The developmental increase in adrenocortical 17, 20-lyase activity (biochemical adrenarche) is driven primarily by increasing cytochrome b5 in neonatal rhesus macaques

Endocrinology

Volumn 150, Issue 4, 2009, Pages 1748-1756

  Nguyen, Ann D ^a   Corbin, C Jo ^a   Pattison, J Christina ^b   Bird, Ian M ^b   Conley, Alan J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Perinatal Research Laboratories   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; CYTOCHROME B5; CYTOCHROME P450C17; PRASTERONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE; STEROID 17,20 LYASE; STEROID 17ALPHA MONOOXYGENASE; STEROID 21 MONOOXYGENASE;

ADOLESCENT; ADRENAL CORTEX; ADRENARCHE; ANDROGEN SYNTHESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MARMOSET; MICROSOME; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHESUS MONKEY; WESTERN BLOTTING;

3-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELL LINE; CHROMATOGRAPHY, THIN LAYER; CYTOCHROMES B5; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MACACA MULATTA; MICROSOMES; STEROID 17-ALPHA-HYDROXYLASE;

EID: 63849311167     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1303     Document Type: Article

References (65)

1. Cutler GJ, Glenn M, Bush M, Hodgen GD, Graham CE, Loriaux DL 1978 Adrenarche: a survey of rodents, domestic animals, and primates. Endocrinology 103:2112-2118
2. Collins DC, Nadler RD, Preedy JRK 1981 Adrenarche in the great apes. Am J Primatol 1:344 (Abstract)
3. Conley AJ, Pattison JC, Bird IM 2004 Variations in adrenal androgen production among (nonhuman) primates. Semin Reprod Med 22:311-326
4. Smail PJ, Faiman C, Hobson WC, Fuller GB, Winter JS 1982 Further studies on adrenarche in nonhuman primates. Endocrinology 111:844-848
5. Castracane VD, Cutler Jr GB, Loriaux DL 1981 Pubertal endocrinology of the baboon: adrenarche. Am J Physiol 241:E305-E309
6. Arlt W, Martens JW, Song M, Wang JT, Auchus RJ, Miller WL 2002 Molecular evolution of adrenarche: structural and functional analysis of p450c17 from four primate species. Endocrinology 143:4665-4672
7. Abbott DH, Bird IM 6 August 2008 Nonhuman primates as models for human adrenal androgen production: function and dysfunction. Rev Endocr Metab Disord 10.1007/5 11154-008-9099-8
8. Fevold HR, Lorence MC, McCarthy JL, Trant JM, Kagimoto M, Waterman MR, Mason JI 1989 Rat P450(17 a) from testis: characterization of a full- length cDNA encoding a unique steroid hydroxylase capable of catalyzing both δ 4- and δ 5-steroid-17, 20-lyase reactions. Mol Endocrinol 3:968-975
9. Lin D, Black SM, Nagahama Y, Miller WL 1993 Steroid 17 α-hydroxylase and 17, 20-lyaseactivities of P450c17: contributions of serine106 and P450 reductase. Endocrinology 132:2498-2506
10. Brock BJ, Waterman MR 1999 Biochemical differences between rat and human cytochrome P450c17 support the different steroidogenic needs of these two species. Biochemistry 38:1598-1606
11. Fluck CE, Miller WL, Auchus RJ 2003 The 17, 20-lyase activity of cytochrome p450c17 from human fetal testis favors the 85 steroidogenic pathway. J Clin Endocrinol Metab 88:3762-3766
12. Conley AJ, Bird IM 1997 The role of cytochrome P450 17 α-hydroxylase and 3 β-hydroxysteroid dehydrogenase in the integration of gonadal and adrenal steroidogenesis via the δ 5 and δ 4 pathways of steroidogenesis in mammals. Biol Reprod 56:789-799
13. Couch RM, Muller J, Winter JS 1986 Regulation of the activities of 17-hydroxylase and 17, 20-desmolase in the human adrenal cortex: kinetic analysis and inhibition by endogenous steroids. J Clin Endocrinol Metab 63:613-618
