Intraovarian control of early folliculogenesis

Endocrine Reviews

Volumn 36, Issue 1, 2015, Pages 1-24

  Hsueh, Aaron J W ^a   Kawamura, Kazuhiro ^b   Cheng, Yuan ^a   Fauser, Bart C J M ^c  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLITROPIN; GROWTH FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; NATRIURETIC PEPTIDE TYPE C; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN SERINE KINASE; PROTEIN TYROSINE KINASE; WNT1 PROTEIN; TARGET OF RAPAMYCIN KINASE;

DEVELOPMENTAL STAGE; FEMALE INFERTILITY; GERMINAL VESICLE; GRANULOSA CELL; HORMONAL REGULATION; HUMAN; NONHUMAN; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; OVARY INSUFFICIENCY; OVARY POLYCYSTIC DISEASE; OVULATION; PREMATURE OVARIAN FAILURE; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECTS; FEMALE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OOCYTE; OVARIAN DISEASES; OVARY; OVARY FOLLICLE; PATHOLOGY; PHYSIOLOGY; PRIMARY OVARIAN INSUFFICIENCY;

ANIMALS; FEMALE; FOLLICLE STIMULATING HORMONE; GRANULOSA CELLS; HUMANS; NATRIURETIC PEPTIDE, C-TYPE; OOCYTES; OVARIAN DISEASES; OVARIAN FOLLICLE; OVARY; POLYCYSTIC OVARY SYNDROME; PRIMARY OVARIAN INSUFFICIENCY; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84922139179     PISSN: None     EISSN: 0163769X     Source Type: Journal    
DOI: 10.1210/er.2014-1020     Document Type: Review

References (230)

1. McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev. 2000;21:200-214.
2. Hsueh AJ, Billig H, Tsafriri A. Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr Rev. 1994;15:707-724.
3. Zeleznik AJ. Follicle selection in primates:"manyare called but few are chosen". Biol Reprod. 2001;65:655-659.
4. Richards JS. Maturation of ovarian follicles: actions and interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiol Rev. 1980;60:51-89.
5. Goodman A, Hodgen G. The ovarian triad of the primate menstrual cycle. Recent Prog Horm Res. 1983;39:1.
6. Hsueh AJ, Adashi EY, Jones PB, Welsh TH Jr. Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocr Rev. 1984;5:76-127.
7. Fauser BC, Van Heusden AM. Manipulation of human ovarian function: physiological concepts and clinical consequences. Endocr Rev. 1997;18:71-106.
8. Macklon NS, Stouffer RL, Giudice LC, Fauser BC. The science behind 25 years of ovarian stimulation for in vitro fertilization. Endocr Rev. 2006;27:170-207.
9. Reddy P, Zheng W, Liu K. Mechanisms maintaining the dormancy and survival of mammalian primordial follicles. Trends Endocrinol Metab. 2010;21:96-103.
10. Broekmans FJ, Soules MR, Fauser BC. Ovarian aging: mechanisms and clinical consequences. Endocr Rev. 2009; 30:465-493.
11. Richards JS. Hormonal control of gene expression in the ovary. Endocr Rev. 1994;15:725-751.
12. Oktay K, Briggs D, Gosden RG. Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J Clin Endocrinol Metab. 1997;82: 3748-3751.
13. McGee EA, Perlas E, LaPolt PS, Tsafriri A, Hsueh AJ. Follicle- stimulating hormone enhances the development of preantral follicles in juvenile rats. Biol Reprod. 1997;57: 990-998.
14. Abel MH, Wootton AN, Wilkins V, Huhtaniemi I, Knight PG, Charlton HM. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology. 2000;141:1795-1803.
15. SchootDC,Harlin J,ShohamZ, et al. Recombinanthuman follicle-stimulating hormone and ovarian response in gonadotrophin- deficient women. Hum Reprod. 1994;9: 1237-1242.
16. Kreeger PK, Fernandes NN, Woodruff TK, Shea LD. Regulation of mouse follicle development by follicle-stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose. Biol Reprod. 2005; 73:942-950.
17. Xu M, West-Farrell ER, Stouffer RL, Shea LD, Woodruff TK, Zelinski MB. Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol Reprod. 2009;81:587-594.
18. Cortvrindt R, Smitz J, Van Steirteghem A. Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Hum Reprod. 1997;12: 759-768.
19. Wright CS, Hovatta O, Margara R, et al. Effects of folliclestimulating hormone and serum substitution on the invitro growth of human ovarian follicles. Hum Reprod. 1999;14:1555-1562.
20. Brenner BM, Ballermann BJ, Gunning ME, Zeidel ML. Diverse biological actions of atrial natriuretic peptide. Physiol Rev. 1990;70:665-699.
21. Sudoh T, Minamino N, Kangawa K, Matsuo H. C-type natriuretic peptide (CNP): a new member of natriuretic peptide family identified in porcine brain. Biochem Biophys Res Commun. 1990;168:863-870.
22. Koller KJ, Lowe DG, Bennett GL, et al. Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science. 1991;252:120-123.
23. Tremblay J, Desjardins R,HumD, Gutkowska J, Hamet P. Biochemistry and physiology of the natriuretic peptide receptor guanylyl cyclases. Mol Cell Biochem. 2002;230:31-47.
