Effect of ovarian aging on androgen biosynthesis in a cynomolgus macaque model

Climacteric

Volumn 15, Issue 1, 2012, Pages 82-92

  Ethun, K F ^a   Wood, C E ^a   Parker, C R ^b   Kaplan, J R ^a   Chen, H ^a   Appt, S E ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

aging; animal model; follicles; immunohistochemistry; Menopause; monkey; ovarian reserve

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ANDROGEN; ANDROSTENEDIONE; CYTOCHROME B5; CYTOCHROME P450C17; TESTOSTERONE;

AGING; ANDROGEN BLOOD LEVEL; ANDROGEN SYNTHESIS; ANDROGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; MACACA FASCICULARIS; NONHUMAN; OVARIECTOMY; OVARY; OVARY FOLLICLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

EID: 84855238162     PISSN: 13697137     EISSN: 14730804     Source Type: Journal    
DOI: 10.3109/13697137.2011.571321     Document Type: Article

References (64)

1. Zumoff B, Strain GW, Miller LK, Rosner W. Twenty-four-hour mean plasma testosterone concentration declines with age in normal premenopausal women. J Clin Endocrinol Metab 1995;80:1429-30
2. 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;90:3847-53 (Pubitemid 41058142)
3. Erickson GF, Magoffi n DA, Dyer CA, Hofeditz C. The ovarian androgen producing cells: A review of structure/function relationships. Endocrine Rev 1985;6:371-99
4. Magoffi n DA. Ovarian theca cell. I nt J Biochem 2005;37: 1344-9
5. Richardson SJ, Senikas V, Nelson JF. Follicular depletion during the menopause transition: Evidence for accelerated loss and ultimate exhaustion. J Clin Endocrinol Metab 1987;65:1231-7 (Pubitemid 18026863)
6. Adashi EY. The climacteric ovary as a functional gonadotropin- driven androgen-producing gland. Fertil Steril 1994;62:20-7 (Pubitemid 24198053)
7. Couzinet B, Meduri G, Lecce MG, e t al The postmenopausal ovary is not a major androgen-producing gland. J Clin Endocrinol Metab 2001;86:5060-6 (Pubitemid 33020564)
8. Jabara S, Christenson LK, Wang CY, e t al Stromal cells of the human postmenopausal ovary display a distinctive biochemical and molecular phenotype. J Clin Endrocrinol Metab 2003;88:484-92 (Pubitemid 36115206)
9. Havelock JC, Rainey WE, Bradshaw KD, Carr BR. The post-menopausal ovary displays a unique pattern of steroidogenic enzyme expression. Hum Reprod 2006;21:309-17 (Pubitemid 41794326)
10. Hall PF. Cytochrome P-450 c 21scc : One enzyme with two actions: Hydroxylase and lyase. J Steriod Biochem Molec Biol 1991;40: 527-32
11. Conley AJ, Bird IM. The role of cytochrome P450 17á-hydroxylase and 3 ǎ -hydroxysteroid dehydrogenase in the integration of gondal and adrenal steroidogenesis via the Ä5 and Ä4 pathways of steroidogenesis in mammals. Biol Reprod 1997;56: 789-99 (Pubitemid 27150405)
12. Katagiri M, Kagawa N, Waterman MR. The role of cytochrome b 5 in the biosynthesis of androgens by human P450c17. Arch Biochem Biophys 1995;317:343-7
13. Lee-Robichaud P, Wright JN, Akhtar ME, Akhtar M. Modulation of the activity of human 17 á -hydroxylase-17,20-lyase (CYP17) by cytochrome b 5 : Endocrinological and mechanistic implications. Biochem J 1995;308:901-8
14. Auchus RJ, Lee TC, Miller WL. Cytochrome b 5 augments the 17,20-lyase activity of human P450c17 without direct electron transfer. J Biol Chem 1998;273:3158-65 (Pubitemid 28109723)
