Prenatal corticosterone exposure programs sex-specific adrenal adaptations in mouse offspring

Journal of Endocrinology

Volumn 232, Issue 1, 2017, Pages 37-48

  Cuffe, J S M ^a,b   Turton, E L ^a   Akison, L K ^a   Bielefeldt Ohmann, H ^a   Moritz, K M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

Author keywords

Adrenal cortex; DOHAD; Foetal programming; HPA

Indexed keywords

ALDOSTERONE; ALDOSTERONE SYNTHASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CORTICOSTERONE; CORTICOTROPIN; CYTOCHROME P450 FAMILY 11; CYTOCHROME P450 FAMILY 11 SUBFAMILY B POLYPEPTIDE 1; CYTOCHROME P450 FAMILY 21; CYTOCHROME P450 FAMILY 21 SUBFAMILY A POLYPEPTIDE 1; GLUCOCORTICOID; MELANOCORTIN 2 RECEPTOR; STEROIDOGENIC ACUTE REGULATORY PROTEIN; UNCLASSIFIED DRUG;

ADRENAL FUNCTION; ALDOSTERONE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR DISEASE; COMPARATIVE STUDY; CONTROLLED STUDY; FETUS DEVELOPMENT; GENE EXPRESSION; IMMOBILIZATION STRESS; IMMUNOHISTOCHEMISTRY; KIDNEY DISEASE; MALE; MATERNAL PLASMA; MATERNAL STRESS; MOUSE; NONHUMAN; PERINATAL PERIOD; PRENATAL DEVELOPMENT; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; ZONA FASCICULATA; ADRENAL GLAND; ANATOMY AND HISTOLOGY; ANIMAL; BLOOD; DRUG EFFECTS; FEMALE; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM; ORGAN SIZE; PREGNANCY;

ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; ALDOSTERONE; ANIMALS; CORTICOSTERONE; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MICE; ORGAN SIZE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEX FACTORS;

EID: 85007560401     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-16-0417     Document Type: Article

References (39)

