Endocrinology. 1993; 132, 2001-2008.
37. Berdusco ET, Milne WK, Challis Jr. Low-dose cortisol infusion increases plasma corticosteroid-binding globulin (CBG) and the amount of hepatic CBG mRNA in fetal sheep on day 100 of gestation. J Endocrinol. 1994; 140, 425-430.
38. Clifton VL. Sexually dimorphic effects of maternal asthma during pregnancy on placental glucocorticoid metabolism and fetal growth. Cell Tissue Res. 2005; 322, 63-71.
39. Braun T, Li S, Sloboda DM, et al. Effects of maternal dexamethasone treatment in early pregnancy on pituitary-adrenal axis in fetal sheep. Endocrinology. 2009; 150, 5466-5477.
40. Ross JT, McMillen IC, Adams MB, Coulter CL. A premature increase in circulating cortisol suppresses expression of 11beta hydroxysteroid dehydrogenase type 2 messenger ribonucleic acid in the adrenal of the fetal sheep. Biol Reprod. 2000; 62, 1297-1302.
41. MacLaughlin SM, Walker SK, Kleemann DO, et al. Impact of periconceptional undernutrition on adrenal growth and adrenal insulin-like growth factor and steroidogenic enzyme expression in the sheep fetus during early pregnancy. Endocrinology. 2007; 148, 1911-1920.
42. Matthews SG, Han X, Lu F, Challis Jr. Developmental changes in the distribution of pro-opiomelanocortin and prolactin mRNA in the pituitary of the ovine fetus and lamb. J Mol Endocrinol. 1994; 13, 175-185.
43. Matthews SG, Owen D, Banjanin S, Andrews MH. Glucocorticoids, hypothalamo-pituitary-adrenal (HPA) development, and life after birth. Endocr Res. 2002; 28, 709-718.
44. Matthews SG, Challis Jr. Regulation of the hypothalamo-pituitary- adrenocortical axis in fetal sheep. Trends Endocrinol Metab. 1996; 7, 239-246.
45. Seckl JR, Cleasby M, Nyirenda MJ. Glucocorticoids, 11beta-hydroxysteroid dehydrogenase, and fetal programming. Kidney Int. 2000; 57, 1412-1417.
46. Braun T, Li S, Moss TJ, et al. Maternal betamethasone administration reduces binucleate cell number and placental lactogen in sheep. J Endocrinol. 2007; 194, 337-347.
47. Newnham JP, Moss TJM, Nitsos I, Sloboda DM. Antenatal corticosteroids: the good, the bad and the unknown. Curr Opin Obstet Gynecol. 2002; 14, 607-612.
48. Matthews SG, Challis Jr. Regulation of CRH and AVP mRNA in the developing ovine hypothalamus: effects of stress and glucocorticoids. Am J Physiol. 1995; 268, E1096-E1107.
49. Bloomfield FH, Oliver MH, Hawkins P, et al. A periconceptional nutritional origin for noninfectious preterm birth. Science. 2003; 300, 606.
50. Matthews SG, Yang K, Challis Jr. Changes in glucocorticoid receptor mRNA in the developing ovine pituitary and the effects of exogenous cortisol. J Endocrinol. 1995; 144, 483-490.
51. Jones CT, Roebuck MM. ACTH peptides and the development of the fetal adrenal. J Steroid Biochem. 1980; 12, 77-82.
52. Rousseau K, Kauser S, Pritchard LE, et al. Proopiomelanocortin (POMC), the ACTH/melanocortin precursor, is secreted by human epidermal keratinocytes and melanocytes and stimulates melanogenesis. FASEB J. 2007; 21, 1844-1856.
53. Rainey WE, Carr BR, Wang ZN, Parker CR Jr. Gene profiling of human fetal and adult adrenals. J Endocrinol. 2001; 171, 209-215.
54. Mansfield CW, Carr BR, Faye-Petersen OM, et al. Differential gene expression in the adrenals of normal and anencephalic fetuses and studies focused on the Fras-1-related extracellular matrix protein (FREM2) gene. Reprod Sci. 2011; 18, 1146-1153.
55. Moritz K, Butkus A, Hantzis V, et al. Prolonged low-dose dexamethasone, in early gestation, has no long-term deleterious effect on normal ovine fetuses. Endocrinology. 2002; 143, 1159-1165.