14. Auchus RJ, Rainey WE 2004 Adrenarche-physiology, biochemistry and human disease. Clin Endocrinol (Oxf) 60:288-296
15. Onoda M, Hall PF 1982 Cytochrome b5 stimulates purified testicular micro-somal cytochrome P-450 (C21 side-chain cleavage). Biochem Biophys Res Commun 108:454-460
16. Katagiri M, Suhara K, Shiroo M, Fujimura Y 1982 Role of cytochrome b5 in the cytochrome P-450-mediated C21-steroid 17, 20-lyase reaction. Biochem Biophys Res Commun 108:379-384
17. Shinzawa K, Kominami S, Takemori S 1985 Studies on cytochrome P-450 (P-450 17α, lyase) from guinea pig adrenal microsomes. Dual function of a single enzyme and effect of cytochrome b5. Biochim Biophys Acta 833:151-160
18. Lee-Robichaud P, Wright JN, Akhtar ME, Akhtar M 1995 Modulation of the activity of human 17 α-hydroxylase-17, 20-lyase CYP17 by cytochrome b5: endocrinological and mechanistic implications. Biochem J 308(Pt3):901-908
19. Katagiri M, Kagawa N, Waterman MR 1995 The role of cytochrome b5 in the biosynthesis of androgens by human P450c17. Arch Biochem Biophys 317:343-347
20. Auchus RJ, Lee TC, Miller WL1998 Cytochrome b5 augments the 17, 20-lyase activity of human P450c17 without direct electron transfer. J Biol Chem 273:3158-3165
21. Narasaka T, Suzuki T, Moriya T, Sasano H 2001 Temporal and spatial distribution of corticosteroidogenic enzymes immunoreactivity in developing human adrenal. Mol Cell Endocrinol 174:111-120
22. Schiebinger RJ, Albertson BD, Cassorla FG, Bowyer DW, Geelhoed GW, Cutler Jr GB, Loriaux DL 1981 The developmental changes in plasma adrenal androgens during infancy and adrenarche are associated with changing activities of adrenal microsomal 17-hydroxylase and 17, 20-desmolase. J Clin Invest 67:1177-1182
23. Mapes S, Corbin CJ, Tarantal A, Conley A 1999 The primate adrenal zona reticularis is defined by expression of cytochrome b5, 17α- hydroxylase/17, 20-lyase cytochrome P450 (P450c17) and NADPH-cytochrome P450 reductase (reductase) but not 3β-hydroxysteroid dehydrogenase/δ5-4 isomerase (3β-HSD). J Clin Endocrinol Metab 84:3382-3385
24. Mapes S, Tarantal AF, Parker CR, Moran FM, Bahr JM, Pyter L, Conley AJ 2002 Adrenocortical cytochrome b5 expression during fetal development of the rhesus macaque. Endocrinology143:1451-1458
25. Nguyen A, Mapes S, Corbin C, Conley AJ 2008 Morphological adrenarche in rhesus macaques: development of the zona reticularis is concurrent with fetal zone regression in the early neonatal period. J Endocrinol 199:367-378
26. Grigoryev DN, Kato K, Njar VC, Long BJ, Ling YZ, Wang X, Mohler J, Brodie AM 1999 Cytochrome P450c17-expressing Escherichia coli as a first-step screening system for 17α-hydroxylase-C17, 20-lyase inhibitors. Anal Biochem 267:319-330
27. Moran FM, Ford JJ, Corbin CJ, Mapes S, Njar VC, Brodie AM, Conley AJ 2002 Regulation of microsomal P450, redox partner proteins and steroidogenesis in the developing testes of the neonatal pig. Endocrinology 143:3361-3369
28. Pattison JC, Abbott DH, Saltzman W, Nguyen AD, Henderson G, Jing H, Pryce CR, Allen AJ, Conley AJ, Bird IM 2005 Male marmoset monkeys express an adrenal fetal zone at birth, but not a zona reticularis in adulthood. Endocrinology 146:365-374
29. Endoh A, Kristiansen SB, Casson PR, Buster JE, Hornsby PJ 1996 The zona reticularis is the site of biosynthesis of dehydroepiandrosterone and dehydro-epiandrosterone sulfate in the adult human adrenal cortex resulting from its low expression of 3β-hydroxysteroid dehydrogenase. J Clin Endocrinol Metab 81:3558-3565