24. Schulz S. C-type natriuretic peptide and guanylyl cyclase B receptor. Peptides. 2005;26:1024-1034.
25. Troughton RW, Frampton CM, Yandle TG, Espiner EA, Nicholls MG, Richards AM. Treatment of heart failure guided by plasma aminoterminal brain natriuretic peptide (N-BNP) concentrations. Lancet. 2000;355:1126-1130.
26. Suga S, Nakao K, Itoh H, et al. Endothelial production of C-type natriuretic peptide and its marked augmentation by transforming growth factor-beta. Possible existence of "vascular natriuretic peptide system". J Clin Invest. 1992; 90:1145-1149.
27. Hobbs A, Foster P, Prescott C, Scotland R, Ahluwalia A. Natriuretic peptide receptor-C regulates coronary blood flow and prevents myocardial ischemia/reperfusion injury: novel cardioprotective role for endothelium-derived C-type natriuretic peptide. Circulation. 2004;110:1231- 1235.
28. Jankowski M, Reis AM, Mukaddam-Daher S, Dam TV, Farookhi R, Gutkowska J. C-type natriuretic peptide and the guanylyl cyclase receptors in the rat ovary are modulated by the estrous cycle. Biol Reprod. 1997;56:59-66.
29. Gutkowska J, Jankowski M, Sairam MR, et al. Hormonal regulation of natriuretic peptide system during induced ovarian follicular development in the rat. Biol Reprod. 1999;61:162-170.
30. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science. 2010;330:366-369.
31. Norris RP, Ratzan WJ, Freudzon M, et al. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development. 2009;136: 1869-1878.
32. Kawamura K, Cheng Y, Kawamura N, et al. Pre-ovulatory LH/hCG surge decreases C-type natriuretic peptide secretion by ovarian granulosa cells to promote meiotic resumption of pre-ovulatory oocytes. Hum Reprod. 2011;26: 3094-3101.
33. Tsafriri A, Pomerantz SH. Oocyte maturation inhibitor. Clin Endocrinol Metab. 1986;15:157-170.
34. Chusho H, Tamura N, Ogawa Y, et al. Dwarfism and early death in mice lacking C-type natriuretic peptide. Proc Natl Acad Sci U S A. 2001;98:4016-4021.
35. Tamura N, Doolittle LK, Hammer RE, Shelton JM, Richardson JA, Garbers DL. Critical roles of the guanylyl cyclase B receptor in endochondral ossification and development of female reproductive organs. Proc Natl Acad Sci U S A. 2004;101:17300-17305.
36. Kiyosu C, Tsuji T, Yamada K, Kajita S, Kunieda T. NPPC/ NPR2 signaling is essential for oocyte meiotic arrest and cumulus oophorus formation during follicular development in the mouse ovary. Reproduction. 2012;144:187- 193.
37. McGee E, Spears N, Minami S, et al. Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3',5'-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone. Endocrinology. 1997;138: 2417-2424.
38. Sato Y, Cheng Y, Kawamura K, Takae S, Hsueh AJ. C-type natriuretic peptide stimulates ovarian follicle development. Mol Endocrinol. 2012;26:1158-1166.
39. Hannema SE, van Duyvenvoorde HA, Premsler T, et al. An activating mutation in the kinase homology domain of the natriuretic peptide receptor-2 causes extremely tall stature without skeletal deformities. J Clin Endocrinol Metab. 2013;98:E1988-E1998.
40. Barletta G, Lazzeri C, Vecchiarino S, et al. Low-dose Ctype natriuretic peptide does not affect cardiac and renal function in humans. Hypertension. 1998;31:802-808.
41. Cheng Y, Kawamura K, Takae S, et al. Oocyte-derived R-spondin2 promotes ovarian follicle development. FASEB J. 2013;27:2175-2184.
42. Juengel JL, Bodensteiner KJ, Heath DA, et al. Physiology of GDF9 and BMP15 signalling molecules. Anim Reprod Sci. 2004;82:447-460.
43. Wodarz A, Nusse R. Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol. 1998;14:59-88.
44. Mao J, Wang J, Liu B, et al. Low-density lipoprotein receptor- related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol Cell. 2001;7:801- 809.
45. de Lau W, Barker N, Low TY, et al. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature. 2011;476:293-297.
46. Carmon KS, Gong X, Lin Q, Thomas A, Liu Q. 2011 Rspondins function as ligands of the orphan receptorsLGR4 and LGR5 to regulate Wnt/β-catenin signaling. Proc Natl Acad Sci U S A. 2011;108:11452-11457.
47. Kim KA, Wagle M, Tran K, et al. R-Spondin family members regulate the Wnt pathway by a common mechanism. Mol Biol Cell. 2008;19:2588-2596.
48. Kim KA, Kakitani M, Zhao J, et al. Mitogenic influence of human R-spondin1 on the intestinal epithelium. Science. 2005;309:1256-1259.
49. Bell SM, Schreiner CM, Hess KA, Anderson KP, Scott WJ. Asymmetric limb malformations in a new transgene insertional mutant, footless. Mech Dev. 2003;120:597-605.
50. Nam JS, Park E, Turcotte TJ, et al. Mouse R-spondin2 is required for apical ectodermal ridge maintenance in the hindlimb. Dev Biol. 2007;311:124-135.
51. Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science. 2004;305: 1157-1159.
52. Qin Y, Choi Y, Zhao H, Simpson JL, Chen ZJ, Rajkovic A. NOBOX homeobox mutation causes premature ovarian failure. Am J Hum Genet. 2007;81:576-581.
