Variations in adrenal androgen production among (nonhuman) primates

Seminars in Reproductive Medicine

Volumn 22, Issue 4, 2004, Pages 311-326

  Conley, Alan J ^a   Pattison, J Christina ^b   Bird, Ian M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

17 hydroxylase 17 dehydrogenase; Adrenal cortex; Adrenal gland; Adrenarche; Androgen; Dehydroepiandrosterone (DHEA); Dehydroepiandrosterone sulphate (DS); Fetal zone; Nonhuman primate; Primate; Senescence; Zona reticularis

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ANDROGEN; CYTOCHROME B5; CYTOCHROME P450 REDUCTASE; CYTOCHROME P450C17; ESTROGEN; PRASTERONE; PRASTERONE SULFATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; STEROID 17,20 LYASE; STEROID 17ALPHA MONOOXYGENASE;

ADOLESCENCE; ADRENAL CORTEX; ADRENAL FUNCTION; ADRENARCHE; AGING; ANDROGEN METABOLISM; ANDROGEN RELEASE; ANDROGEN SYNTHESIS; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; ESTROGEN URINE LEVEL; HUMAN; IMMUNOHISTOCHEMISTRY; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PRIMATE; PROTEIN EXPRESSION; REVIEW; SENESCENCE; STEROIDOGENESIS;

ADRENAL GLANDS; ANDROGENS; ANIMALS; CYTOCHROMES B5; DEHYDROEPIANDROSTERONE; DEHYDROEPIANDROSTERONE SULFATE; ESTROGENS; FEMALE; GONADS; HUMANS; MALE; PRIMATES; SPECIES SPECIFICITY; STEROID 17-ALPHA-HYDROXYLASE; ZONA RETICULARIS;

EID: 11144232802     PISSN: 15268004     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2004-861548     Document Type: Review

References (171)

1. Mesiano S, Jaffe RB. Developmental and functional biology of the primate fetal adrenal cortex. Endocr Rev 1997;18:378-403
2. Pepe GJ, Albrecht ED. Regulation of the primate fetal adrenal cortex. Endocr Rev 1990;11:151-176
3. Baulieu EE. Dehydroepiandrosterone (DHEA): a fountain of youth? J Clin Endocrinol Metab 1996;81:3147-3151
4. Haning RV Jr, Chabot M, Flood CA, Hackett R, Longcope C. Metabolic clearance rate (MCR) of dehydroepiandrosterone sulfate (DS), its metabolism to dehydroepiandrosterone, androstenedione, testosterone, and dihydrotestosterone, and the effect of increased plasma DS concentration on DS MCR in normal women. J Clin Endocrinol Metab 1989;69: 1047-1052
5. Farah MJ, Givens JR, Kitabchi AE. Bimodal correlation between the circulating insulin level and the production rate of dehydroepiandrosterone: positive correlation in controls and negative correlation in the polycystic ovary syndrome with acanthosis nigricans. J Clin Endocrinol Metab 1990; 70:1075-1081
6. Longcope C. Dehydroepiandrosterone metabolism. J Endocrinol 1996;150(Suppl):S125-S127
7. Longcope C, Tast J. Dehydroepiandrosterone metabolism in the female rhesus monkey: oral versus intravenous administration. Steroids 1996;61:7-10
8. Seron-Ferre 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
9. Schut HA, Pepe GJ, Townsley JD. Clearance and production of dehydroepiandrosterone and its sulfate in female baboons. Am J Physiol 1978;235:E74-E77
10. Grollman A. The Adrenals. Baltimore, MD: Williams & Wilkins; 1936
11. Wilkins L, Fleischmann W, Howard JE. Macrogenitosomia precox associated with hyperplasia of the androgenic tissue of the adrenal and death from corticoadrenal insifficiency. Endocrinology 1940;26:385-395
12. Vande Wiele RL, MacDonald PC, Bolte E, Lieberman S. Precursors of the urinary 11-desoxy-17-ketosteroids: estimation of the secretory rate of dehydroisoandrosterone. J Clin Endocrinol Metab 1962;22:1207-1221
13. Short RV. The secretion of sex hormones by the adrenal gland. In: Clark F, Grant JK, eds. The Biosynthesis and Secretion of Adrenocortical Hormones. Cambridge: Cambridge University Press; 1960:59-85
14. Wieland RG, Decourcy C, Levy RP, Zala AP, Hirschmann H. C-19-O-2 steroids and some of their precursors in blood from normal human adrenals. J Clin Invest 1965;44:159-168
15. Abbott DH, Dumesic DA, Eisner JR, Colman RJ, Kemnitz JW. Insights into the development of PCOS from studies of prenatally androgenized female rhesus monkeys. Trends Endocrinol Metab 1998;9:62-67