30. Dharia S, Slane A, Jian M, Conner M, Conley AJ, Parker Jr CR 2004 Colo-calization of P450c17 and cytochrome b5 in androgen-synthesizing tissues of the human. Biol Reprod 71:83-88
31. Seron-Ferre M, Hess DL, Lindholm U, Jaffe RB 1986 Persistence of fetal zone function in the infant rhesus monkey adrenal gland. J Clin Endocrinol Metab 62:460-465
32. Pattison JC, Saltzman W, Abbott DH, Hogan BK, Nguyen AD, Husen B, Einspanier A, Conley AJ, Bird IM 2007 Gender and gonadal status differences in zona reticularis expression in marmoset monkey adrenals: cytochrome b5 localization with respect to cytochrome P450 17, 20-lyase activity. Mol Cell Endocrinol 265-266:93-101
33. Nguyen AD, Conley AJ 2008 Adrenal androgens in humans and nonhuman primates: production, zonation and regulation. Endocr Dev 13:33-54
34. Yanagibashi K, Hall PF 1986 Role of electron transport in the regulation of the lyase activity of C21 side-chain cleavage P-450 from porcine adrenal and testicular microsomes. J Biol Chem 261:8429-8433
35. Pandey AV, Miller WL 2005 Regulation of 17, 20 lyase activity by cytochrome b5 and by serine phosphorylation of P450c17. J Biol Chem 280:13265-13271
36. Naffin-Olivos JL, Auchus RJ 2006 Human cytochrome b5 requires residues E48 and E49 to stimulate the 17, 20-lyase activity of cytochrome P450c17. Biochemistry 45:755-762
37. Shet MS, Fisher CW, Tremblay Y, Belanger A, Conley AJ, Mason JI, Estabrook RW 2007 Comparison of the 17α-hydroxylase/C17, 20-lyaseactivities of porcine, guinea pig and bovine P450c17 using purified recombinant fusion proteins containing P450c17 linked to NADPH-P450 reductase. Drug Metab Rev 39:289-307
38. Kominami S, Ogawa N, Morimune R, De-Ying H, Takemori S 1992 The role of cytochrome b5 in adrenal microsomal steroidogenesis. J Steroid Biochem Mol Biol 42:57-64
39. Sakai Y, Yanase T, Hara T, Takayanagi R, Haji M, Nawata H 1994 In-vitro evidence for the regulation of 17, 20-lyase activity by cytochrome b5 in adrenocortical adenomas from patients with Cushing's syndrome. Clin Endocrinol (Oxf) 40:205-209
40. Yanase T, Sasano H, Yubisui T, Sakai Y, Takayanagi R, Nawata H 1998 Immunohistochemical study of cytochrome b5 in human adrenal gland and in adrenocortical adenomas from patients with Cushing's syndrome. Endocr J 45:89-95
41. Dharia S, Parker Jr CR 2004 Adrenal androgens and aging. Semin Reprod Med 22:361-368
42. Dharia S, Slane A, Jian M, Conner M, Conley AJ, Brissie RM, Parker Jr CR 2005 Effects of aging on cytochrome b5 expression in the human adrenal gland. J Clin Endocrinol Metab 90:4357-4361
43. Soucy P, Luu-The V 2000 Conversion of pregnenolone to DHEA by human 17α-hydroxylase/17, 20-lyase (P450c17). Evidence that DHEA is produced from the released intermediate, 17α-hydroxypregnenolone. Eur J Biochem 267:3243-3247
44. Gell JS, Carr BR, Sasano H, Atkins B, Margraf L, Mason JI, Rainey WE 1998 Adrenarche results from development of a 3β-hydroxysteroid dehydrogenase- deficient adrenal reticularis. J Clin Endocrinol Metab 83:3695-3701
45. Sholl SA 1981 17-Hydroxy progesterone metabolism in the monkey fetal adrenal: C17-20lyase and 21-hydroxylase activities. Steroids 38:221-228
46. Sakai Y, Yanase T, Hara T, Takayanagi R, Haji M, Nawata H 1994 Mechanism of abnormal production of adrenal androgens in patients with adrenocortical adenomas and carcinomas. J Clin Endocrinol Metab 78:36 -40
47. Koritnik DR, Laherty RF, Rotten D, Jaffe RB 1983 A radioimmunoassay for dehydroepiandrosterone sulfate in the circulation of rhesus monkeys. Steroids 42:653-667