53. Choi Y, Qin Y, Berger MF, Ballow DJ, Bulyk ML, Rajkovic A. Microarray analyses of newborn mouse ovaries lacking Nobox. Biol Reprod. 2007;77:312-319.
54. Vitt UA, Hsu SY, Hsueh AJ. Evolution and classification of cystine knot-containing hormones and related extracellular signaling molecules. Mol Endocrinol. 2001;15:681- 694.
55. Shi Y, Massagué J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell. 2003;113:685-700.
56. Vitt UA, Mazerbourg S, Klein C, Hsueh AJ. Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol Reprod. 2002;67:473-480.
57. Mazerbourg S, Klein C,RohJ, et al. Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. Mol Endocrinol. 2004;18:653- 665.
58. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996;383: 531-535.
59. Vitt UA, Hayashi M, Klein C, Hsueh AJ. Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol Reprod. 2000;62:370-377.
60. Solovyeva EV, Hayashi M, Margi K, et al. Growth differentiation factor-9 stimulates rat theca-interstitial cell androgen biosynthesis. Biol Reprod. 2000;63:1214-1218.
61. Spicer LJ, Aad PY, Allen DT, Mazerbourg S, Payne AH, Hsueh AJ. Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: influence of follicle size on responses to GDF9. Biol Reprod. 2008;78:243-253.
62. Vitt UA, McGee EA, Hayashi M, Hsueh AJ. In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology. 2000;141:3814-3820.
63. Orisaka M, Orisaka S, Jiang JY, et al. Growth differentiation factor 9 is antiapoptotic during follicular development from preantral to early antral stage. Mol Endocrinol. 2006;20:2456-2468.
64. Otsuka F, Yao Z, Lee T, Yamamoto S, Erickson GF, Shimasaki S. Bone morphogenetic protein-15. Identification of target cells and biological functions. J Biol Chem. 2000; 275:39523-39528.
65. Galloway SM, McNatty KP, Cambridge LM, et al. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosagesensitive manner. Nat Genet. 2000;25:279-283.
66. Persani L, Rossetti R, Di Pasquale E, Cacciatore C, Fabre S. The fundamental role of bone morphogenetic protein 15 in ovarian function and its involvement in female fertility disorders. Hum Reprod Update. 2014;pii:dmu036.
67. Yan C, Wang P, DeMayo J, et al. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol. 2001;15:854- 866.
68. Davis GH, McEwan JC, Fennessy PF, et al. Infertility due to bilateral ovarian hypoplasia in sheep homozygous (FecXI FecXI) for the Inverdale prolificacy gene located on the X chromosome. Biol Reprod. 1992;46:636-640.
69. Hanrahan JP, Gregan SM, Mulsant P, et al. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol Reprod. 2004;70:900-909.
70. Di Pasquale E, Beck-Peccoz P, Persani L. Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am J Hum Genet. 2004;75:106-111.
71. Dixit H, Rao LK, Padmalatha VV, et al. Missense mutations in the BMP15 gene are associated with ovarian failure. Hum Genet. 2006;119:408-415.
72. Tiotiu D, Alvaro Mercadal B, Imbert R, et al. Variants of the BMP15 gene in a cohort of patients with premature ovarian failure. Hum Reprod. 2010;25:1581-1587.
73. Laissue P, Christin-Maitre S, Touraine P, et al. Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur J Endocrinol. 2006; 154:739-744.
74. Simpson CM, Robertson DM, Al-Musawi SL, et al. Aberrant GDF9 expression and activation are associated with common human ovarian disorders. J Clin Endocrinol Metab. 2014;99:E615-E624.
75. Peng J, Li Q, Wigglesworth K, et al. Growth differentiation factor 9:bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc Natl Acad Sci U S A. 2013;110:E776-E785.
76. Durlinger AL, Gruijters MJ, Kramer P, et al. Anti-Müllerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology. 2001;142: 4891-4899.
77. Durlinger AL, Kramer P, Karels B, et al. Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary. Endocrinology. 1999;140:5789-5796.
78. Campbell BK, Clinton M, Webb R. The role of anti-Müllerian hormone (AMH) during follicle development in a monovulatory species (sheep). Endocrinology. 2012;153: 4533-4543.
79. Richards JS, Russell DL, Ochsner S, et al. Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent ProgHormRes. 2002; 57:195-220.
80. Lee J, Park HJ, Choi HS, et al. Gonadotropin stimulation of pituitary adenylate cyclase-activating polypeptide (PACAP) messenger ribonucleic acid in the rat ovary and the role of PACAP as a follicle survival factor. Endocrinology. 1999;140:818-826.
81. Qin Y, Sun M, You L, et al. ESR1, HK3 and BRSK1 gene variants are associated with both age at natural menopause and premature ovarian failure. Orphanet J Rare Dis. 2012; 7:1- 6.
82. Xia Y, Che Y, Zhang X, et al. Polymorphic CAG repeat in the androgen receptor gene in polycystic ovary syndrome patients. Mol Med Report. 2012;5:1330-1334.
83. Zhang T, Liang W, Fang M, Yu J, Ni Y, Li Z. Association of the CAG repeat polymorphisms in androgen receptor gene with polycystic ovary syndrome: a systemic review and meta-analysis. Gene. 2013;524:161-167.
84. Lee S, Kang DW, Hudgins-Spivey S, et al. Theca-specific estrogen receptor-α knockout mice lose fertility prematurely. Endocrinology. 2009;150:3855-3862.