16. Barker DJ. The developmental origins of adult disease. Eur J Epidemiol 2003;18:733-736
17. Conley AJ, Bird IM. The role of cytochrome P450 17α-hydroxylase and 3β-hydroxysteroid dehydrogenase in the integration of gonadal and adrenal steroidogenesis via the Δ5 and Δ4 pathways of steroidogenesis in mammals. Biol Reprod 1997;56:789-799
18. Le Goascogne C, Sananaes N, Gouaezou M, et al. Immunoreactive cytochrome P-450 17 alpha in rat and guinea-pig gonads, adrenal glands and brain. J Reprod Fertil 1991;93:609-622
19. van Weerden WM, Bierings HG, van Steenbrugge GJ, de Jong FH, Schroder FH. Adrenal glands of mouse and rat do not synthesize androgens. Life Sci 1992;50:857-861
20. Cloutier M, Fleury A, Courtemanche J, et al. Characterization of the adrenal cytochrome P450C17 in the hamster, a small animal model for the study of adrenal dehydroepiandrosterone biosynthesis. DNA Cell Biol 1997;16:357-368
21. Pieper DR, Lobocki CA. Characterization of serum dehydroepiandrosterone secretion in golden hamsters. Proc Soc Exp Biol Med 2000;224:278-284
22. Cutler GJ, Glenn M, Bush M, et al. Adrenarche: a survey of rodents, domestic animals, and primates. Endocrinology 1978;103:2112-2118
23. Wichmann U, Wichmann G, Krause W. Serum levels of testosterone precursors, testosterone and estradiol in 10 animal species. Exp Clin Endocrinol 1984;83:283-290
24. Guillemette C, Hum DW, Belanger A. Levels of plasma C19 steroids and 5 alpha-reduced C19 steroid glucuronides in primates, rodents, and domestic animals. Am J Physiol 1996;271:E348-E353
25. Schiebinger RJ, Albertson BD, Barnes KM, Cutler GB Jr, Loriaux DL. Developmental changes in rabbit and dog adrenal function: a possible homologue of adrenarche in the dog. Am J Physiol 1981;240:E694-E699
26. Jones IC. The Adrenal Cortex. London: Cambridge University Press; 1957
27. Enders AC, Schlafke S, Warren R. Cytology of the fetal zone of the adrenal gland of the armadillo. Anat Rec 1966;154:807-821
28. Auchus RJ. Overview of dehydroepiandrosterone biosynthesis. Semin Reprod Med 2004;22:281-288
29. Dharia S, Parker CR Jr. Adrenal androgens and aging. Semin Reprod Med 2004;22:361-368
30. Dharia S, Slane A, Jian M, et al. Colocalization of P450c17 and cytochrome b5 in androgen-synthesizing tissues of the human. Biol Reprod 2004;71:83-88
31. Arlt W, Martens JW, Song M, et al. Molecular evolution of adrenarche: structural and functional analysis of P450c17 from four primate species. Endocrinology 2002;143:4665-4672
32. Ainsworth L, Daenen M, Ryan KJ. Steroid hormone transformations by endocrine organs from pregnant mammals. IV. Biosynthesis and metabolism of estrogens and progesterone by primate placental preparations in vitro. Endocrinology 1969;84:1421-1429
33. Siiteri PK, MacDonald PC. The utilization of circulating dehydroisoandrosterone sulfate for estrogen synthesis during human pregnancy. Steroids 1963;2:713-730
34. Heinrichs WL, Feder HH, Colas A. The steroid 16-alpha-hydroxylase system in mammalian liver. Steroids 1966;7: 91-98
35. Townsley JD. Estrogen excretion of the pregnant baboon (Papio papio). Endocrinology 1974;95:1759-1762
36. Czekala NM, Benirschke K, McClure H, Lasley BL. Urinary estrogen excretion during pregnancy in the gorilla (Gorilla gorilla), orangutan (Pongo pygmaeus) and the human (Homo sapiens). Biol Reprod 1983;28:289-294
37. Hopper BR, Tullner WW, Gray CW. Urinary estrogen excretion during pregnancy in a gorilla (Gorilla gorilla). Proc Soc Exp Biol Med 1968;129:213-214
38. Hopper BR, Tullner WW. Urinary estrogen excretion patterns in pregnant rhesus monkeys. Steroids 1967;9:517-527
39. Liskowski L, Wolf RC, Chandler S, Meyer RK. Urinary estrogen excretion in pregnant rhesus monkeys. Biol Reprod 1970;3:55-60
40. Monfort SL, Thompson MA, Czekala NM, et al. Identification of a non-steroidal estrogen, equol, in the urine of pregnant macaques: correlation with steroidal estrogen excretion. J Steroid Biochem 1984;20:869-876