15. Doody KJ, Lorence MC, Mason JI, Simpson ER. Expression of messenger ribonucleic acid species encoding steroidogenic enzymes in human follicles and corpora lutea throughout the menstrual cycle. J Clin Endocrinol Metab 1990;70:1041-5
16. Rhéaume E, Lachance Y, Zhao HF, e t al Structure and expression of a new complementary DNA encoding the almost exclusive 3 beta-hydroxysteroid dehydrogenase/delta 5-delta 4-isomerase in human adrenals and gonads. Mol Endocrinol 1991;5: 1147-57
17. Dharia S, Slane A, Jian M, Conner M, Conley AJ, Parker CP. Colocalization of P450c17 and cytochrome b5 in androgensynthesizing tissues of the human. Biol Reprod 2004;71:83-8 (Pubitemid 38915312)
18. Davis SR, McCloud P, Strauss BJ, Burger H. Testosterone enhances estradiol' s effects on postmenopausal bone density and sexuality. Maturitas 1995;21:227-36
19. Žofková I, Bahbouh R, Hill M. The pathophysiological implications of circulating androgens on bone mineral density in a normal female population. Steroids 2000;65:857-61
20. Notelovitz M. Androgen effects on bone and muscle. F ertil Steril 2002;77:S34-40
21. Bachmann GA, Leiblum SR. The impact of hormones on menopausal sexuality: A literature review. Menopause 2004;11: 120-30 (Pubitemid 40362209)
22. Tok EC, Ertunc D, Oz U, Camdeviren H, Ozdemir G, Dilek S. The effect of circulating androgens on bone mineral density in postmenopausal women. Maturitas 2004;48:235-42 (Pubitemid 38786464)
23. Will MA, Randolph JF. The infl uence of reproductive hormones on brain function in the menopausal transition. Minerva Ginecol 2009;61:469-81
24. Liu Y, Ding J, Bush TL, et al Relative androgen excess and increased cardiovascular risk after menopause: A hypothesized relation. Am J Epidemiol 2001;154:489-94 (Pubitemid 32867947)
25. Torré ns JI, Sutton-Tyrrell K, Zhao X, e t al Relative androgen excess during the menopausal transition predicts incident metabolic syndrome in midlife women: Study of Women's Health Across the Nation. Menopause 2008;16:257-64
26. Shifren JL, Braunstein GD, Simon JA, et al Transdermal testerosterone treatment in women with impaired sexual function after oophorectomy. N Engl J Med 2000;343:682-8
27. Shifren JL. Androgen defi ciency in the oophorectomized women. Fertil Steril 2002;77:S60-2 (Pubitemid 34465845)
28. Corner GW. Ovulation and menstruation in Macacus rhesus. Contrib Embryol 1923;15:73-102
29. Martel C, Melner MH, Gagné D, Simard J, Labrie F. Widespread tissue distribution of steroid sulfatase, 3 beta-hydroxysteroid dehydrogenase/delta 5-delta 4 isomerase (3 beta-HSD), 17 beta- HSD 5 alpha-reductase and aromatase activities in the rhesus monkey. Mol Cell Endocrinol 1994;104:103-11
30. Gilardi KVK, Shideler SE, Valverde CR, Roberts JA, Lasley BL. Characterization of the onset of menopause in the rhesus macaque. Biol Reprod 1997;57:335-40 (Pubitemid 27343692)
31. Kavanagh K, Williams JK, Wagner JD. Naturally occurring menopause in cynomolgus monkeys: Changes in hormone, lipid, and carbohydrate measures with hormonal status. J Med Primatol 2005;34:171-7 (Pubitemid 40932216)
32. Nichols SM, Bavister BD, Brenner CA, Didier PJ, Harrison RM, Kubisch HM. Ovarian senescence in the rhesus monkey ( Macaca mulatta ). Hum Reprod 2005;20:79-83
