Androgen actions in the ovary: Balance is key

Journal of Endocrinology

Volumn 222, Issue 3, 2014, Pages 141-151

  Prizant, Hen ^a   Gleicher, Norbert ^b   Sen, Aritro ^a,b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b CENTER FOR HUMAN REPRODUCTION   (United States)

Author keywords

Androgen; Androgen receptor; Female reproduction; Ovary

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; CYCLIN DEPENDENT KINASE INHIBITOR 1; GROWTH DIFFERENTIATION FACTOR 9; MICRORNA 125B; SOMATOMEDIN; STEM CELL FACTOR; TESTOSTERONE; AMPHIREGULIN; AREG PROTEIN, HUMAN; AREG PROTEIN, MOUSE; CYCLOOXYGENASE 2; EPIDERMAL GROWTH FACTOR DERIVATIVE; FOLLITROPIN RECEPTOR; GLYCOPROTEIN; MICRORNA; SIGNAL PEPTIDE;

ANDROGEN THERAPY; CORPUS LUTEUM; ESTRUS CYCLE; FEMALE FERTILITY; FERTILIZATION IN VITRO; GENE EXPRESSION; GRANULOSA CELL; HORMONE ACTION; HUMAN; HYPOPHYSIS; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; NONHUMAN; OOCYTE; OVARY; OVARY FOLLICLE; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE DEVELOPMENT; OVARY FUNCTION; PERCEPTION; PRIORITY JOURNAL; REPRODUCTION; REPRODUCTIVE HEALTH; REVIEW; SIGNAL TRANSDUCTION; TESTICULAR FEMINIZATION; THECA CELL; X CHROMOSOME; ANIMAL; ANIMAL MODEL; DEFICIENCY; FEMALE; FERTILITY; GENETICS; MOUSE; PHYSIOLOGY;

AMPHIREGULIN; ANDROGENS; ANIMALS; CYCLOOXYGENASE 2; EGF FAMILY OF PROTEINS; FEMALE; FERTILITY; GENE EXPRESSION; GLYCOPROTEINS; GROWTH DIFFERENTIATION FACTOR 9; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; MICRORNAS; MODELS, ANIMAL; OVARIAN FOLLICLE; OVARY; RECEPTORS, ANDROGEN; RECEPTORS, FSH; SIGNAL TRANSDUCTION; SOMATOMEDINS; STEM CELL FACTOR;

EID: 84907328414     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0296     Document Type: Review

References (100)