41. Eastman SA, Makawiti DW, Collins WP, Hodges JK. Pattern of excretion of urinary steroid metabolites during the ovarian cycle and pregnancy in the marmoset monkey. J Endocrinol 1984;102:19-26
42. Hodges JK, Brand H, Henderson C, Kelly RW. Levels of circulating and urinary oestrogens during pregnancy in the marmoset monkey (Callithrix jacchus). J Reprod Fertil 1983; 67:73-82
43. Lasley BL, Hodges JK, Czekala NM. Monitoring the female reproductive cycle of great apes and other primate species by determination of oestrogen and LH in small volumes of urine. J Reprod Fertil Suppl 1980;28(Suppl):121-129
44. Ziegler TE, Snowdon CT, Warneke M, Bridson WE. Urinary excretion of oestrone conjugates and gonadotrophins during pregnancy in the Goeldi's monkey (Callimico goeldii). J Reprod Fertil 1990;89:163-168
45. Shideler SE, Czekala NM, Benirschke K, Lasley BL. Urinary estrogens during pregnancy of the ruffed lemur (Lemur variegatus). Biol Reprod 1983;28:963-969
46. Chambers PL, Hearn JP. Peripheral plasma levels of progesterone, oestradiol-17 beta, oestrone, testosterone, androstenedione and chorionic gonadotrophin during pregnancy in the marmoset monkey, Callithrix jacchus. J Reprod Fertil 1979;56:23-32
47. Reyes FI, Winter JS, Faiman C, Hobson WC. Serial serum levels of gonadotropins, prolactin and sex steroids in the nonpregnant and pregnant chimpanzee. Endocrinology 1975;96:1447-1455
48. Smith R, Wickings EJ, Bowman ME, et al. Corticotropin-releasing hormone in chimpanzee and gorilla pregnancies. J Clin Endocrinol Metab 1999;84:2820-2825
49. Goncharov N, Katzija G, Todua T. Peripheral plasma levels of 12 steroids during pregnancy in the baboon (Papio hamadryas). Eur J Obstet Gynecol Reprod Biol 1980;11: 201-208
50. Stevens VC. Some reproductive studies in the baboon. Hum Reprod Update 1997;3:533-540
51. Hodgen GD, Dufau ML, Catt KJ, Tullner WW. Estrogens, progesterone and chorionic gonadotropin in pregnant rhesus monkeys. Endocrinology 1972;91:896-900
52. Bosu WT, Johansson ED, Gemzell C. Patterns of circulating oestrone, oestradiol-17beta and progesterone during pregnancy in the rhesus monkey. Acta Endocrinol (Copenh) 1973;74:743-755
53. Atkinson LE, Hotchkiss J, Fritz GR, et al. Circulating levels of steroids and chorionic gonadotropin during pregnancy in the rhesus monkey, with special attention to the rescue of the corpus luteum in early pregnancy. Biol Reprod 1975;12:335-345
54. Monfort SL, Hess DL, Shideler SE, et al. Comparison of serum estradiol to urinary estrone conjugates in the rhesus macaque (Macaca mulatta). Biol Reprod 1987;37: 832-837
55. Ryan KJ, Hopper BR. Placental biosynthesis and metabolism of steroid hormones in primates. Contrib Primatol 1974;3: 258-283
56. Shackleton CH, Mitchell FL. The comparison of perinatal steroid endocrinology in simians with a view to finding a suitable animal model to study human problems. Laboratory Animal Handbooks 1975;6:159-181
57. Solomon S, Leung K. Steroid hormones in non-human primates during pregnancy. Acta Endocrinol Suppl (Copenh) 1972;166:178-190
58. Hodgen GD, Tullner WW. Plasma estrogens, progesterone and chorionic gonadotropin in pregnant rhesus monkeys (Macaca mulatta) after ovariectomy. Steroids 1975;25:275-282
59. Resko JA, Pleom JG, Stadelman HL. Estrogens in fetal and maternal plasma of the rhesus monkey. Endocrinology 1975;97:425-430
60. Challis JR, Hartley P, Johnson P, et al. Steroids in the amniotic fluid of the rhesus monkey (Macaca mulatta). J Endocrinol 1977;73:355-363
61. Walsh SW, Stanczyk FZ, Novy MJ. Daily hormonal changes in the maternal, fetal, and amniotic fluid compartments before parturition in a primate species. J Clin Endocrinol Metab 1984;58:629-639
62. Heinrichs WL, Colas AE. Hepatic microsomal 16-alpha-hydroxylation of 3-beta-hydroxyandrost-5-en-17-one (DHA) by fetal, newborn, and adult rhesus monkeys. Gen Comp Endocrinol 1970;14:159-163