33. Shideler SE, Gee NA, Chen J, Lasley BL. Estrogen and progesterone metabolites and follicle stimulating hormone in the aged macaque female. Biol Reprod 2001;65:1718-25 (Pubitemid 33081661)
34. Lees CJ, Kaplan JR, Chen H, Jerome CP, Register TC, Franke AA. Bone mass and soy isofl avones in socially housed, premenopausal macaques. Am J Clin Nutr 2007;86:245-50 (Pubitemid 47041617)
35. Walker SE, Register TC, Appt SE, e t al Plasma lipid-dependent and -independent effects of dietary soy protein and social status on atherogenesis in premenopausal monkeys: Implications for postmenopausal atherosclerosis burden. Menopause 2008;15: 950-7
36. Appt SE, Chen H, Goode AK, e t al The effect of diet and cardiovascular risk on ovarian aging in cynomolgus monkeys ( Macaca fascicularis ). Menopause 2010;17:741-8
37. Kaplan JR, Chen H, Appt SE, e t al Impairment of ovarian function and associated health-related abnormalities are attributed to low social status in premenopausal monkeys and not mitigated by a high-isofl avone soy diet. Hum Reprod 2010;25: 3083-94
38. Miller PB, Charleston JS, Battaglia DE, Klein NA, Soules MR. Morphometric analysis of primordial follicle number in pigtailed monkey ovaries: Symmetry and relationship with age. Biol Reprod 1999;61:553-6 (Pubitemid 29344777)
39. Appt SE, Clarkson TB, Hoyer PB, e t al Experimental induction of reduced ovarian reserve in a nonhuman primate model. Comp Med 2010;60:380-8
40. Buse, E, Zö ller M, Van Esch E. The macaque ovary with special reference to the cynomolgus macaque ( Macaca fascicularis ). Toxicol Pathol 2008 36:24-66.S.
41. Judd, HL, Lucas WE, Yen SSC. Effect of oophorectomy on circulating testosterone and androstenedione levels in patients with endometrial cancer Am J Obstet Gynecol 1974 118 793-8
42. Fogle RH, Stanczyk FZ, Zhang X, Paulson RJ. Ovarian androgen production in postmenopausal women. J Clin Endocrinol Metab 2007;92:3040-3 (Pubitemid 47236368)
43. Judd HL, Judd GE, Lucas WE, Yen SSC. Endocrine function of the postmenopausal ovary: Concentration of androgens and estrogens in ovarian and peripheral vein blood. J Clin Endocrinol Metab 1974;39:1020-4
44. Vermeulen A. The hormonal activity of the postmenopausal ovary. J Clin Endocrinol Metab 1976;42:247-53
45. Longcope C, Hunter R, Franz C. Steroid secretion by the postmenopausal ovary. Am J Obstet Gynecol 1980;138:564-8 (Pubitemid 11250685)
46. Lucisano A, Acampora MG, Russo N, Maniccia E, Montemurro A, Dell ' Acqua S. Ovarian and peripheral plasma levels of progestogens, androgens and oestrogens in post-menopausal women. Maturitas 1984;6:45-53 (Pubitemid 14088227)
47. Aiman J, Forney JP, Parker CR Jr.. Secretion of androgens and estrogens by normal and neoplastic ovaries in postmenopausal women. Obstet Gynecol 1986;68:1-5 (Pubitemid 16090827)
48. Tamura T, Kitawaki J, Yamamoto T, e t al Immunohistochemical localization of 17 á -hydroxylase/C17-20 lyase and aromatase cytochrome P-450 in the human ovary during the menstrual cycle. J Endrocinol 1992;135:589-95
49. Hild-Petito S, West NB, Brenner RM, Stouffer RL. Localization of androgen receptor in the follicle and corpus luteum of the primate ovary during the menstrual cycle. Biol Reprod 1991;44: 561-8
50. Simard J, Melner MH, Breton N, et al Characterization of macaque 3 ǎ -hydroxy-5-ene steroid dehydrogenas/Ä5-Ä4 isomerase: Structure and expression in steroidogenic and peripheral tissues in primate. Mol Cell Endocrinol 1991;75:101-10