1. Abbott DH, Dumesic DA, Eisner JR, Colman RJ & Kemnitz JW 1998 Insights into the development of polycystic ovary syndrome (PCOS) from studies of prenatally androgenized female rhesus monkeys. Trends in Endocrinology and Metabolism 9 62-67.
2. Abbott DH, Barnett DK, Bruns CM & Dumesic DA 2005 Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome? Human Reproduction Update 11 357-374
3. Barad DH & Gleicher N 2005 Increased oocyte production after treatment with dehydroepiandrosterone. Fertility and Sterility 84 756.
4. Barad D & Gleicher N 2006 Effect of dehydroepiandrosterone on oocyte and embryo yields, embryo grade and cell number in IVF. Human Reproduction 21 2845-2849.
5. Carbajal L, Biswas A, Niswander LM, Prizant H & Hammeset SR 2011 GPCR/EGFR cross talk is conserved in gonadal and adrenal steroidogenesis but is uniquely regulated by matrix metalloproteinases 2 and 9 in the ovary. Molecular Endocrinology 25 1055-1065.
6. Cardenas H & Pope WF 1994 Administration of testosterone during the follicular phase increased the number of corpora lutea in gilts. Journal of Animal Science 72 2930-2935.
7. Cardenas H & Pope WF 2002 Androgen receptor and follicle-stimulating hormone receptor in the pig ovary during the follicular phase of the estrous cycle. Molecular Reproduction and Development 62 92-98.
8. Cardenas H, Herrick JR & Pope WF 2002 Increased ovulation rate in gilts treated with dihydrotestosterone. Reproduction 123 527-533.
9. Casson PR, Lindsay MS, Pisarska MD, Carson SA & Buster JE 2000 Dehydroepiandrosterone supplementation augments ovarian stimulation in poor responders: a case series. Human Reproduction 15 2129-2132.
10. Chadha S, Pache TD, Huikeshoven JM, Brinkmann AO & van der Kwast TH 1994 Androgen receptor expression in human ovarian and uterine tissue of long-term androgen-treated transsexual women. Human Pathology 25 1198-1204.
11. Dart DA, Waxman J, Aboagye EO & Bevan CL 2013 Visualising androgen receptor activity in male and female mice. PLoS ONE 8 e71694.
12. Dorrington JH, McKeracher HL, Chan AK & Gore-Langton RE 1983 Hormonal interactions in the control of granulosa cell differentiation. Journal of Steroid Biochemistry 19 17-32.
13. Duffy DM, Abdelgadir SE, Stott KR, Resko JA, Stouffer RL & Zelinski-Wooten MB 1999 Androgen receptor mRNA expression in the rhesus monkey ovary. Endocrine 11 23-30.
14. Evaul K & Hammes SR 2008 Cross-talk between G protein-coupled and epidermal growth factor receptors regulates gonadotropin-mediated steroidogenesis in Leydig cells. Journal of Biological Chemistry 283 27525-27533.
15. Falender AE, Lanz R, Malenfant D, Belanger L & Richards JS 2003 Differential expression of steroidogenic factor-1 and FTF/LRH-1 in the rodent ovary. Endocrinology 144 3598-3610.
16. Fitzpatrick SL & Richards JS 1991 Regulation of cytochrome P450 aromatase messenger ribonucleic acid and activity by steroids and gonadotropins in rat granulosa cells. Endocrinology 129 1452-1462.
17. Gill A, Jamnongjit M & Hammes SR 2004 Androgens promote maturation and signaling in mouse oocytes independent of transcription: a release of inhibition model for mammalian oocyte meiosis. Molecular Endocrinology 18 97-104.
18. Gleicher N & Barad DH 2006 Effects of transdermal testosterone application on the ovarian response to FSH in poor responders undergoing assisted reproduction technique - a prospective, randomized, double-blind study. Human Reproduction 21 3027; author reply 3027-3028.
19. Gleicher N & Barad DH 2011 Dehydroepiandrosterone (DHEA). supplementation in diminished ovarian reserve (DOR). Reproductive Biology and Endocrinology 9 67.
20. Gleicher N, Weghofer A & Barad DH 2011 The role of androgens in follicle maturation and ovulation induction: friend or foe of infertility treatment? Reproductive Biology and Endocrinology 9 116
21. Gleicher N, Kim A, Weghofer A, Kushnir VA, Shohat-Tal A, Lazzaroni E, Lee HJ & Barad DH 2013a Hypoandrogenism in association with diminished functional ovarian reserve. Human Reproduction 28 1084-1091.
