Estrogen regulation of fetal adrenal cortical zone-specific development in the nonhuman primate impacts adrenal production of androgen and cortisol and response to acth in females in adulthood

Endocrinology

Volumn 157, Issue 5, 2016, Pages 1905-1913

  Pepe, Gerald J ^a   Maniu, Adina ^a   Aberdeen, Graham ^b   Lynch, Terrie J ^a   Albrecht, Eugene D ^b  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; CORTICOTROPIN; ESTRADIOL; ESTROGEN; HYDROCORTISONE; LETROZOLE; PRASTERONE SULFATE; PROLACTIN; AROMATASE INHIBITOR; NITRILE; TRIAZOLE DERIVATIVE;

ADRENAL CORTEX; ADRENAL GLAND; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUSTRALIAN; BRAIN DEVELOPMENT; CLINICAL ASSESSMENT; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; ESTROGEN SYNTHESIS; FEMALE; FETUS BLOOD SAMPLING; FETUS CELL; FETUS DEVELOPMENT; GESTATIONAL AGE; HORMONE BLOOD LEVEL; HORMONE RELEASE; HYDROCORTISONE BLOOD LEVEL; HYPOPHYSIS ADRENAL SYSTEM; MALE; NONHUMAN; PAPIO ANUBIS; POSTNATAL DEVELOPMENT; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; ANIMAL; BABOON; BLOOD; DRUG EFFECTS; FETUS; METABOLISM;

ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; ANDROGENS; ANIMALS; AROMATASE INHIBITORS; DEHYDROEPIANDROSTERONE SULFATE; ESTRADIOL; FEMALE; FETUS; HYDROCORTISONE; NITRILES; PAPIO; PROLACTIN; TRIAZOLES;

EID: 84969822945     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-2087     Document Type: Article

References (40)