85. Sen A, Hammes SR. Granulosa cell-specific androgen receptors are critical regulators of ovarian development and function. Mol Endocrinol. 2010;24:1393-1403.
86. Walters KA, Middleton LJ, Joseph SR, et al. Targeted loss of androgen receptor signaling in murine granulosa cells of preantral and antral follicles causes female subfertility. Biol Reprod. 2012;87:151.
87. Lydon JP, DeMayo FJ, Funk CR, et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 1995;9:2266-2278.
88. Natraj U, Richards JS. Hormonal regulation, localization, and functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinology. 1993;133:761-769.
89. Zeleznik AJ. The physiology of follicle selection. Reprod Biol Endocrinol. 2004;2:31.
90. Sen A, Prizant H, Light A, et al. Androgens regulate ovarian follicular development by increasing follicle stimulating hormone receptor and microRNA-125b expression. Proc Natl Acad Sci U S A. 2014;111:3008-3013.
91. Hillier SG, De Zwart FA. Evidence that granulosa cell aromatase induction/activation by follicle-stimulating hormone is an androgen receptor-regulated process in-vitro. Endocrinology. 1981;109:1303-1305.
92. Armstrong DT, Dorrington JH. Androgens augment FSHinduced progesterone secretion by cultured rat granulosa cells. Endocrinology. 1976;99:1411-1414.
93. McNatty KP, Baird DT, Bolton A, Chambers P, Corker C, McLean H. Concentration of oestrogens and androgens in humanovarian venous plasma and follicular fluid throughout the menstrual cycle. J Endocrinol. 1976;71:77-85.
94. Murray AA, Gosden RG, Allison V, Spears N. Effect of androgens on the development of mouse follicles growing in vitro. J Reprod Fertil. 1998;113:27-33.
95. Weil S, Vendola K, Zhou J, Bondy CA. Androgen and follicle-stimulating hormone interactions in primate ovarian follicle development. J Clin Endocrinol Metab. 1999; 84:2951-2956.
96. Casson PR, Lindsay MS, Pisarska MD, Carson SA, Buster JE. Dehydroepiandrosterone supplementation augments ovarian stimulation in poor responders: a case series. Hum Reprod. 2000;15:2129-2132.
97. Gleicher N, Barad DH. Dehydroepiandrosterone (DHEA) supplementation in diminished ovarian reserve (DOR). Reprod Biol Endocrinol. 2011;9:67.
98. Sunkara SK, Coomarasamy A, Arlt W, Bhattacharya S. Should androgen supplementation be used for poor ovarian response in IVF? Hum Reprod. 2012;27:637-640.
99. Zangmo R, Singh N, Kumar S, Vanamail P, Tiwari A. Role of dehydroepiandrosterone in improving oocyte and embryo quality in IVF cycles. Reprod Biomed Online. 2014; 28:743-747.
100. Stein IF, Leventhal ML Amenorrhea associated with bilateral polycystic ovaries. Am J Obstet Gynecol. 1935;29: 181.
101. Farquhar C, Brown J, Marjoribanks J. Laparoscopic drilling by diathermy or laser for ovulation induction in anovulatory polycystic ovary syndrome. Cochrane Database Syst Rev. 2012;6:CD001122.
102. Donnez J, Silber S, Andersen CY, et al. Children born after autotransplantation of cryopreserved ovarian tissue. a review of 13 live births. Ann Med. 2011;43:437-450.
103. Kawamura K, Cheng Y, Suzuki N, et al. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci U S A. 2013;110: 17474-17479.
104. Pan D. Hippo signaling in organ size control. Genes Dev. 2007;21:886-897.
105. Halder G, Johnson RL. Hippo signaling: growth control and beyond. Development. 2011;138:9-22.
106. Hergovich A. Mammalian Hippo signalling: a kinase network regulated by protein-protein interactions. Biochem Soc Trans. 2012;40:124-128.
107. Holbourn KP, Acharya KR, Perbal B. The CCN family of proteins: structure-function relationships. Trends Biochem Sci. 2008;33:461-473.
108. LuL, Li Y,KimSM,et al.Hipposignaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc Natl Acad Sci U S A. 2010;107:1437-1442.
109. Lee KP, Lee JH, Kim TS, et al. The Hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis. Proc Natl Acad Sci U S A. 2010;107: 8248-8253.
110. Heallen T, Zhang M, Wang J, et al. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science. 2011;332:458-461.
111. Zhao B, Tumaneng K, Guan KL. The Hippo pathway in organ size control, tissue regeneration and stem cell selfrenewal. Nat Cell Biol. 2011;13:877-883.
112. Johnson R, Halder G. The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat Rev Drug Discov. 2014;13:63-79.
113. Sansores-Garcia L, Bossuyt W, Wada K, et al. Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J. 2011;30:2325-2335.
114. Fernández BG, Gaspar P, Brás-Pereira C, Jezowska B, Rebelo SR, Janody F. Actin-capping protein and the Hippo pathway regulate F-actin and tissue growth in Drosophila. Development. 2011;138:2337-2346.
115. Liu-Chittenden Y, Huang B, Shim JS, et al. Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev. 2012;26:1300-1305.