22. Gleicher N, Kim A, Weghofer A, Shohat-Tal A, Lazzaroni E, Lee HJ & Barad DH 2013b Starting and resulting testosterone levels after androgen supplementation determine at all ages in vitro fertilization (IVF) pregnancy rates in women with diminished ovarian reserve (DOR). Journal of Assisted Reproduction and Genetics 30 49-62.
23. Gonzalez-Comadran M, Duran M, Sola I, Fabregues F, Carreras R & Checa MA 2012 Effects of transdermal testosterone in poor responders undergoing IVF: systematic review and meta-analysis. Reproductive Biomedicine Online 25 450-459.
24. Hampton JH, Manikkam M, Lubahn DB, Smith MF & Garverick HA 2004 Androgen receptor mRNA expression in the bovine ovary. Domestic Animal Endocrinology 27 81-88.
25. Harlow CR, Shaw HJ, Hillier SG & Hodges JK 1988 Factors influencing follicle-stimulating hormone-responsive steroidogenesis in marmoset granulosa cells: effects of androgens and the stage of follicular maturity. Endocrinology 122 2780-2787.
26. Hickey TE, Marrocco DL, Gilchrist RB, Norman RJ & Armstrong DT 2004 Interactions between androgen and growth factors in granulosa cell subtypes of porcine antral follicles. Biology of Reproduction 71 45-52.
27. Hickey TE, Marrocco DL, Amato F, Ritter LJ, Norman RJ, Gilchrist RB & Armstrong DT 2005 Androgens augment the mitogenic effects of oocyte-secreted factors and growth differentiation factor 9 on porcine granulosa cells. Biology of Reproduction 73 825-832.
28. Hillier SG 1987 Intrafollicular paracrine function of ovarian androgen. Journal of Steroid Biochemistry 27 351-357.
29. Hillier SG 1994 Current concepts of the roles of follicle stimulating hormone and luteinizing hormone in folliculogenesis. Human Reproduction 9 188-191.
30. Hillier SG & De Zwart FA 1981 Evidence that granulosa cell aromatase induction/activation by follicle-stimulating hormone is an androgen receptor-regulated process in-vitro. Endocrinology 109 1303-1305.
31. Hillier SG & de Zwart FA 1982 Androgen/antiandrogen modulation of cyclic AMP-induced steroidogenesis during granulosa cell differentiation in tissue culture. Molecular and Cellular Endocrinology 28 347-361.
32. Hillier SG, Harlow CR, Shaw HJ,Wickings EJ, Dixson AF & Hodges JK 1988 Cellular aspects of pre-ovulatory folliculogenesis in primate ovaries. Human Reproduction 3 507-511.
33. Hillier SG, Tetsuka M & Fraser HM 1997 Location and developmental regulation of androgen receptor in primate ovary. Human Reproduction 12 107-111.
34. Hirai M, Hirata S, Osada T, Hagihara K & Kato J 1994 Androgen receptor mRNA in the rat ovary and uterus. Journal of Steroid Biochemistry and Molecular Biology 49 1-7.
35. Horie K, Takakura K, Imai K, Liao S & Mori T 1992 Immunohistochemical localization of androgen receptor in the human endometrium, decidua, placenta and pathological conditions of the endometrium. Human Reproduction 7 1461-1466.
36. Hsueh AJ, Adashi EY, Jones PB & Welsh TH Jr 1984 Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocrine Reviews 5 76-127.
37. Hu YC, Wang PH, Yeh S,Wang RS, Xie C, Xu Q, Zhou X, Chao HT, Tsai MY & Chang C 2004 Subfertility and defective folliculogenesis in female mice lacking androgen receptor. PNAS 101 11209-11214.
38. Hyman JH, Margalioth EJ, Rabinowitz R, Tsafrir A, Gal M, Alerhand S, Algur N & Eldar-Geva T 2013 DHEA supplementation may improve IVF outcome in poor responders: a proposed mechanism. European Journal of Obstetrics, Gynecology, and Reproductive Biology 168 49-53.
39. Juengel JL, Heath DA, Quirke LD & McNatty KP 2006 Oestrogen receptor a and b, androgen receptor and progesterone receptor mRNA and protein localisation within the developing ovary and in small growing follicles of sheep. Reproduction 131 81-92.
40. Kimura S, Matsumoto T, Matsuyama R, Shiina H, Sato T, Takeyama K & Kato S 2007 Androgen receptor function in folliculogenesis and its clinical implication in premature ovarian failure. Trends in Endocrinology and Metabolism 18 183-189.
41. Knecht M, Ranta T & Catt KJ 1983 Hormonal regulation of a plasma membrane phosphodiesterase in differentiating granulosa cells. Reciprocal actions of follicle-stimulating hormone and a gonadotropinreleasing hormone agonist on cAMP degradation. Journal of Biological Chemistry 258 12420-12426.