48. Seron-Ferre M, Taylor NF, Rotten D, Koritnik DR, Jaffe RB 1983 Changes in fetal rhesus monkey plasma dehydroepiandrosterone sulfate: relationship to gestational age, adrenal weight and preterm delivery. J Clin Endocrinol Metab 57:1173-1178
49. Guillemette C, Hum DW, Belanger A 1996 Levels of plasma C19 steroids and 5 α-reduced C19 steroid glucuronides in primates, rodents, and domestic animals. Am J Physiol 271(2 Pt 1):E348 -E353
50. Schut HA, Pepe GJ, Townsley JD 1978 Clearance and production of dehydro-epiandrosterone and its sulfate in female baboons. Am J Physiol 235:E74-E77
51. Remer T, Boye KR, Hartmann MF, Wudy SA 2005 Urinary markers of adrenarche: reference values in healthy subjects, aged 3-18 years. J Clin Endocrinol Metab 90:2015-2021
52. Benner MC 1940 Studies on the involution of the fetal cortex of the adrenal glands. Am J Pathol 16:787-798
53. Parker Jr CR 1999 Dehydroepiandrosterone and dehydroepiandrosterone sulfate production in the human adrenal during development and aging. Steroids 64:640-647
54. Suzuki T, Sasano H, Takeyama J, Kaneko C, Freije WA, Carr BR, Rainey WE 2000 Developmental changes in steroidogenic enzymes in human postnatal adrenal cortex: immunohistochemical studies. Clin Endocrinol (Oxf) 53:739-747
55. Ibanez L, DiMartino-Nardi J, Potau N, Saenger P 2000 Premature adrenarche- normal variant or forerunner of adult disease? Endocr Rev 21:671-696
56. Palmert MR, Hayden DL, Mansfield MJ, Crigler Jr JF, Crowley Jr WF, Chandler DW, Boepple PA 2001 The longitudinal study of adrenal maturation during gonadal suppression: evidence that adrenarche is a gradual process. J Clin Endocrinol Metab 86:4536-4542
57. Martin DD, Schweizer R, Schwarze CP, Elmlinger MW, Ranke MB, Binder G 2004 The early dehydroepiandrosterone sulfate rise of adrenarche and the delay of pubarche indicate primary ovarian failure in Turner syndrome. J Clin Endocrinol Metab 89:1164-1168
58. de Peretti E, Forest MG 1976 Unconjugated dehydroepiandrosterone plasma levels in normal subjects from birth to adolescence in human: the use of a sensitive radioimmunoassay. J Clin Endocrinol Metab 43:982-991
59. de Peretti E, Forest MG 1978 Pattern of plasma dehydroepiandrosterone sulfate levels in humans from birth to adulthood: evidence for testicular production. J Clin Endocrinol Metab 47:572-577
60. Plant TM, Zorub DS 1982 The role of nongonadal restraint of gonadotropin secretion in the delay of the onset of puberty in the rhesus monkey (Macaca mulatta). J Anim Sci 55(Suppl 2):43-55
61. Sklar CA, Kaplan SL, Grumbach MM 1980 Evidence for dissociation between adrenarche and gonadarche: studies in patients with idiopathic precocious puberty, gonadal dysgenesis, isolated gonadotropin deficiency, and constitutionally delayed growth and adolescence. J Clin Endocrinol Metab 51:548 -556
62. Huang N, Dardis A, Miller WL 2005 Regulation of cytochrome b5 gene transcription by Sp3, GATA-6, and steroidogenic factor 1 in human adrenal NCI-H295A cells. Mol Endocrinol 19:2020 -2034
63. Abbott DH, Dumesic DA, Franks S 2002 Developmental origin of polycystic ovary syndrome-a hypothesis. J Endocrinol 174:1-5
64. Abbott DH, Padmanabhan V, Dumesic DA 2006 Contributions of androgen and estrogen to fetal programming of ovarian dysfunction. Reprod Biol Endocrinol 4:17
65. Abbott DH, Zhou R, Bird IM, Dumesic DA, Conley AJ 2008 Fetal programming of adrenal androgen excess: lessons from a nonhuman primate model of polycystic ovary syndrome. Endocr Dev 13:145-158