116. Brigstock D. The CCN family: a new stimulus package. J Endocrinol. 2003;178:169-175.
117. Robertson GA. Ovarian transplantation in the house mouse. Proc Soc Exp Biol Med. 1940;44:302-304.
118. Russell WL, Hurst JG. Pure strain mice born to hybrid mothers following ovarian transplantation. Proc Natl Acad Sci U S A. 1945;31:267-273.
119. Stevens LC. A modification of Robertson's technique of homoiotopic ovarian transplantation in mice. Transplant Bull. 1957;4:106-107.
120. Baird DT, Webb R, Campbell BK, Harkness LM, Gosden RG. Long-term ovarian function in sheep after ovariectomy and transplantation of autografts stored at -196 C. Endocrinology. 1999;140:462-471.
121. XuJ, Bernuci MP, Lawson MS, et al. Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated threedimensional culture: effects of gonadotropins and insulin. Reproduction. 2010;140:685-697.
122. Zheng W, Zhang H, Gorre N, Risal S, Shen Y, Liu K. Two classes of ovarian primordial follicles exhibit distinct developmental dynamics and physiological functions. Hum Mol Genet. 2014;23:920-928.
123. Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev. 1996;17: 121-155.
124. Baker SJ, Spears N. The role of intra-ovarian interactions in the regulation of follicle dominance. Hum Reprod Update. 1999;5:153-165.
125. Xia Y, Chang T, Wang Y, et al. YAP promotes ovarian cancer cell tumorigenesis and is indicative of a poor prognosis for ovarian cancer patients. PLoS One. 2014;9: e91770.
126. Bione S, Sala C, Manzini C, et al. A human homologue of the Drosophila melanogaster diaphanous gene is disrupted in a patient with premature ovarian failure: evidence for conserved function in oogenesis and implications for human sterility. Am J Hum Genet. 1998;62:533-541.
127. He C, Kraft P, Chasman DI, et al. A large-scale candidate gene association study of age at menarche and age at natural menopause. Hum Genet. 2010;128:515-527.
128. Schuh-Huerta SM, Johnson NA, Rosen MP, Sternfeld B, Cedars MI, Reijo Pera RA. Genetic markers of ovarian follicle number and menopause in women of multiple ethnicities. Hum Genet. 2012;131:1709-1724.
129. St John MA, Tao W, Fei X, et al. Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nat Genet. 1999;21:182-186.
130. Pisarska MD, Kuo FT, Bentsi-Barnes IK, Khan S, Barlow GM. LATS1 phosphorylates forkhead L2 and regulates its transcriptional activity. Am J Physiol Endocrinol Metab. 2010;299:E101-E109.
131. Li T, Zhao H, Zhao X, et al. Identification of YAP1 as a novel susceptibility gene for polycystic ovary syndrome. J Med Genet. 2012;49:254-257.
132. Hall CA, Wang R, Miao J, et al. Hippo pathway effector Yap is an ovarian cancer oncogene. Cancer Res. 2010;70: 8517-8525.
133. Nagashima T, Kim J, Li Q, et al. Connective tissue growth factor is required for normal follicle development and ovulation. Mol Endocrinol. 2011;25:1740-1759.
134. Aboura A, Dupas C, Tachdjian G, et al. Array comparative genomic hybridization profiling analysis reveals deoxyribonucleic acid copy number variations associated with premature ovarian failure. J Clin Endocrinol Metab. 2009; 94:4540-4546.
135. Halder G, Dupont S, Piccolo S. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat Rev Mol Cell Biol. 2012;13:591-600.
136. Dupont S, Morsut L, Aragona M, et al. Role of YAP/TAZ in mechanotransduction. Nature. 2011;474:179-183.
137. Slager HG, Good MJ, Schaart G, Groenewoud JS, Mummery CL. Organization of non-muscle myosin during early murine embryonic differentiation. Differentiation. 1992; 50:47-56.
138. Nishioka N, Inoue K, Adachi K, et al. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell. 2009;16:398-410.
139. Weigelt B, Bissell MJ. Unraveling the microenvironmental influences on the normal mammary gland and breast cancer. Semin Cancer Biol. 2008;311-321.
140. Paszek MJ, Zahir N, Johnson KR, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell. 2005;8: 241-254.
141. West ER, Xu M, Woodruff TK, Shea LD. Physical properties of alginate hydrogels and their effects on in vitro follicle development. Biomaterials. 2007;28:4439-4448.
142. Woodruff TK, Shea LD. A new hypothesis regarding ovarian follicle development: ovarian rigidity as a regulator of selection and health. J Assist Reprod Genet. 2011;28:3-6.
143. Gallardo TD, John GB, Shirley L, et al. Genomewide discovery and classification of candidate ovarian fertility genes in the mouse. Genetics. 2007;177:179-194.
144. Hutt KJ, McLaughlin EA, Holland MK. KIT/KIT ligand in mammalian oogenesis and folliculogenesis: roles in rabbit and murine ovarian follicle activation and oocyte growth. Biol Reprod. 2006;75:421-433.
145. Parrott JA, SkinnerMK.Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology. 1999;140:4262-4271.
146. Ojeda SR, Romero C, Tapia V, Dissen GA. Neurotrophic and cell-cell dependent control of early follicular development. Mol Cell Endocrinol. 2000;163:67-71.
147. Roberts AE, Arbogast LK, Friedman CI, Cohn DE, KaumayaPT, DanforthDR.Neutralization of endogenous vascular endothelial growth factor depletes primordial follicles in the mouse ovary. Biol Reprod. 2007;76:218-223.