63. Seron-Ferre M, Taylor NF, Rotten D, Koritnik DR, Jaffe RB. Changes in fetal rhesus monkey plasma dehydroepiandrosterone sulfate: relationship to gestational age, adrenal weight and preterm delivery. J Clin Endocrinol Metab 1983; 57:1173-1178
64. Walsh SW, Ducsay CA, Novy MJ. Circadian hormonal interactions among the mother, fetus, and amniotic fluid. Am J Obstet Gynecol 1984;150:745-753
65. Hess DL, Spies HG, Hendrickx AG. Diurnal steroid patterns during gestation in the rhesus macaque: onset, daily variation, and the effects of dexamethasone treatment. Biol Reprod 1981;24:609-616
66. Challis JR, Socol M, Murata Y, Manning FA, Martin CB Jr. Diurnal variations in maternal and fetal steroids in pregnant rhesus monkeys. Endocrinology 1980;106:1283-1288
67. Gorwill RH, Snyder DL, Lindholm UB, Jaffe RB. Metabolism of pregnenolone-4-14C and pregnenolone-7-alpha-3H sulfate by the Macaca mulatta fetal adrenal in vitro. Gen Comp Endocrinol 1971;16:21-29
68. Kittinger GW, Beamer NB. Ontogeny of adrenal function in fetal and neonatal rhesus monkeys: in vitro corticosteroidogenesis. Endocrinology 1971;89:86-9S
69. Jaffe RB, Seron-Ferre M, Huhtaniemi I, Korenbrot C. Regulation of the primate fetal adrenal gland and testis in vitro and in vivo. J Steroid Biochem 1977;8:479-490
70. Bosu WT, Johansson ED, Gemzell C. Peripheral plasma levels of oestrogen and progesterone in pregnant rhesus monkeys treated with dexamethasone. Acta Endocrinol (Copenh) 1973;74:338-347
71. Walsh SW, Norman RL, Novy MJ. In utero regulation of rhesus monkey fetal adrenals: effects of dexamethasone, adrenocorticotropin, thyrotropin-releasing hormone, prolactin, human chorionic gonadotropin, and alpha-melanocyte- stimulating hormone on fetal and maternal plasma steroids. Endocrinology 1979;104:1805-1813
72. Novy MJ, Walsh SW. Dexamethasone and estradiol treatment in pregnant rhesus macaques: effects on gestational length, maternal plasma hormones, and fetal growth. Am J Obstet Gynecol 1983;145:920-931
73. Walsh SW, Resko JA, Grumbach MM, Novy MJ. In utero evidence for a functional fetoplacental unit in rhesus monkeys. Biol Reprod 1980;23:264-270
74. Tullner WW, Gulyas BJ, Hodgen GD. Maternal estrogen and progesterone levels after hypophysectomy in early pregnancy and in term fetuses or newborn monkeys. Steroids 1975;26:625-633
75. Tullner WW, Hodgen GD. Effects of fetectomy on plasma estrogens and progesterone in monkeys (Macaca mulatta). Steroids 1974;24:887-897
76. Bosu WT, Johansson ED, Gemzell C. Influence of oophorectomy, luteectomy, foetal death and dexamethasone on the peripheral plasma levels of oestrogens and progesterone in the pregnant Macaca mulatta. Acta Endocrinol (Copenh) 1974;75:601-616
77. Novy MJ, Walsh SW, Kittinger GW. Experimental fetal anencephaly in the rhesus monkey: effect on gestational length and fetal and maternal plasma steroids. J Clin Endocrinol Metab 1977;45:1031-1038
78. Walsh SW, Kittinger GW, Novy MJ. Maternal peripheral concentrations of estradiol, estrone, cortisol, and progesterone during late pregnancy in rhesus monkeys (Macaca mulatta) and after experimental fetal anencephaly and fetal death. Am J Obstet Gynecol 1979;135:37-42
79. Dawood MY, Fuchs F. Estradiol and progesterone in the maternal and fetal circulation in the baboon. Biol Reprod 1980;22:179-184
80. Merkatz IR, Beling CG. Urinary excretion of oestrogens and pregnanediol in the pregnant baboon. J Reprod Fertil Suppl 1969;6:129-13S
81. Albrecht ED, Haskins AL, Pepe GJ. The influence of fetectomy at midgestation upon the serum concentrations of progesterone, estrone, and estradiol in baboons. Endocrinology 1980;107:766-770
82. Pepe GJ, Waddell BJ, Albrecht ED. Effect of estrogen on pituitary peptide-induced dehydroepiandrosterone secretion in the baboon fetus at midgestation. Endocrinology 1989; 125:1519-1524