1. Anagnostis P, Athyros VG, Tziomalos K, Karagiannis A & Mikhailidis DP 2009 Clinical review: the pathogenetic role of cortisol in the metabolic syndrome: a hypothesis. Journal of Clinical Endocrinology and Metabolism 94 2692-2701. (doi:10.1210/jc.2009-0370)
2. Banjanin S, Kapoor A & Matthews SG 2004 Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function and blood pressure in mature male guinea pigs. Journal of Physiology 558 305-318. (doi:10.1113/jphysiol.2004.063669)
3. Bielohuby M, Herbach N, Wanke R, Maser-Gluth C, Beuschlein F, Wolf E & Hoeflich A 2007 Growth analysis of the mouse adrenal gland from weaning to adulthood: time-and gender-dependent alterations of cell size and number in the cortical compartment. American Journal of Physiology: Endocrinology and Metabolism 293 E139-E146. (doi:10.1152/ajpendo.00705.2006)
4. Chatelain A & Dupouy JP 1981 Activity of the pituitary-adrenal system in rat fetuses subjected to encephalectomy in early or late stages of pregnancy. Neuroendocrinology 33 148-152. (doi:10.1159/000123220)
5. Cheong JN, Cuffe JS, Jefferies AJ, Anevska K, Moritz KM & Wlodek ME 2016 Sex-specific metabolic outcomes in offspring of female rats born small or exposed to stress during pregnancy. Endocrinology en20161335. (doi:10.1210/en.2016-1335)
6. Chida D, Nakagawa S, Nagai S, Sagara H, Katsumata H, Imaki T, Suzuki H, Mitani F, Ogishima T, Shimizu C, et al. 2007 Melanocortin 2 receptor is required for adrenal gland development, steroidogenesis, and neonatal gluconeogenesis. PNAS 104 18205-18210. (doi:10.1073/pnas.0706953104)
7. Cole TJ, Blendy JA, Monaghan AP, Krieglstein K, Schmid W, Aguzzi A, Fantuzzi G, Hummler E, Unsicker K & Schutz G 1995 Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes and Development 9 1608-1621. (doi:10.1101/gad.9.13.1608)
8. Cottrell EC & Seckl JR 2009 Prenatal stress, glucocorticoids and the programming of adult disease. Frontiers in Behavioral Neuroscience 3 19. (doi:10.3389/neuro.08.019.2009)
9. Cuffe JS, O'Sullivan L, Simmons DG, Anderson ST & Moritz KM 2012 Maternal corticosterone exposure in the mouse has sex-specific effects on placental growth and mRNA expression. Endocrinology 153 5500-5511. (doi:10.1210/en.2012-1479)
10. Cuffe JS, Walton SL, Singh RR, Spiers JG, Bielefeldt-Ohmann H, Wilkinson L, Little MH & Moritz KM 2014 Mid-to late term hypoxia in the mouse alters placental morphology, glucocorticoid regulatory pathways and nutrient transporters in a sex-specific manner. Journal of Physiology 592 3127-3141. (doi:10.1113/jphysiol.2014.272856)
11. Cuffe JS, Burgess DJ, O'Sullivan L, Singh RR & Moritz KM 2016 Maternal corticosterone exposure in the mouse programs sex-specific renal adaptations in the renin-angiotensin-aldosterone system in 6-month offspring. Physiological Reports 4 e12754. (doi:10.14814/phy2.12754)
12. de Vries A, Holmes MC, Heijnis A, Seier JV, Heerden J, Louw J, Wolfe-Coote S, Meaney MJ, Levitt NS & Seckl JR 2007 Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic-pituitary-adrenal axis function. Journal of Clinical Investigation 117 1058-1067. (doi:10.1172/JCI30982)
13. Dillberger JE, Cronin NS & Carr GJ 1992 Prednisone is not a mouse carcinogen. Toxicologic Pathology 20 18-26. (doi:10.1177/019262339 202000103)
14. Dunn TB 1970 Normal and pathologic anatomy of the adrenal gland of the mouse, including neoplasms. Journal of the National Cancer Institute 44 1323-1389. (doi:10.1093/jnci/44.6.1323)
15. Ferreira JG, Cruz CD, Neves D & Pignatelli D 2007 Increased extracellular signal regulated kinases phosphorylation in the adrenal gland in response to chronic ACTH treatment. Journal of Endocrinology 192 647-658. (doi:10.1677/joe.1.06961)
16. Frith CH 1983 Lipogenic pigmentation, adrenal cortex, mouse. In Endocrine System, pp 60-64. Eds TC Jones, U Mohr, RD Hunt & CC Capen. Berlin, Heidelberg, Germany: Springer Berlin Heidelberg. (doi:10.1007/978-3-642-96720-7_15)
17. Garcia-Caceres C, Lagunas N, Calmarza-Font I, Azcoitia I, Diz-Chaves Y, Garcia-Segura LM, Baquedano E, Frago LM, Argente J & Chowen JA 2010 Gender differences in the long-term effects of chronic prenatal stress on the HPA axis and hypothalamic structure in rats. Psychoneuroendocrinology 35 1525-1535. (doi:10.1016/j. psyneuen.2010.05.006)
18. Hu MC, Chou SJ, Huang YY, Hsu NC, Li H & Chung BC 1999 Tissue-specific, hormonal, and developmental regulation of SCC-LacZ expression in transgenic mice leads to adrenocortical zone characterization. Endocrinology 140 5609-5618. (doi:10.1210/en.140.12.5609)
19. Huxley RR, Shiell AW & Law CM 2000 The role of size at birth and postnatal catch-up growth in determining systolic blood pressure: a systematic review of the literature. Journal of Hypertension 18 815-831. (doi:10.1097/00004872-200018070-00002)