148. Tanwar PS, O'Shea T, McFarlane JR. In vivo evidence of role of bone morphogenetic protein-4 in the mouse ovary. Anim Reprod Sci. 2008;106:232-240.
149. Lee WS, Otsuka F, Moore RK, Shimasaki S. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol Reprod. 2001;65:994-999.
150. Nilsson EE, Kezele P, Skinner MK. Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol Cell Endocrinol. 2002;188: 65-73.
151. Nilsson E, Parrott JA, SkinnerMK.Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol Cell Endocrinol. 2001;175:123- 130.
152. Kezele P, Nilsson EE, Skinner MK. Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biol Reprod. 2005;73:967-973.
153. Adhikari D, Liu K. Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocr Rev. 2009;30:438-464.
154. Reddy P, Shen L, Ren C, et al. Activation of Akt (PKB) and suppression of FKHRL1 in mouse and rat oocytes by stem cell factor during follicular activation and development. Dev Biol. 2005;281:160-170.
155. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science. 2003;301:215- 218.
156. Reddy P, Liu L, Adhikari D, Jet al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science. 2008;319:611-613.
157. John GB, Gallardo TD, Shirley LJ, Castrillon DH. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol. 2008;321:197-204.
158. Tarnawa ED, BakerMD,AloisioGM,Carr BR, Castrillon DH. Gonadal expression of foxo1, but not foxo3, is conserved in diverse mammalian species. Biol Reprod. 2013; 88:103.
159. Fan HY, Liu Z, Cahill N, Richards JS. Targeted disruption of Pten in ovarian granulosa cells enhances ovulation and extends the life span of luteal cells. Mol Endocrinol. 2008; 22:2128-2140.
160. Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci. 2009;122:3589-3594.
161. Adhikari D, Flohr G, Gorre N, et al. Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol Hum Reprod. 2009;15:765-770.
162. Adhikari D, Zheng W, Shen Y, Gorre N, et al. Tsc/ mTORC1 signaling in oocytes governs the quiescence and activation of primordial follicles. Hum Mol Genet. 2010; 19:397-410.
163. Adhikari D, Liu K. mTOR signaling in the control of activation of primordial follicles. Cell Cycle. 2010;9:1673- 1674.
164. Huang L, Wang ZB, Jiang ZZ, et al. Specific disruption of Tsc1 in ovarian granulosa cells promotes ovulation and causes progressive accumulation of corpora lutea. PLoS One. 2013;8:e54052.
165. Li J, Kawamura K, Cheng Y, et al. Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci U S A. 2010;107:10280-10284.
166. Zeleznik AJ, Saxena D, Little-Ihrig L. Protein kinase B is obligatory for follicle-stimulating hormone-induced granulosa cell differentiation. Endocrinology. 2003;144: 3985-3994.
167. Kalous J, Solc P, Baran V, Kubelka M, SchultzRM, Motlik J. PKB/AKT is involved in resumption of meiosis in mouse oocytes. Biol Cell. 2006;98:111-123.
168. Adashi E. Growth factors and ovarian function: the IGF-I paradigm. Horm Res Paediatr. 1994;42:44-48.
169. McGee EA, Chun SY, Lai S, He Y, Hsueh AJ. Keratinocyte growth factor promotes the survival, growth, and differentiation of preantral ovarian follicles. Fertil Steril. 1999; 71:732-738.
170. Danforth DR, Arbogast LK, Ghosh S, Dickerman A, Rofagha R, Friedman CI. Vascular endothelial growth factor stimulates preantral follicle growth in the rat ovary. Biol Reprod. 2003;68:1736-1741.
171. Matos MH, Lima-Verde IB, Bruno JB, et al. Follicle stimulating hormone and fibroblast growth factor-2 interact and promote goat primordial follicle development in vitro. Reprod Fertil Dev. 2007;19:677-684.
172. Chaves RN, Lima-Verde IB, Celestino JJ, et al. Fibroblast growth factor-10 maintains the survival and promotes the growth of cultured goat preantral follicles. Domest Anim Endocrinol. 2010;39:249-258.
173. Coulam CB, Adamson SC, Annegers JF. Incidence of premature ovarian failure. Obstet Gynecol. 1986;67:604- 606.
174. Goswami D, Conway GS. Premature ovarian failure.Hum Reprod Update. 2005;11:391-410.
175. De Vos M, Devroey P, Fauser BC. Primary ovarian insufficiency. Lancet. 2010;376:911-921.
176. Fénichel P, Sosset C, Barbarino-Monnier P, et al. Prevalence, specificity and significance of ovarian antibodies during spontaneous premature ovarian failure. Hum Reprod. 1997;12:2623-2628.
177. Hoek A, Schoemaker J, Drexhage H. Premature ovarian failure and ovarian autoimmunity. Endocr Rev. 1997;18: 107-134.
178. Donnez J, Dolmans MM. Fertility preservation in women. Nat Rev Endocrinol. 2013;9:735-749.
179. Sauer MV, Paulson RJ, Lobo RA. A preliminary report on oocyte donation extending reproductive potential to women over 40. N Engl J Med. 1990;323:1157-1160.
180. Suzuki N, Hashimoto S, Igarashi S, et al. Assessment of long-term function of heterotopic transplants of vitrified ovarian tissue in cynomolgus monkeys. Hum Reprod. 2012;27:2420-2429.