83. Crystle CD, Townsley JD. The effect of increasing maternal dehydroepiandrosterone sulfate on estrogen synthesis by pregnant baboons. Endocrinology 1974;94:1743-1745
84. Schut HA, Pepe GJ, Chez RA, Townsley JD. Contribution of dehydroepiandrosterone and its sulfate to estradiol in baboon pregnancy. Am J Physiol 1978;235:E78-E81
85. Waddell BJ, Albrecht ED, Pepe GJ. Utilization of maternal and fetal androstenedione for placental estrogen production at mid and late baboon pregnancy. J Steroid Biochem Mol Biol 1992;41:171-178
86. Kling OR, Rubin EJ, Townsley JD. Estrogen synthesis by the pregnant baboon. J Med Primatol 1972;1:102-113
87. Aberdeen GW, Leavitt MG, Pepe GJ, Albrecht ED. Effect of maternal betamethasone administration at midgestation on baboon fetal adrenal gland development and adrenocorticotropin receptor messenger ribonucleic acid expression. J Clin Endocrinol Metab 1998;83:976-982
88. Castracane VD. The effect of dexamethasone administration at different stages of gestation on maternal plasma steroid concentrations in the baboon (Papio cynocephalus). Hum Reprod 1998;13:2282-2285
89. Townsley JD, Pepe GJ. Serum dehydroepiandrosterone and dehydroepiandrosterone sulphate in baboon (Papio Papio) pregnancy. Acta Endocrinol (Copenh) 1977;85:415-421
90. Albrecht ED, Pepe GJ. The placenta remains functional following fetectomy in baboons. Endocrinology 1985;116: 843-845
91. Babischkin JS, Pepe GJ, Albrecht ED. Estrogen regulation of placental P-450 cholesterol side-chain cleavage enzyme messenger ribonucleic acid levels and activity during baboon pregnancy. Endocrinology 1997;138:452-459
92. O'Neil JS, Green AE, Edwards DE, et al. Regulation of leptin and leptin receptor in baboon pregnancy: effects of advancing gestation and fetectomy. J Clin Endocrinol Metab 2001;86:2518-2524
93. Putney DJ, Pepe GJ, Albrecht ED. Influence of the fetus and estrogen on serum concentrations and placental formation of insulin-like growth factor I during baboon pregnancy. Endocrinology 1990;127:2400-2407
94. Pepe GJ, Albrecht ED. Regulation of baboon fetal adrenal androgen production by adrenocorticotropic hormone, prolactin, and growth hormone. Biol Reprod 1985;33:545-550
95. 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
96. Berghorn KA, Albrecht ED, Pepe GJ. Activation of the baboon fetal pituitary-adrenocortical axis at midgestation by estrogen: responsivity of the fetal adrenal gland to adrenocorticotropic hormone in vitro. Biol Reprod 1995;53:996-1002
97. Aberdeen GW, Babischkin JS, Davies WA, Pepe GJ, Albrecht ED. Decline in adrenocorticotropin receptor messenger ribonucleic acid expression in the baboon fetal adrenocortical zone in the second half of pregnancy. Endocrinology 1997;138:1634-1641
98. Lanman JT. The fetal zone of the adrenal. Its developmental course, comparative anatomy, and possible physiology function. Medicine 1953;32:389-430
99. Hill WCO. Observations on the growth of the suprarenal cortex. J Anat 1930;64:479-502
100. Blackman SS Jr. Concerning the function and origin of the reticular zone of the adrenal cortex. Bull Johns Hopkins Hosp 1946;78:180-216
101. Howard E. The X zone of the suprarenal cortex in relation to gonadal maturation in monkeys and mice and to epiphyseal unions in monkeys. Anat Rec 1930;46:93-104
102. Benirschke K, Richart R. Observations on the fetal adrenals of marmoset monkeys. Endocrinology 1964;74: 382-387
103. Levine J, Wolfe LG, Schiebinger RJ, Loriaux DL, Cutler GB Jr. Rapid regression of fetal adrenal zone and absence of adrenal reticular zone in the marmoset. Endocrinology 1982; 111:1797-1802
104. Pryce CR, Palme R, Feldon J. Development of pituitary-adrenal endocrine function in the marmoset monkey: infant hypercortisolism is the norm. J Clin Endocrinol Metab 2002; 87:691-699
105. McNulty WP, Novy MJ, Walsh SW. Fetal and postnatal development of the adrenal glands in Macaca mulatta. Biol Reprod 1981;25:1079-1089
106. Pepe GJ, Titus JA, Townsley JD. Increasing fetal adrenal formation of cortisol from pregnenolone during baboon (Papio papio) gestation. Biol Reprod 1977;17:701-705