51. Sanders SL, Stouffer RL. Localization of steroidogenic enzymes in macaque luteal tissue during the menstrual cycle and stimulated early pregnancy: Immunohistochemical evidence supporting the two-cell model for estrogen production in the primate corpus luteum. Biol Reprod 1997;56;1077-87 (Pubitemid 27184489)
52. Sasano H, Mori T, Sasano N, Nagura H, Mason JI. Immunolocalization of 3 ǎ -hydroxysteroid dehydrogenase in human ovary. J Reprod Fertil 1990;89:743-51 (Pubitemid 20238693)
53. Dupont E, Labrie F, Luu-The V, Pelletier G. Immunocytochemical localization of 3 ǎ -hydroxysteroid dehydrogenase/ Ä5-Ä4- isomerase in human ovary. J Clin Endocrinol Metab 1992;74:994-8
54. Laughlin GA, Barrett-Connor E, Kritz-Silverstein D, von Mü hlen D. Hysterectomy, oophorectomy, and endogenous sex hormone levels in older women: The Rancho Bernardo Study. J Clin Endocrinol Metab 2000;85:645-51 (Pubitemid 32273648)
55. Cappola AR, Ratcliffe SJ, Bhasin S, e t al Determinants of serum total and free testosterone levels in women over the age of 65 years. J Clin Endocrinol Metab 2007;92:509-16
56. Korse CM, Bonfrer JMG, van Beurden M, Verheijen RHM, Rookus MA. Estradiol and testosterone levels are lower after oophorectomy than after natural menopause. Tumor Biol 2009;30:37-42
57. McTiernan A, Wu L, Barnabei VM, et al Relation of demographic factors, menstrual history, reproduction and medication use to sex hormone levels in postmenopausal women. Breast Cancer Res Treat 2008;108:217-31 (Pubitemid 351311354)
58. Burger HG, Dudley EC, Cui J, Dennerstein L, Hopper JL. A prospective longitudinal study of serum testosterone, dehydroepiandrosterone sulfate, and sex hormone-binding globulin levels through the menopause transition. J Clin Endocrinol Metab 2000;85:2832-8 (Pubitemid 32269161)
59. Sutton-Tyrrell K, Wildman RP, Matthews KA, e t al Sexhormone- binding globulin and the free androgen index are related to cardiovascular risk factors in multiethnic premenopausal and perimenopausal women enrolled in the Study of Women Across the Nation (SWAN). Circulation 2005;111: 1242-9 (Pubitemid 40389087)
60. Sowers MR, Jannausch M, Randolph JF, et al Androgens are associated with hemostatic and infl ammatory factors among women at the mid-life. J Clin Endocrinol Metab 2005;90: 6064-71 (Pubitemid 41606526)
61. Janssen I, Powell LH, Crawford S, Lasley B, Sutton-Tyrrell K. Menopause and the metabolic syndrome. Arch Intern Med 2008;168:1568-75
62. Jongen VH, Sluijmer AV, Heineman MJ. The postmenopausal ovary as an androgen-producing gland; hypothesis on the etiology of endometrial cancer. Maturitas 2002;43:77-85 (Pubitemid 35217766)
63. Zumoff B, Rosenfeld RS, Strain GW, e t al Sex differences in the twenty-four hour mean plasma concentrations of dehydroisoandrosterone (DHA) and dehydroiandrosterone sulfate (DHAS) and the DHA to DHAS ratio in normal adults. J Clin Endocrinol Metab 1980;51:330-3 (Pubitemid 10007644)
64. Labrie F, B é langer A, Cusan L, Gomez J, Candas B. Marked decline in serum concentrations of adrenal C19 sex steroid precursors and conjugated androgen metabolites during aging. J Clin Endocrinol Metab 1997;82:2396-402 (Pubitemid 27337846).