181. Adhikari D, Gorre N, Risal S, et al. The safe use of a PTEN inhibitor for the activation of dormant mouse primordial follicles and generation of fertilizable eggs. PLoS One. 2012;7:e39034.
182. Bidet M, Bachelot A, Bissauge E, et al. Resumption of ovarian function and pregnancies in 358 patients with premature ovarian failure. J Clin Endocrinol Metab. 2011; 96:3864-3872.
183. McLaughlin M, Kinnell HL, Anderson RA, Telfer EE. Inhibition of phosphatase and tensin homolog (PTEN) in human ovary in vitro results in increased activation of primordial follicles but compromises development of growing follicles. Mol Hum Reprod. 2014;20:736-744.
184. Broer SL, Dólleman M, Opmeer BC, Fauser BC, Mol BW, Broekmans FJ. AMH and AFC as predictors of excessive response in controlled ovarian hyperstimulation: a metaanalysis. Hum Reprod Update. 2011;17:46-54.
185. La Marca A, Sighinolfi G, Radi D, et al. Anti-Mullerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update. 2010; 16:113-130.
186. Dewailly D, Andersen CY, Balen A, et al. The physiology and clinical utility of anti-Müllerian hormone in women. Hum Reprod Update. 2014;20:804.
187. Broer SL BF, Laven JS, Fauser BC. Anti-Mullerian hormone: ovarian reserve testing and its potential clinical implications. Hum Reprod Update. 2014;20:688-701.
188. Weenen C, Laven JS, Von Bergh AR, et al. Anti-Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol Hum Reprod. 2004;10:77-83.
189. Pigny P, Merlen E, Robert Y, et al. Elevated serum level of anti-Mullerian hormone in patients with polycystic ovary syndrome: relationship to the ovarian follicle excess and to the follicular arrest. J Clin Endocrinol Metab. 2003;88: 5957-5962.
190. Iliodromiti S, Kelsey TW, Anderson RA, Nelson SM. Can anti-Mullerian hormone predict the diagnosis of polycystic ovary syndrome?Asystematic review and meta-analysis of extracted data. J Clin Endocrinol Metab. 2013;98:3332- 3340.
191. van Rooij IA, Broekmans FJ, te Velde ER, et al. Serum anti-Müllerian hormone levels: a novel measure of ovarian reserve. Hum Reprod. 2002;17:3065-3071.
192. Modi D, Bhartiya D, Puri C. Developmental expression and cellular distribution of Mullerian inhibiting substance in the primate ovary. Reproduction. 2006;132:443-453.
193. Tran ND, Cedars MI, Rosen MP. The role of anti-müllerian hormone (AMH) in assessing ovarian reserve. J Clin Endocrinol Metab. 2011;96:3609-3614.
194. Hansen KR, Hodnett GM, Knowlton N, Craig LB. Correlation of ovarian reserve tests with histologically determined primordial follicle number. Fertil Steril. 2011;95: 170-175.
195. McGrath SA, Esquela AF, Lee SJ. Oocyte-specific expression of growth/differentiation factor-9. Mol Endocrinol. 1995;9:131-136.
196. Aaltonen J, Laitinen MP, Vuojolainen K, et al. Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab. 1999;84:2744- 2750.
197. Pache T, Wladimiroff J, De Jong F, Hop W, Fauser B. Growth patterns of nondominant ovarian follicles during the normal menstrual cycle. Fertil Steril. 1990;54:638.
198. van Stanbrink EJ, Hop WC, van Dessel TJ, de Jong FH, Fauser BC. Decremental follicle-stimulating hormone and dominant follicle development during the normal menstrual cycle. Fertil Steril. 1995;64:37-43.
199. Ferraretti AP, La Marca A, Fauser BC, et al. ESHRE consensus on the definition of 'poor response' to ovarian stimulation for in vitro fertilization: the Bologna criteria. Hum Reprod. 2011;26:1616-1624.
200. Ventura SJ, Abma JC, Mosher WD, Henshaw SK. 2008 Estimated pregnancy rates by outcome for the United States, 1990-2004. Natl Vital StatRep. 2008;56:1-25, 28.
201. Santoro N. Update in hyper- and hypogonadotropic amenorrhea. J Clin Endocrinol Metab. 2011;96:3281-3288.
202. Broekmans FJ, Knauff EA, Valkenburg O, Laven JS, Eijkemans MJ, Fauser BC.PCOSaccording to the Rotterdam consensus criteria: Change in prevalence among WHO-II anovulation and association with metabolic factors. BJOG. 2006;113:1210-1217.
203. Dewailly D, Lujan ME, Carmina E, et al. Definition and significance of polycystic ovarian morphology: a task force report from the Androgen Excess and Polycystic Ovary Syndrome Society. Hum Reprod Update. 2014;20:334- 352.
204. Farquhar C, Lilford RJ, Marjoribanks J, Vandekerckhove P. Laparoscopic 'drilling' by diathermy or laser for ovulation induction in anovulatory polycystic ovary syndrome. Cochrane Database Syst Rev. 2007;3:CD001122.
205. Abu Hashim H, Al-Inany H, De Vos M, Tournaye H. Three decades after Gjönnaess's laparoscopic ovarian drilling for treatment of PCOS; what do we know? An evidence- based approach. Arch Gynecol Obstet. 2013;288: 409-422.
206. Bayram N, Van Wely M, Kaaijk EM, Bossuyt PM, van der Veen F. Using an electrocautery strategy or recombinant follicle stimulating hormone to induce ovulation in polycystic ovary syndrome: randomised controlled trial. BMJ. 2004;328:192.