42. Lebbe M & Woodruff TK 2013 Involvement of androgens in ovarian health and disease. Molecular Human Reproduction 19 828-837.
43. Luo W & Wiltbank MC 2006 Distinct regulation by steroids of messenger RNAs for FSHR and CYP19A1 in bovine granulosa cells. Biology of Reproduction 75 217-225.
44. Lyon MF & Glenister PH 1974 Evidence from Tfm-O that androgen is essential for reproduction in female mice. Nature 247 366-367.
45. Lyon MF & Glenister PH 1980 Reduced reproductive performance in androgen-resistant Tfm/Tfm female mice. PNAS 208 1-12.
46. Magamage M, Zengyo M, MoniruzzamanM&Miyano T 2011 Testosterone induces activation of porcine primordial follicles in vitro. Reproductive Medicine and Biology 10 21-30.
47. Mamas L & Mamas E 2009 Premature ovarian failure and dehydroepiandrosterone. Fertility and Sterility 91 644-646.
48. Mori T, Suzuki A, Nishimura T & Kambegawa A 1977 Evidence for androgen participation in induced ovulation in immature rats. Endocrinology 101 623-626.
49. Motro B & Bernstein A 1993 Dynamic changes in ovarian c-kit and Steel expression during the estrous reproductive cycle. Developmental Dynamics 197 69-79.
50. Murray AA, Gosden RG, Allison V & Spears N 1998 Effect of androgens on the development of mouse follicles growing in vitro. Journal of Reproduction and Fertility 113 27-33.
51. Nielsen ME, Rasmussen IA, Kristensen SG, Christensen ST, Mollgard K, Wreford Andersen E, Byskov AG & Yding Andersen C 2011 In human granulosa cells from small antral follicles, androgen receptor mRNA and androgen levels in follicular fluid correlate with FSH receptor mRNA. Molecular Human Reproduction 17 63-70.
52. Orisaka M, Jiang JY, Orisaka S, Kotsuji F & Tsang BK 2009 Growth differentiation factor 9 promotes rat preantral follicle growth by up-regulating follicular androgen biosynthesis. Endocrinology 150 2740-2748.
53. Peluso JJ, Charlesworth J & England-Charlesworth C 1981 Role of estrogen and androgen in maintaining the preovulatory follicle. Cell and Tissue Research 216 615-624.
54. Rasar M, DeFranco DB & Hammes SR 2006 Paxillin regulates steroidtriggered meiotic resumption in oocytes by enhancing an all-or-none positive feedback kinase loop. Journal of Biological Chemistry 281 39455-39464.
55. Rice S, Ojha K, Whitehead S & Mason H 2007 Stage-specific expression of androgen receptor, follicle-stimulating hormone receptor, and anti-Mullerian hormone type II receptor in single, isolated, human preantral follicles: relevance to polycystic ovaries. Journal of Clinical Endocrinology and Metabolism 92 1034-1040.
56. Richards JS, Sehgal N & Tash JS 1983 Changes in content and cAMPdependent phosphorylation of specific proteins in granulosa cells of preantral and preovulatory ovarian follicles and in corpora lutea. Journal of Biological Chemistry 258 5227-5232.
57. Robker RL & Richards JS 1998 Hormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Molecular Endocrinology 12 924-940.
58. Sen A & Hammes SR 2010 Granulosa cell-specific androgen receptors are critical regulators of ovarian development and function. Molecular Endocrinology 24 1393-1403.
59. Sen A & Hammes SR 2011 Androgens: they don't just make a man out of you. Expert Review of Obstetrics & Gynecology 6 19-22.
60. Sen A, O'Malley K, Wang Z, Raj GV, Defranco DB & Hammes SR 2010 Paxillin regulates androgen- and epidermal growth factor-induced MAPK signaling and cell proliferation in prostate cancer cells. Journal of Biological Chemistry 285 28787-28795.
61. Sen A, De Castro I, Defranco DB, Deng FM, Melamed J, Kapur P, Raj GV, Rossi R & Hammes SR 2012 Paxillin mediates extranuclear and intranuclear signaling in prostate cancer proliferation. Journal of Clinical Investigation 122 2469-2481.
62. Sen A, Prizant H, Light A, Biswas A, Hayes E, Lee HJ, Barad D, Gleicher N & Hammes SR 2014 Androgens regulate ovarian follicular development by increasing follicle stimulating hormone receptor and microRNA-125b expression. PNAS 111 3008-3013.