20. Kapoor A, Leen J & Matthews SG 2008 Molecular regulation of the hypothalamic-pituitary-adrenal axis in adult male guinea pigs after prenatal stress at different stages of gestation. Journal of Physiology 586 4317-4326. (doi:10.1113/jphysiol.2008.153684)
21. Langdown ML, Smith ND, Sugden MC & Holness MJ 2001 Excessive glucocorticoid exposure during late intrauterine development modulates the expression of cardiac uncoupling proteins in adult hypertensive male offspring. Pflügers Archiv: European Journal of Physiology 442 248-255. (doi:10.1007/s004240100519)
22. Leret ML, Peinado V, Gonzalez JC, Suarez LM & Rua C 2004 Maternal adrenalectomy affects development of adrenal medulla. Life Science 74 1861-1867. (doi:10.1016/j.lfs.2003.07.050)
23. Moritz K, Butkus A, Hantzis V, Peers A, Wintour EM & Dodic M 2002 Prolonged low-dose dexamethasone, in early gestation, has no long-term deleterious effect on normal ovine fetuses. Endocrinology 143 1159-1165. (doi:10.1210/endo.143.4.8747)
24. Moritz KM, Cuffe JS, Wilson LB, Dickinson H, Wlodek ME, Simmons DG & Denton KM 2010 Review: sex specific programming: a critical role for the renal renin-angiotensin system. Placenta 31 (Supplement) S40-S46. (doi:10.1016/j.placenta.2010.01.006)
25. O'Sullivan L, Cuffe JS, Koning A, Singh RR, Paravicini TM & Moritz KM 2015 Excess prenatal corticosterone exposure results in albuminuria, sex-specific hypotension, and altered heart rate responses to restraint stress in aged adult mice. American Journal of Physiology: Renal Physiology 308 F1065-F1073. (doi:10.1152/ajprenal.00676.2014)
26. Ojeda NB, Grigore D, Robertson EB & Alexander BT 2007 Estrogen protects against increased blood pressure in postpubertal female growth restricted offspring. Hypertension 50 679-685. (doi:10.1161/HYPERTENSIONAHA.107.091785)
27. Ozanne SE 2001 Metabolic programming in animals. British Medical Bulletin 60 143-152. (doi:10.1093/bmb/60.1.143)
28. Quinn TA, Ratnayake U, Castillo-Melendez M, Moritz KM, Dickinson H & Walker DW 2014 Adrenal steroidogenesis following prenatal dexamethasone exposure in the spiny mouse. Journal of Endocrinology 221 347-362. (doi:10.1530/JOE-13-0514)
29. Raber J, Akana SF, Bhatnagar S, Dallman MF, Wong D & Mucke L 2000 Hypothalamic-pituitary-adrenal dysfunction in Apoe(-/-) mice: possible role in behavioral and metabolic alterations. Journal of Neuroscience 20 2064-2071.
30. Rosol TJ, Yarrington JT, Latendresse J & Capen CC 2001 Adrenal gland: structure, function, and mechanisms of toxicity. Toxicologic Pathology 29 41-48. (doi:10.1080/019262301301418847)
31. Schardein JL, Patton GR & Lucas JA 1967 The microscopy of 'brown degeneration' in the adrenal gland of the mouse. Anatomical Record 159 291-309. (doi:10.1002/ar.1091590307)
32. Singh RR, Cuffe JS & Moritz KM 2012 Short-and long-term effects of exposure to natural and synthetic glucocorticoids during development. Clinical and Experimental Pharmacology and Physiology 39 979-989. (doi:10.1111/1440-1681.12009)
33. Spiers JG, Chen H-JC, Cuffe JSM, Sernia C & Lavidis NA 2016 Acute restraint stress induces rapid changes in central redox status and protective antioxidant genes in rats. Psychoneuroendocrinology 67 104-112. (doi:10.1016/j.psyneuen.2016.02.005)
34. Su Y, Carey LC, Rose JC & Pulgar VM 2013 Antenatal glucocorticoid exposure enhances the inhibition of adrenal steroidogenesis by leptin in a sex-specific fashion. American Journal of Physiology: Endocrinology and Metabolism 304 E1404-E1411. (doi:10.1152/ajpendo.00013.2013)
35. Sugimoto M, Kojima A & Endo H 1976 Role of glucocorticoids in terminal differentiation and tissue specific function. Development Growth and Differentiation 18 319-327. (doi:10.1111/j.1440-169X.1976.00319.x)
36. Valenzuela OA, Jellyman JK, Allen VL, Holdstock NB & Fowden AL 2016 Effects of maternal dexamethasone treatment on pancreatic beta cell function in the pregnant mare and postnatal foal. Equine Veterinary Journal [in press]. (doi:10.1111/evj.12560)
37. Van Cauwenberge JR, Hustin J, Demey-Ponsart E, Sulon J, Reuter A, Lambotte R & Franchimont P 1987 Changes in fetal and maternal blood levels of prolactin, cortisol, and cortisone during eutocic and dystocic childbirth. Hormone Research 25 125-131. (doi:10.1159/000180643)
38. Waddell BJ, Bollen M, Wyrwoll CS, Mori TA & Mark PJ 2010 Developmental programming of adult adrenal structure and steroidogenesis: effects of fetal glucocorticoid excess and postnatal dietary omega-3 fatty acids. Journal of Endocrinology 205 171-178. (doi:10.1677/JOE-09-0459)
39. Zilio M, Barbot M, Ceccato F, Camozzi V, Bilora F, Casonato A, Frigo AC, Albiger N, Daidone V, Mazzai L, et al. 2014 Diagnosis and complications of Cushing's disease: gender-related differences. Clinical Endocrinology 80 403-410. (doi:10.1111/cen.12299)