207. Judd HL, Rigg LA, Anderson DC, Yen SS. The effects of ovarian wedge resection on circulating gonadotropin and ovarian steroid levels in patients with polycystic ovary syndrome. J Clin Endocrinol Metab. 1976;43:347-355.
208. Hendriks ML, Ket JC, Hompes PG, Homburg R, Lambalk CB. Why does ovarian surgery in PCOS help? Insight into the endocrine implications of ovarian surgery for ovulation induction in polycystic ovary syndrome.HumReprod Update. 2007;13:249-264.
209. Chen ZJ, Zhao H, He L, et al. Genome-wide association study identifies susceptibility loci for polycystic ovary syndrome on chromosome 2p16.3, 2p21 and 9q33.3. Nat Genet. 2011;43:55-59.
210. Evian Annual Reproduction (EVAR) Workshop Group 2010; Fauser B, Diedrich K, Bouchard P, et al. Contemporary genetic technologies and female reproduction. Hum Reprod Update. 2011;17:829-847.
211. Louwers YV, Stolk L, Uitterlinden AG, Laven JS. Crossethnic meta-analysis of genetic variants for polycystic ovary syndrome. J Clin Endocrinol Metab. 2013;98: E2006-E2012.
212. Zhao H, Chen ZJ. Genetic association studies in female reproduction: from candidate-gene approaches to genome- wide mapping. Mol Hum Reprod. 2013;19:644- 654.
213. Urbanek M, Legro RS, Driscoll DA, et al. Thirty-seven candidate genes for polycystic ovary syndrome: strongest evidence for linkage is with follistatin. Proc Natl Acad Sci U S A. 1999;96:8573-8578.
214. Ewens KG, Stewart DR, Ankener W, et al. Family-based analysis of candidate genes for polycystic ovary syndrome. J Clin Endocrinol Metab. 2010;95:2306-2315.
215. Louwers YV, de Jong FH, van Herwaarden NA, et al. Variants in SULT2A1 affect theDHEAsulphate toDHEAratio in patients with polycystic ovary syndrome but not the hyperandrogenic phenotype. J Clin Endocrinol Metab. 2013;98:3848-3855.
216. Wang P, Zhao H, Li T, et al. Hypomethylation of the LH/ choriogonadotropin receptor promoter region is a potential mechanism underlying susceptibility to polycystic ovary syndrome. Endocrinology. 2014;155:1445-1452.
217. McAllister JM, Modi B, Miller BA, et al. Overexpression of a DENND1A isoform produces a polycystic ovary syndrome theca phenotype. Proc Natl Acad Sci U S A. 2014; 111:E1519-E1527.
218. Hsueh AJ, Rauch R. Ovarian Kaleidoscope database: ten years and beyond. Biol Reprod. 2012;86:192.
219. Hughesdon P. Morphology and morphogenesis of the Stein-Leventhal ovary and of so-called "hyperthecosis". Obstet Gynecol Surv. 1982;37:59-77.
220. Blank SK, McCartney CR, Chhabra S, et al. Modulation of gonadotropin-releasing hormone pulse generator sensitivity to progesterone inhibition in hyperandrogenic adolescent girls-implications for regulation of pubertal maturation. J Clin Endocrinol Metab. 2009;94:2360-2366.
221. Urbanek M, Sam S, Legro RS, Dunaif A. Identification of a polycystic ovary syndrome susceptibility variant in fibrillin- 3 and association with a metabolic phenotype. J Clin Endocrinol Metab. 2007;92:4191-4198.
222. Hatzirodos N, Bayne RA, Irving-Rodgers HF, et al. Linkage of regulators of TGF-β activity in the fetal ovary to polycystic ovary syndrome. FASEB J. 2011;25:2256- 2265.
223. Garrido N, Bellver J, Remohí J, Simón C, Pellicer A. Cumulative live-birth rates per total number of embryos needed to reach newborn in consecutive in vitro fertilization (IVF) cycles: a new approach to measuring the likelihood of IVF success. Fertil Steril. 2011;96:40-46.
224. Kawwass JF, Monsour M, Crawford S, et al. Trends and outcomes for donor oocyte cycles in the United States, 2000-2010. JAMA. 2013;310:2426-2434.
225. Dunaif A, Fauser B. RenamingPCOS-atwo-state solution. J Clin Endocrinol Metab. 2013;98:4325-4328.
226. Reddy P, Deguchi M, Cheng Y, Hsueh AJ. Actin cytoskeleton regulates Hippo signaling. PLoS One. 2013;8: e73763.
227. Yu FX, Zhao B, Panupinthu N, et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell. 2012;150:780-791.
228. Miller E, Yang J, DeRan M, et al. Identification of Serumderived sphingosine-1-phosphate as a small molecule regulator of YAP. Chem Biol. 2012;19:955-962.
229. Mo JS, Yu FX, Gong R, Brown JH, Guan KL. Regulation of the Hippo-YAP pathway by protease-activated receptors (PARs). Genes Dev. 2012;26:2138-2143.
230. Schuh-Huerta SM, Johnson NA, Rosen MP, Sternfeld B, Cedars MI, Reijo Pera RA. Genetic variants and environmental factors associated with hormonal markers of ovarian reserve in Caucasian and African American women. Hum Reprod. 2012;27:594-608.