107. Leavitt MG, Albrecht ED, Pepe GJ. Development of the baboon fetal adrenal gland: regulation of the ontogenesis of the definitive and transitional zones by adrenocorticotropin. J Clin Endocrinol Metab 1999;84:3831-3835
108. Coulter CL, Read LC, Barry SJ, Tarantal AF, Styne DM. Role of hypothalamic-pituitary axis in EGF action on maturation of adrenal gland in fetal rhesus monkey in vivo. Pediatr Res 2001;50:210-216
109. Coulter CL, Read LC, Carr BR, et al. A role for epidermal growth factor in the morphological and functional maturation of the adrenal gland in the fetal rhesus monkey in vivo. J Clin Endocrinol Metab 1996;81:1254-1260
110. Mesiano S, Coulter CL, Jaffe RB. Localization of cytochrome P450 cholesterol side-chain cleavage, cytochrome P450 17 alpha-hydroxylase/17,20- lyase, and 3 beta-hydroxysteroid dehydrogenase isomerase steroidogenic enzymes in human and rhesus monkey fetal adrenal glands: reappraisal of functional zonation. J Clin Endocrinol Metab 1993;77: 1184-1189
111. Coulter CL, Goldsmith PC, Mesiano S, et al. Functional maturation of the primate fetal adrenal in vivo. II. Ontogeny of corticosteroid synthesis is dependent upon specific zonal expression of 3 beta-hydroxysteroid dehydrogenase/isomerase. Endocrinology 1996;137:4953-4959
112. Mapes S, Tarantal AF, Parker CR, et al. Adrenocortical cytochrome b5 expression during fetal development of the rhesus macaque. Endocrinology 2002;143:1451-1458
113. Narasaka T, Suzuki T, Moriya T, Sasano H. Temporal and spatial distribution of corticosteroidogenic enzymes immunoreactivity in developing human adrenal. Mol Cell Endocrinol 2001;174:111-120
114. Kerr GR, Allen JR, Scheffler G, Couture J. Fetal and postnatal growth of rhesus monkeys (M. mulatta). J Med Primatol 1974;3:221-235
115. Pattison JC, Abbott DH, Saltzman W, et al. Male marmoset monkeys express an adrenal fetal zone at birth, but not a zona reticularis in adulthood. Endocrinology 2004 Sep 30 [Epub ahead of print] PMID: 15459122
116. Ibanez L, DiMartino-Nardi J, Potau N, Saenger P. Premature adrenarche-normal variant or forerunner of adult disease? Endocr Rev 2000;21:671-696
117. Ilondo MM, Vanderschueren-Lodeweyckx M, Vlietinck R, et al. Plasma androgens in children and adolescents. Part I: control subjects. Horm Res 1982;16:61-77
118. Kelnar CJ, Brook CG. A mixed longitudinal study of adrenal steroid excretion in childhood and the mechanism of adrenarche. Clin Endocrinol (Oxf) 1983;19:117-129
119. Sizonenko PC, Paunier L, Carmignac D. Hormonal changes during puberty. IV. Longitudinal study of adrenal androgen secretions. Horm Res 1976;7:288-302
120. Remer T, Manz F. The midgrowth spurt in healthy children is not caused by adrenarche. J Clin Endocrinol Metab 2001; 86:4183-4186
121. Remer T, Manz F. Role of nutritional status in the regulation of adrenarche. J Clin Endocrinol Metab 1999;84: 3936-3944
122. Palmert MR, Hayden DL, Mansfield MJ, et al. The longitudinal study of adrenal maturation during gonadal suppression: evidence that adrenarche is a gradual process. J Clin Endocrinol Metab 2001;86:4536-4542
123. Gell JS, Carr BR, Sasano H, et al. Adrenarche results from development of a 3beta-hydroxysteroid dehydrogenase-deficient adrenal reticularis. J Clin Endocrinol Metab 1998; 83:3695-3701
124. Gell JS, Atkins B, Margraf L, et al. Adrenarche is associated with decreased 3beta-hydroxysteroid dehydrogenase expression in the adrenal reticularis. Endocr Res 1996;22:723-728
125. Smith CJ, Norman RL. Circadian periodicity in circulating cortisol is absent after orchidectomy in rhesus macaques. Endocrinology 1987;121:2186-2191
126. Smith CJ, Norman RL. Influence of the gonads on cortisol secretion in female rhesus macaques. Endocrinology 1987; 121:2192-2198
127. 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