1. Pepe GJ, Albrecht ED. Regulation of the primate fetal adrenal cortex. Endocr Rev. 1990;11:151-176.
2. Pepe GJ, Albrecht ED. Actions of placental and fetal adrenal steroid hormones in primate pregnancy. Endocr Rev. 1995;16:608-648.
3. Mesiano S, Jaffe RB. Developmental and functional biology of the primate fetal adrenal cortex. Endocr Rev. 1997;18:378-403.
4. Ishimoto H, Jaffe RB. Development and function of the human fetal adrenal cortex: a key component in the feto-placental unit. Endocr Rev. 2011;32:317-355.
5. Benner MC. Studies on the involution of the fetal cortex of the adrenal glands. Am J Pathol. 1940;16:787-798.
6. Lanman JT. The adrenal fetal zone: its occurrence in primates and a possible relationship to chorionic gonadotropin. Endocrinology. 1957;61:684-691.
7. McNulty WP, Novy MJ, Walsh SW. Fetal and postnatal development of the adrenal glands in Macaca mulatta. Biol Reprod. 1981; 25:1079-1089.
8. Sidiropoulou E, Ghizzoni L, Mastorakos G. Adrenal androgens. In: De Groot LJ, Beck-Peccoz P, Chrousos G, et al, eds. Endotext. South Dartmouth, MA: MDText. com, Inc; 2012:2000.
9. Samaras N, Samaras D, Frangos E, Forster A, Philippe J. A review of age-related dehydroepiandrosterone decline and its association with well-known geriatric syndromes: is treatment beneficial? Rejuvenation Res. 2013;16:285-294.
10. Suzuki T, Sasano H, Takeyama J, et al. Developmental changes in steroidogenic enzymes in human postnatal adrenal cortex: immunohistochemical studies. Clin Endocrinol (Oxf). 2000;53:739-747.
11. Havelock JC, Auchus RJ, Rainey WE. The rise in adrenal androgen biosynthesis: adrenarche. Semin Reprod Med. 2004;22:337-347.
12. Rosenfield RL, Bongiovanni AM, Eberlein WR, Wright FH. Plasma testosterone and dehydroepiandrosterone sulfate during puberty. J Pediatr. 1969;74:830-831.
13. de Peretti E, Forest MG. Unconjugated dehydroepiandrosterone plasma levels in normal subjects from birth to adolescence in human: the use of a sensitive radioimmunoassay. J Clin Endocrinol Metab. 1976;43:982-991.
14. de Peretti E, Forest MG. Pattern of plasma dehydroepiandrosterone sulfate levels in humans from birth to adulthood: evidence for testicular production. J Clin Endocrinol Metab. 1978;47:572-577.
15. Nguyen AD, Mapes SM, Corbin CJ, Conley AJ. Morphological adrenarche in rhesus macaques: development of the zona reticularis is concurrent with fetal zone regression in the early neonatal period. J Endocrinol. 2008;199:367-378.
16. Cutler GB Jr, Glenn M, Bush M, Hodgen GD, Graham CE, Loriaux DL. Adrenarche: a survey of rodents, domestic animals, and primates. Endocrinology. 1978;103:2112-2118.
17. Arlt W, Martens JW, Song M, Wang JT, Auchus RJ, Miller WL. Molecular evolution of adrenarche: structural and functional analysis of P450c17 from four primate species. Endocrinology. 2002; 143:4665-4672.
18. Castracane VD, Cutler GB Jr, Loriaux DL. Pubertal endocrinology of the baboon: adrenarche. Am J Physiol. 1981;241:E305-E309.
19. Orentreich N, Brind JL, Rizer RL, Vogelman JH. Age changes and sex differences in serum dehydroepiandrosterone sulfate concentrations throughout adulthood. J Clin Endocrinol Metab. 1984;59: 551-555.
20. Davison SL, Bell R, Donath S, Montalto JG, Davis SR. Androgen levels in adult females: changes with age, menopause, and oophorectomy. J Clin Endocrinol Metab. 2005;90:3847-3853.
21. Goncharova ND, Lapin BA. Changes of hormonal function of the adrenal and gonadal glands in baboons of different age groups. J Med Primatol. 2000;29:26-35.
22. Yen SS, Laughlin GA. Aging and the adrenal cortex. Exp Gerontol. 1998;33:897-910.
23. Albrecht ED, Aberdeen GW, Pepe GJ. Estrogen elicits cortical zonespecific effects on development of the primate fetal adrenal gland. Endocrinology. 2005;146:1737-1744.
24. Albrecht ED, Babischkin JS, DaviesWA,LeavittMG,Pepe GJ. Identification and developmental expression of the estrogen receptor and in the baboon fetal adrenal gland. Endocrinology. 1999;140: 5953-5961.
25. Dumitrescu A, Aberdeen GW, Pepe GJ, Albrecht ED. Placental estrogen suppresses cyclin D1 expression in the nonhuman primate fetal adrenal cortex. Endocrinology. 2014;155:4774-4784.
26. Albrecht ED, Aberdeen GW, Pepe GJ. The role of estrogen in the maintenance of primate pregnancy. Am J Obstet Gynecol. 2000; 182:432-438.
27. Pepe GJ, Lynch TJ, Albrecht ED. Regulation of baboon fetal ovarian development by placental estrogen: onset of puberty is delayed in offspring deprived of estrogen in utero. Biol Reprod. 2013;89:132.
28. Pepe GJ, Lynch TJ, Davies WA, Albrecht ED. Regulation of baboon fetal pituitary prolactin expression by estrogen. Biol Reprod. 2009; 80:1189-1195.
29. Albrecht ED, Pepe GJ. Endocrinology of pregnancy. In: Brans YW, Kuehl TJ, eds. Non-Human Primates in Perinatal Research. New York, NY: John Wiley and Sons; 1988:13-78.
30. Mapes S, Corbin CJ, Tarantal A, Conley A. The primate adrenal zona reticularis is defined by expression of cytochrome b5, 17-hydroxylase/17,20-lyase cytochrome P450 (P450c17) and NADPH-cytochrome P450 reductase (reductase) but not 3-hydroxysteroid dehydrogenase/-5-4 isomerase (3-HSD). J Clin Endocrinol Metab. 1999;84:3382-3385.
31. Conley AJ, Plant TM, Abbott DH, Moeller BC, Stanley SD. Adrenal androgen concentrations increase during infancy in male rhesus macaques (Macaca mulatta). Am J Physiol Endocrinol Metab. 2011; 301:E1229-E1235.
32. Ducsay CA, Hess DL, McClellan MC, Novy MJ. Endocrine and morphological maturation of the fetal and neonatal adrenal cortex in baboons. J Clin Endocrinol Metab. 1991;73:385-395.
33. Serón-Ferré M, Hess DL, Lindholm U, Jaffe RB. Persistence of fetal zone function in the infant rhesus monkey adrenal gland. J Clin Endocrinol Metab. 1986;62:460-465.
34. Labrie F, Bélanger A, Cusan L,GomezJL, Candas B. Markeddecline in serum concentrations of adrenal C19 sex steroid precursors and conjugated androgen metabolites during aging. J Clin Endocrinol Metab. 1997;82:2396-2402.
35. Legrain S, Massien C, Lahlou N, et al. Dehydroepiandrosterone replacement administration: pharmacokinetic and pharmacodynamic studies in healthy elderly subjects. J Clin Endocrinol Metab. 2000;85:3208-3217.
36. Liu D, Dillon JS. Dehydroepiandrosterone activates endothelial cell nitric-oxide synthase by a specific plasma membrane receptor coupled to G-(i2,3). J Biol Chem. 2002;277:21379-21388.
37. Liu D, Dillon JS. Dehydroepiandrosterone stimulates nitric oxide release in vascular endothelial cells: evidence for a cell surface receptor. Steroids. 2004;69:279-289.
38. Simoncini T, Mannella P, Fornari L, Varone G, Caruso A, Genazzani AR. Dehydroepiandrosterone modulates endothelial nitric oxide synthesis via direct genomic and nongenomic mechanisms. Endocrinology. 2003;144:3449-3455.
39. Traish AM, Kang HP, Saad F, Guay AT. Dehydroepiandrosterone (DHEA)-a precursor steroid or an active hormone in human physiology. J Sex Med. 2011;8:2960-2982; quiz 2983.
40. Maniu A, Aberdeen GW, Lynch TJ, Kim SO, Pepe GJ, Albrecht ED. Fetal programming in the nonhuman primate: impact of estrogen deprivation in utero on insulin sensitivity in offspring after birth. Program of the 6II Annual Meeting of the Society for Reproductive Investigation, San Francisco, CA, 2015 (Abstract T-189).