63. Shiina H, Matsumoto T, Sato T, Igarashi K, Miyamoto J, Takemasa S, Sakari M, Takada I, Nakamura T, Metzger D et al. 2006 Premature ovarian failure in androgen receptor-deficient mice. PNAS 103 224-229.
64. Sirianni R, Seely JB, Attia G, Stocco DM, Carr BR, Pezzi V & Rainey WE 2002 Liver receptor homologue-1 is expressed in human steroidogenic tissues and activates transcription of genes encoding steroidogenic enzymes. Journal of Endocrinology 174 R13-R17.
65. Slomczynska M & Tabarowski Z 2001 Localization of androgen receptor and cytochrome P450 aromatase in the follicle and corpus luteum of the porcine ovary. Animal Reproduction Science 65 127-134.
66. Slomczynska M, Duda M & Sl zak K 2001 The expression of androgen receptor, cytochrome P450 aromatase and FSH receptor mRNA in the porcine ovary. Folia Histochemica et Cytobiologica 39 9-13.
67. Slomczynska M, Szoltys M, Duda M, Sikora K & Tabarowski Z 2003 Androgens and FSH affect androgen receptor and aromatase distribution in the porcine ovary. Folia Biologica 51 63-68.
68. Smith P, Steckler TL, Veiga-Lopez A & Padmanabhan V 2009 Developmental programming: differential effects of prenatal testosterone and dihydrotestosterone on follicular recruitment, depletion of follicular reserve, and ovarian morphology in sheep. Biology of Reproduction 80 726-736.
69. Sonmezer M, Ozmen B,Cil AP, Ozkavukcu S, Tasci T, OlmusH&Atabekoglu CS 2009 Dehydroepiandrosterone supplementation improves ovarian response and cycle outcome in poor responders. Reproductive Biomedicine Online 19 508-513.
70. Sullivan SD & Moenter SM 2004 Prenatal androgens alter GABAergic drive to gonadotropin-releasing hormone neurons: implications for a common fertility disorder. PNAS 101 7129-7134.
71. Sunkara SK & Coomarasamy A 2011 Androgen pretreatment in poor responders undergoing controlled ovarian stimulation and in vitro fertilization treatment. Fertility and Sterility 95 e73-e74; author reply e75.
72. Sunkara SK, Coomarasamy A, Arlt W & Bhattacharya S 2012 Should androgen supplementation be used for poor ovarian response in IVF? Human Reproduction 27 637-640
73. Suzuki T, Sasano H, Kimura N, Tamura M, Fukaya T, Yajima A & Nagura H 1994 Immunohistochemical distribution of progesterone, androgen and oestrogen receptors in the human ovary during the menstrual cycle: relationship to expression of steroidogenic enzymes. Human Reproduction 9 1589-1595.
74. Szoltys M & Slomczynska M 2000 Changes in distribution of androgen receptor during maturation of rat ovarian follicles. Experimental and Clinical Endocrinology & Diabetes 108 228-234.
75. Tetsuka M & Hillier SG 1996 Androgen receptor gene expression in rat granulosa cells: the role of follicle-stimulating hormone and steroid hormones. Endocrinology 137 4392-4397.
76. Tetsuka M & Hillier SG 1997 Differential regulation of aromatase and androgen receptor in granulosa cells. Journal of Steroid Biochemistry and Molecular Biology 61 233-239.
77. Tetsuka M, Whitelaw PF, Bremner WJ, Millar MR, Smyth CD & Hillier SG 1995 Developmental regulation of androgen receptor in rat ovary. Journal of Endocrinology 145 535-543.
78. Thomas FH & Vanderhyden BC 2006 Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reproductive Biology and Endocrinology 4 19.
79. Vegetti W & Alagna F 2006 FSH, and folliculogenesis: from physiology to ovarian stimulation. Reproductive Biomedicine Online 12 684-694.
80. Vendola KA, Zhou J, Adesanya OO, Weil SJ & Bondy CA 1998 Androgens stimulate early stages of follicular growth in the primate ovary. Journal of Clinical Investigation 101 2622-2629.
81. Vendola K, Zhou J,Wang J & Bondy CA 1999a Androgens promote insulinlike growth factor-I and insulin-like growth factor-I receptor gene expression in the primate ovary. Human Reproduction 14 2328-2332.
82. Vendola K, Zhou J, Wang J, Famuyiwa OA, Bievre M & Bondy CA 1999b Androgens promote oocyte insulin-like growth factor I expression and initiation of follicle development in the primate ovary. Biology of Reproduction 61 353-357.
83. Vitt UA, McGee EA, Hayashi M & Hsueh AJ 2000 In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 141 3814-3820.