128. Kemnitz JW, Roecker EB, Haffa AL, et al. Serum dehydroepiandrosterone sulfate concentrations across the life span of laboratory-housed rhesus monkeys. J Med Primatol 2000;29:330-337
129. Lashansky G, Saenger P, Fishman K, et al. Normative data for adrenal steroidogenesis in a healthy pediatric population: age- and sex-related changes after adrenocorticotropin stimulation. J Clin Endocrinol Metab 1991;73:674-686
130. Small PJ, Faiman C, Hobson WC, Fuller GB, Winter JS. Further studies on adrenarche in nonhuman primates. Endocrinology 1982;111:844-848
131. Winter JS, Faiman C, Hobson WC, Reyes FI. The endocrine basis of sexual development in the chimpanzee. J Reprod Fertil Suppl 1980;28(Suppl):131-138
132. Copeland KC, Eichberg JW, Parker CR Jr, Bartke A. Puberty in the chimpanzee: somatomedin-C and its relationship to somatic growth and steroid hormone concentrations. J Clin Endocrinol Metab 1985;60:1154-1160
133. Auchus RJ, Rainey WE. Adrenarche - physiology, biochemistry and human disease. Clin Endocrinol (Oxf) 2004; 60:288-296
134. Castracane VD, Cutler GB Jr, Loriaux DL. Pubertal endocrinology of the baboon: adrenarche. Am J Physiol 1981;241:E305-E309
135. Koritnik DR, Laherty RF, Rotten D, Jaffe RB. A radioimmunoassay for dehydroepiandrosterone sulfate in the circulation of rhesus monkeys. Steroids 1983;42:653-667
136. Sapolsky RM, Vogelman JH, Orentreich N, Altmann J. Senescent decline in serum dehydroepiandrosterone sulfate concentrations in a population of wild baboons. J Gerontol 1993;48:B196-B200
137. Parker CR Jr, Slayden SM, Azziz R, et al. Effects of aging on adrenal function in the human: responsiveness and sensitivity of adrenal androgens and cortisol to adrenocorticotropin in premenopausal and postmenopausal women. J Clin Endocrinol Metab 2000;85:48-54
138. Giordano R, Di Vito L, Lanfranco F, et al. Elderly subjects show severe impairment of dehydroepiandrosterone sulphate and reduced sensitivity of cortisol and aldosterone response to the stimulatory effect of ACTH(1-24). Clin Endocrinol (Oxf) 2001;55:259-265
139. Peterson JK, Moran F, Conley AJ, Bird IM. Zonal expression of endothelial nitric oxide synthase in sheep and rhesus adrenal cortex. Endocrinology 2001;142:5351-5363
140. Bird IM, Mason JI, Rainey WE. Battle of the kinases: integration of adrenal responses to cAMP, DG and Ca2+ at the level of steroidogenic cytochromes P450 and 3betaHSD expression in H295R cells. Endocr Res 1998;24:345-354
141. Parker CR Jr, Jian M, Conley AJ. The localization of DHEA sulfotransferase in steroidogenic and steroid metabolizing tissues of the adult rhesus macaque monkey. Endocr Res 2000;26:517-522
142. Hornsby PJ. Biosynthesis of DHEAS by the human adrenal cortex and its age-related decline. Ann N Y Acad Sci 1995; 774:29-46
143. Hornsby PJ. Cellular senescence and tissue aging in vivo. J Gerontol A Biol Sci Med Sci 2002;57:B251-B256
144. Parker CR Jr, Mixon RL, Brissie RM, Grizzle WE. Aging alters zonation in the adrenal cortex of men. J Clin Endocrinol Metab 1997;82:3898-3901
145. Lane MA, Ingram DK, Ball SS, Roth GS. Dehydroepiandrosterone sulfate: a biomarker of primate aging slowed by calorie restriction. J Clin Endocrinol Metab 1997;82:2093-2096
146. Lane MA, Ingram DK, Roth GS. Effects of aging and long-term calorie restriction on DHEA and DHEA sulfate in rhesus monkeys. Ann N Y Acad Sci 1995;774:319-322
147. Muehlenbein MP, Campbell BC, Richards RJ, et al. Dehydroepiandrosterone- sulfate as a biomarker of senescence in male non-human primates. Exp Gerontol 2003;38: 1077-1085
148. Muehlenbein MP, Campbell BC, Phillippi KM, et al. Reproductive maturation in a sample of captive male baboons. J Med Primatol 2001;30:273-282
149. 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
150. Goncharova ND, Lapin BA. Age-related endocrine dysfunction in nonhuman primates. Ann N Y Acad Sci 2004; 1019:321-325
151. Shideler SE, Gee NA, Chen J, Lasley BL. Estrogen and progesterone metabolites and follicle-stimulating hormone in the aged macaque female. Biol Reprod 2001;65:1718-1725
