Androgen stimulates growth of mouse preantral follicles in vitro: Interaction with follicle-stimulating hormone and with growth factors of the TGFβ super family

Endocrinology

Volumn 158, Issue 4, 2017, Pages 920-935

  Laird, Mhairi ^a   Thomson, Kacie ^a   Fenwick, Mark ^a   Mora, Jocelyn ^a   Franks, Stephen ^a   Hardy, Kate ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXY 1 METHYLTETRALIN; ANDROGEN RECEPTOR; ANDROSTANOLONE; ANTI MULLERIAN HORMONE RECEPTOR TYPE 2; BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; CASPASE 3; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYTOCHROME P450 FAMILY 17; CYTOCHROME P450 FAMILY 19; FLUTAMIDE; FOLLITROPIN; FOLLITROPIN RECEPTOR; GROWTH DIFFERENTIATION FACTOR 9; GROWTH FACTOR; HORMONE RECEPTOR; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TESTOSTERONE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG; ANDROGEN; ANDROGEN RECEPTOR ANTAGONIST;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; HORMONE ACTION; IMMUNOFLUORESCENCE; IN VITRO STUDY; MOUSE; NONHUMAN; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; STEROIDOGENESIS; TUNEL ASSAY; UPREGULATION; ANIMAL; CELL CULTURE; DRUG EFFECT; GENETICS; GRANULOSA CELL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OVARY FOLLICLE; SIGNAL TRANSDUCTION;

ANDROGEN RECEPTOR ANTAGONISTS; ANDROGENS; ANIMALS; CELLS, CULTURED; DIHYDROTESTOSTERONE; DOWN-REGULATION; FEMALE; FLUTAMIDE; FOLLICLE STIMULATING HORMONE; GRANULOSA CELLS; MICE; OVARIAN FOLLICLE; RECEPTORS, FSH; SIGNAL TRANSDUCTION; TESTOSTERONE; TRANSFORMING GROWTH FACTOR BETA;

EID: 85016765036     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2016-1538     Document Type: Article

References (44)