84. Walters KA, Allan CM, Jimenez M, Lim PR, Davey RA, Zajac JD, Illingworth P & Handelsman DJ 2007 Female mice haploinsufficient for an inactivated androgen receptor (AR) exhibit age-dependent defects that resemble the AR null phenotype of dysfunctional late follicle development, ovulation, and fertility. Endocrinology 148 3674-3684.
85. Walters KA, Allan CM & Handelsman DJ 2008 Androgen actions and the ovary. Biology of Reproduction 78 380-389.
86. Walters KA, Simanainen U & Handelsman DJ 2010 Molecular insights into androgen actions in male and female reproductive function from androgen receptor knockout models. Human Reproduction Update 16 543-558.
87. Walters KA, Middleton LJ, Joseph SR, Hazra R, Jimenez M, Simanainen U, Allan CM & Handelsman DJ 2012 Targeted loss of androgen receptor signaling in murine granulosa cells of preantral and antral follicles causes female subfertility. Biology of Reproduction 87 151.
88. Wang H, Andoh K, Hagiwara H, Xiaowei L, Kikuchi N, Abe Y, Yamada K, Fatima R & Mizunuma H 2001 Effect of adrenal and ovarian androgens on type 4 follicles unresponsive to FSH in immature mice. Endocrinology 142 4930-4936.
89. Ware VC 1982 The role of androgens in follicular development in the ovary. I. A quantitative analysis of oocyte ovulation. Journal of Experimental Zoology 222 155-167.
90. Weil SJ, Vendola K, Zhou J, Adesanya OO, Wang J, Okafor J & Bondy CA 1998 Androgen receptor gene expression in the primate ovary: cellular localization, regulation, and functional correlations. Journal of Clinical Endocrinology and Metabolism 83 2479-2485.
91. Weil S, Vendola K, Zhou J & Bondy CA 1999 Androgen and folliclestimulating hormone interactions in primate ovarian follicle development. Journal of Clinical Endocrinology and Metabolism 84 2951-2956.
92. Wiser A, Gonen O, Ghetler Y, Shavit T, Berkovitz A & Shulman A 2010 Addition of dehydroepiandrosterone (DHEA) for poor-responder patients before and during IVF treatment improves the pregnancy rate: a randomized prospective study. Human Reproduction 25 2496-2500.
93. Wu YG, Bennett J, Talla D & Stocco C 2011 Testosterone, not 5a-dihydrotestosterone, stimulates LRH-1 leading to FSH-independent expression of Cyp19 and P450scc in granulosa cells. Molecular Endocrinology 25 656-668.
94. Wu Y, Baumgarten SC, Zhou P & Stocco C 2013 Testosterone-dependent interaction between androgen receptor and aryl hydrocarbon receptor induces liver receptor homolog 1 expression in rat granulosa cells. Molecular and Cellular Biology 33 2817-2828.
95. Xue K, Kim JY, Liu JY & Tsang BK 2014 Insulin-like 3-induced rat preantral follicular growth is mediated by growth differentiation factor 9. Endocrinology 155 156-167.
96. Yang MY & Fortune JE 2006 Testosterone stimulates the primary to secondary follicle transition in bovine follicles in vitro. Biology of Reproduction 75 924-932.
97. Yang JL, Zhang CP, Li L, Huang L, Ji SY, Lu CL, Fan CH, Cai H, Ren Y, Hu ZY et al. 2010 Testosterone induces redistribution of forkhead box-3a and down-regulation of growth and differentiation factor 9 messenger ribonucleic acid expression at early stage of mouse folliculogenesis. Endocrinology 151 774-782.
98. Yazawa T, Kawabe S, Kanno M, Mizutani T, Imamichi Y, Ju Y, Matsumura T, Yamazaki Y, Usami Y, Kuribayashi M et al. 2013 Androgen/androgen receptor pathway regulates expression of the genes for cyclooxygenase-2 and amphiregulin in periovulatory granulosa cells. Molecular and Cellular Endocrinology 369 42-51.
99. Yeung TW, Chai J, Li RH, Lee VC, Ho PC & Ng EH 2014 A randomized, controlled, pilot trial on the effect of dehydroepiandrosterone on ovarian response markers, ovarian response, and in vitro fertilization outcomes in poor responders. Fertility and Sterility 102 108-115.
100. Yilmaz N, Uygur D, Inal H, Gorkem U, Cicek N & Mollamahmutoglu L 2013 Dehydroepiandrosterone supplementation improves predictive markers for diminished ovarian reserve: serum AMH, inhibin B and antral follicle count. European Journal of Obstetrics, Gynecology, and Reproductive Biology 169 257-260.