152. Gust DA, Wilson ME, Stocker T, et al. Activity of the hypothalamic-pituitary-adrenal axis is altered by aging and exposure to social stress in female rhesus monkeys. J Clin Endocrinol Metab 2000;85:2556-2563
153. Goncharova ND, Lapin BA. Effects of aging on hypothalamic-pituitary- adrenal system function in non-human primates. Mech Ageing Dev 2002;123:1191-1201
154. Albertson BD, Hobson WC, Burnett BS, et al. Dissociation of cortisol and adrenal androgen secretion in the hypophysectomized, adrenocorticotropin- replaced chimpanzee. J Clin Endocrinol Metab 1984;59:13-18
155. Mapes S, Corbin CJ, Tarantal A, Conley A. The primate adrenal zona reticularis is defined by expression of cytochrome b5, 17alpha-hydroxylase/17, 20-lyase cytochrome P450 (P450c17) and NADPH-cytochrome P450 reductase (reductase) but not 3beta-hydroxysteroid dehydrogenase/ delta5-4 isomerase (3beta-HSD). J Clin Endocrinol Metab 1999;84:3382-3385
156. Saltzman W, Prudom SL, Schultz-Darken NJ, Wittwer DJ, Abbott DH. Social suppression of cortisol in female marmoset monkeys: role of circulating ACTH levels and glucocorticoid negative feedback. Psychoneuroendocrinology 2004;29:141-161
157. Giussani DA, Farber DM, Jenkins SL, et al. Opposing effects of androgen and estrogen on pituitary-adrenal function in nonpregnant primates. Biol Reprod 2000;62: 1445-1451
158. Hirst JJ, West NB, Brenner RM, Novy MJ. Steroid hormone receptors in the adrenal glands of fetal and adult rhesus monkeys. J Clin Endocrinol Metab 1992;75:308-314
159. van Lier E, Meikle A, Bielli A, et al. Sex differences in oestrogen receptor levels in adrenal glands of sheep during the breeding season. Domest Anim Endocrinol 2003;25: 373-387
160. Vanttinen T, Kuulasmaa T, Liu J, Voutilainen R. Expression of activin/inhibin receptor and binding protein genes and regulation of activin/inhibin peptide secretion in human adrenocortical cells. J Clin Endocrinol Metab 2002;87:4257-4263
161. Vanttinen T, Liu J, Kuulasmaa T, Kivinen P, Voutilainen R. Expression of activin/inhibin signaling components in the human adrenal gland and the effects of activins and inhibins on adrenocortical steroidogenesis and apoptosis. J Endocrinol 2003;178:479-489
162. Arola J, Liu J, Heikkila P, Voutilainen R, Kahri A. Expression of inhibin alpha in the human adrenal gland and adrenocortical tumors. Endocr Res 1998;24:865-867
163. Munro LM, Kennedy A, McNicol AM. The expression of inhibin/activin subunits in the human adrenal cortex and its tumours. J Endocrinol 1999;161:341-347
164. Brand C, Souchelnytskiy S, Chambaz EM, Feige JJ, Bailly S. Smad3 is involved in the intracellular signaling pathways that mediate the inhibitory effects of transforming growth factor-beta on StAR expression. Biochem Biophys Res Commun 1998;253:780-785
165. Wang EY, Ma EY, Woodruff TK. Activin signal transduction in the fetal rat adrenal gland and in human H295R cells. J Endocrinol 2003;178:137-148
166. Chen W, Woodruff TK, Mayo KE. Activin A-induced HepG2 liver cell apoptosis: involvement of activin receptors and smad proteins. Endocrinology 2000;141:1263-1272
167. Spencer SJ, Mesiano S, Lee JY, Jaffe RB. Proliferation and apoptosis in the human adrenal cortex during the fetal and perinatal periods: implications for growth and remodeling. J Clin Endocrinol Metab 1999;84:1110-1115
168. Beuschlein F, Looyenga BD, Bleasdale SE, et al. Activin induces x-zone apoptosis that inhibits luteinizing hormone-dependent adrenocortical tumor formation in inhibin-deficient mice. Mol Cell Biol 2003;23:3951-3964
169. Leblanc M, Labrie C, Belanger A, Candas B, Labrie F. Bioavailability and pharmacokinetics of dehydroepiandrosterone in the cynomolgus monkey. J Clin Endocrinol Metab 2003;88:4293-4302
170. Neville AM, O'Hare MJ. The Human Adrenal Cortex. Berlin: Springer-Verlag; 1982
171. 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