1. Murray AA, Gosden RG, Allison V, Spears N. Effect of androgens on the development of mouse follicles growing in vitro. J Reprod Fertil. 1998;113(1):27-33.
2. Nimrod A, Lindner HR. A synergistic effect of androgen on the stimulation of progesterone secretion by FSH in cultured rat granulosa cells. Mol Cell Endocrinol. 1976;5(3-4):315-320.
3. Hillier SG, Knazek RA, Ross GT. Androgenic stimulation of progesterone production by granulosa cells from preantral ovarian follicles: Further in vitro studies using replicate cell cultures. Endocrinology. 1977;100(6):1539-1549.
4. Wang XN, Greenwald GS. Synergistic effects of steroids with FSH on folliculogenesis, steroidogenesis and FSH- and hCG-receptors in hypophysectomized mice. J Reprod Fertil. 1993;99(2):403-413.
5. Shiina H, Matsumoto T, Sato T, Igarashi K, Miyamoto J, Takemasa S, Sakari M, Takada I, Nakamura T, Metzger D, Chambon P, Kanno J, Yoshikawa H, Kato S. Premature ovarian failure in androgen receptor-deficient mice. Proc Natl Acad Sci USA. 2005; 103(1):224-229.
6. Sen A, Hammes S.R. Granulosa cell-specific androgen receptors are critical regulators of ovarian development and function. Mol Endocrinol. 2010;24(7):1393-1403.
7. Walters KA, Middleton LJ, Joseph SR, Hazra R, Jimenez M, Simanainen U, Allan CM, Handelsman DJ. Targeted loss of androgen receptor signaling in murine granulosa cells of preantral and antral follicles causes female subfertility. Biol Reprod. 2012; 87(6):151.
8. Yang MY, Fortune JE. Testosterone stimulates the primary to secondary follicle transition in bovine follicles in vitro. Biol Reprod. 2006;75(6):924-932.
9. Qureshi AI, Nussey SS, Bano G, Musonda P, Whitehead SA, Mason HD. Testosterone selectively increases primary follicles in ovarian cortex grafted onto embryonic chick membranes: Relevance to polycystic ovaries. Reproduction. 2008;136(2):187-194.
10. Pradeep PK, Li X, Peegel H, Menon KM. Dihydrotestosterone inhibits granulosa cell proliferation by decreasing the cyclin D2 mRNAexpression and cell cycle arrest at G1 phase. Endocrinology. 2002;143(8):2930-2935.
11. Billig H, Furuta I, Hsueh AJ. Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology. 1993; 133(5):2204-2212.
12. Franks S. Polycystic ovary syndrome. NEngl J Med. 1995;333(13): 853-861.
13. Ehrmann DA. Polycystic ovary syndrome. N Engl J Med. 2005; 352(12):1223-1236.
14. Da Silva-Buttkus P, Jayasooriya GS, Mora JM, Mobberley M, Ryder TA, Baithun M, Stark J, Franks S, Hardy K. Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. J Cell Sci. 2008;121(23):3890-3900.
15. Webber LJ, Stubbs S, Stark J, Trew GH, Margara R, Hardy K, Franks S. Formation and early development of follicles in the polycystic ovary. Lancet. 2003;362(9389):1017-1021.
16. Stubbs SA, Stark J, Dilworth SM, Franks S, Hardy K. Abnormal preantral folliculogenesis in polycystic ovaries is associated with increased granulosa cell division. J Clin Endocrinol Metab. 2007; 92(11):4418-4426.
17. Maciel GA, Baracat EC, Benda JA, Markham SM, Hensinger K, Chang RJ, Erickson GF. Stockpiling of transitional and classic primary follicles in ovaries of women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2004;89(11):5321-5327.
18. Hogg K, Wood C, McNeilly AS, Duncan WC. The in utero programming effect of increased maternal androgens and a direct fetal intervention on liver and metabolic function in adult sheep. PLoS One. 2011;6(9):e24877.
19. Padmanabhan V, Veiga-Lopez A. Sheep models of polycystic ovary syndrome phenotype. Mol Cell Endocrinol. 2013;373(1-2):8-20.
20. Crespi EJ, Steckler TL, Mohankumar PS, Padmanabhan V. Prenatal exposure to excess testosterone modifies the developmental trajectory of the insulin-like growth factor system in female sheep. J Physiol. 2006;572(1):119-130.
21. Forsdike RA, Hardy K, Bull L, Stark J, Webber LJ, Stubbs S, Robinson JE, Franks S. Disordered follicle development in ovaries of prenatally androgenized ewes. J Endocrinol. 2007; 192(2):421-428.
22. Fenwick MA, Mansour YT, Franks S, Hardy K. Identification and regulation of bone morphogenetic protein antagonists associated with preantral follicle development in the ovary. Endocrinology. 2011;152(9):3515-3526.
23. Fenwick MA, Mora JM, Mansour YT, Baithun C, Franks S, Hardy K. Investigations of TGF-b signaling in preantral follicles of female mice reveal differential roles for bone morphogenetic protein 15. Endocrinology. 2013;154(9):3423-3436.
24. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, Hoyng SA, Lin HY, Bloch KD, Peterson RT. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol. 2007;4(1):33-41.
25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 22DDC T method. Methods. 2001;25(4):402-408.
26. Hardy K, Fenwick M, Mora J, Laird M, Thomson K, Franks S. Onset and heterogeneity of responsiveness to fsh in mouse preantral follicles in culture [published online ahead of print November 7, 2016]. Endocrinology. doi: 10. 1210/en. 2016-1435.
27. Abbott DH, Dumesic DA, Franks S. Developmental origin of polycystic ovary syndrome-a hypothesis. J Endocrinol. 2002;174(1):1-5.
28. Abbott DH, Nicol LE, Levine JE, Xu N, Goodarzi MO, Dumesic DA. Nonhuman primate models of polycystic ovary syndrome. Mol Cell Endocrinol. 2013;373(1-2):21-28.
29. Vendola KA, Zhou J, Adesanya OO, Weil SJ, Bondy CA. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest. 1998;101(12):2622-2629.
30. Vendola K, Zhou J, Wang J, Bondy CA. Androgens promote insulin-like growth factor-I and insulin-like growth factor-I receptor gene expression in the primate ovary. Hum Reprod. 1999; 14(9):2328-2332.
31. Sen A, Prizant H, Light A, Biswas A, Hayes E, Lee HJ, Barad D, Gleicher N, Hammes S.R. Androgens regulate ovarian follicular development by increasing follicle stimulating hormone receptor and microRNA-125b expression. Proc Natl Acad Sci USA. 2014; 111(8):3008-3013.
32. Erickson GF, Garzo VG, Magoffin DA. Insulin-like growth factor-I regulates aromatase activity in human granulosa and granulosa luteal cells. J Clin Endocrinol Metab. 1989;69(4):716-724.
33. Hernandez ER, HurwitzA, PayneDW, DharmarajanAM, Purchio AF, Adashi EY. Transforming growth factor-beta 1 inhibits ovarian androgen production: Gene expression, cellular localization, mechanisms (s), and site(s) of action. Endocrinology. 1990;127(6):2804-2811.
34. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Ingraham HA, NachtigalMW, Uilenbroek JT, Grootegoed JA, Themmen AP. Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology. 2002;143(3):1076-1084.
35. Veiga-Lopez A, Ye W, Padmanabhan V. Developmental programming: Prenatal testosterone excess disrupts anti-Müllerian hormone expression in preantral and antral follicles. Fertil Steril. 2012;97(3):748-756.
36. Pierre A, Estienne A, Racine C, Picard JY, Fanchin R, Lahoz B, Alabart JL, Folch J, Jarrier P, Fabre S, Monniaux D, di Clemente N. The bone morphogenetic protein 15 up-regulates the anti-Müllerian hormone receptor expression in granulosa cells. J Clin Endocrinol Metab. 2016;101(6):2602-2611.
37. Ogura-Nose S, Yoshino O, Osuga Y, Shi J, Hiroi H, Yano T, Taketani Y. Anti-Mullerian hormone (AMH) is induced by bone morphogenetic protein (BMP) cytokines in human granulosa cells. Eur J Obstet Gynecol Reprod Biol. 2012;164(1):44-47.
38. Salmon NA, Handyside AH, Joyce IM. Oocyte regulation of anti-Müllerian hormone expression in granulosa cells during ovarian follicle development in mice. Dev Biol. 2004;266(1):201-208.
39. Smith P, Steckler TL, Veiga-Lopez A, Padmanabhan V. Developmental programming: Differential effects of prenatal testosterone and dihydrotestosterone on follicular recruitment, depletion of follicular reserve, and ovarian morphology in sheep. Biol Reprod. 2008;80(4):726-736.
40. Rodgers RJ, Irving-Rodgers HF. Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod. 2010;82(6):1021-1029.
41. Grzesiak M, Williams L, Luck MR. Testosterone influences water transport in porcine granulosa cells. Reprod Domest Anim. 2013; 48(4):e52-e54.
42. Grzesiak M, Knapczyk-Stwora K, Luck MR, Mobasheri A, Slomczynska M. Effect of prenatal and neonatal anti-androgen flutamide treatment on aquaporin 5 expression in the adult porcine ovary. Reprod Domest Anim. 2015;51(1):105-113.
43. Franks S. Animal models and the developmental origins of polycystic ovary syndrome: Increasing evidence for the role of androgens in programming reproductive and metabolic dysfunction. Endocrinology. 2012;153(6):2536-2538.
44. Willis DS, Watson H, Mason HD, Galea R, Brincat M, Franks S. Premature response to luteinizing hormone of granulosa cells from anovulatory women with polycystic ovary syndrome: Relevance to mechanism of anovulation. J Clin Endocrinol Metab. 1998;83(11):3984-3991.