The ovarian reserve in mammals: A functional and evolutionary perspective

Molecular and Cellular Endocrinology

Volumn 356, Issue 1-2, 2012, Pages 2-12

  Monget, Philippe ^a,b,c,d   Bobe, Julien ^e   Gougeon, Alain ^f   Fabre, Stéphane ^a,b,c,d   Monniaux, Danielle ^a,b,c,d   Dalbies Tran, Rozenn ^a,b,c,d  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d IFCE   (France)

^e Campus de Beaulieu   (France)

^f CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

Author keywords

Apoptosis; Depletion; Follicles; Oocytes; Proliferation; Reserve

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 15; FORKHEAD BOX L2 TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTOR; MUELLERIAN INHIBITING FACTOR; NOTCH RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN BCL 2; PROTEIN KINASE B; SMAD PROTEIN; SOHLH1 PROTEIN; SOHLH2 PROTEIN; STEM CELL FACTOR; STRA8 PROTEIN; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FIGLA; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR LHX8; TRANSCRIPTION FACTOR NOBOX; UNCLASSIFIED DRUG; VASA PROTEIN; WT1 PROTEIN;

APOPTOSIS; BMP15 GENE; CELL MIGRATION; CELL RENEWAL; COELOMIC EPITHELIUM; EPITHELIUM; GENE; GENE MUTATION; GRANULOSA CELL; HUMAN; INHA GENE; INTRACELLULAR SIGNALING; MESONEPHROS; NONHUMAN; OOCYTE DEVELOPMENT; OVARIAN RESERVE; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; PREMATURE OVARIAN FAILURE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; REVIEW; SEX DIFFERENTIATION; SEX TRANSFORMATION; ZONA PELLUCIDA;

ANIMALS; APOPTOSIS; BIOLOGICAL EVOLUTION; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; OOGENESIS; OVARIAN FOLLICLE; OVARY; OVUM; PRIMARY OVARIAN INSUFFICIENCY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84859644461     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.07.046     Document Type: Review

References (143)

1. Achermann J.C., Ito M., Ito M., et al. A mutation in the gene encoding steroidogenic factor-1 causes XY sex reversal and adrenal failure in humans. Nat. Genet. 1999, 22:125-126.
2. Allen L.A., Achermann J.C., Pakarinen P., et al. A novel loss of function mutation in exon 10 of the FSH receptor gene causing hypergonadotrophic hypogonadism: clinical and molecular characteristics. Hum. Reprod. 2003, 18:251-256.
3. Anderson E.L., Baltus A.E., Roepers-Gajadien H.L., et al. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc. Natl. Acad. Sci. USA 2008, 105:14976-14980.
4. Baarends W.M., Uilenbroek J.T., Kramer P., et al. Anti-müllerian hormone and anti-müllerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during post-natal development, the estrous cycle, and gonadotropin-induced follicle development. Endocrinology 1995, 136:4951-4962.
5. Baron D., Batista F., Chaffaux S., et al. Foxl2 gene and the development of the ovary: a story about goat, mouse, fish and woman. Reprod. Nut. Dev. 2005, 45:377-382.
6. Beck A.R.P., Miller I.J., Anderson P., Streuli M. RNA-binding protein TIAR is essential for primordial germ cell development. Proc. Natl. Acad. Sci. USA 1998, 9:2331-2336.
7. Bedell M.A., Brannan C.I., Evans E.P., et al. DNA rearrangements located over 100kb 5' of the Steel (Sl)-coding region in Steel-panda and Steel-contrasted mice deregulate Sl expression and cause female sterility by disrupting ovarian follicle development. Genes Dev. 1995, 9:455-470.
8. Begum S., Papaioannou V.E., Gosden R.G. The oocyte population is not renewed in transplanted or irradiated adult ovaries. Hum. Reprod. 2008, 23:2326-2330.
9. Benedict J.C., Lin T.M., Loeffler I.K., et al. Physiological role of the aryl hydrocarbon receptor in mouse ovary development. Toxicol. Sci. 2000, 56:382-388.
10. Bergeron L., Perez G.I., Macdonald G., et al. Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev. 1998, 12:1304-1314.
11. Beysen D., Vandesompele J., Messiaen L., et al. The human FOXL2 mutation database. Hum. Mutat. 2004, 24:189-193.
12. Billard R. The reproductive cycle of male and female brown trout (Slamo trutta fario): a quantitative study. Reprod. Nut. Dev. 1987, 27:29-44.
13. Birk O.S., Casiano D.E., Wassif C.A., et al. The LIM homeobox gene Lhx9 is essential for mouse gonad formation. Nature 2000, 403:909-913.
14. Bobe J., Nguyen T., Mahe S., Monget P. In silico identification and molecular characterization of genes predominantly expressed in the fish oocyte. BMC Genomics 2008, 9:499.
15. Bowles J., Knight D., Smith C., et al. Retinoid signaling determines germ cell fate in mice. Science 2006, 312:596-600.
16. Brenkman A.B., Burgering B.M. FoxO3a eggs on fertility and aging. Trends Mol. Med. 2003, 9:464-467.
17. Brinster R.L., Zimmermann J.W. Spermatogenesis following male germ cell transplantation. Proc. Natl. Acad. Sci. USA 1994, 91:11298-11302.
18. Bukovsky A., Caudle M.R., Svetlikova M., Upadhyaya N.B. Origin of germ cells and formation of new primary follicles in adult human ovaries. Reprod. Biol. Endocrinol. 2004, 2:1-30.
19. Byskov A.G., Faddy M.J., Lemmen J.G., Andersen C.Y. Eggs forever?. Differentiation 2005, 73:438-446.
20. Calvi L.M., Adams G.B., Weibrecht K.W. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425:841-846.
21. Castrillon D.H., Miao L., Kollipara R., et al. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003, 301:215-218.
22. Chang H., Matzuk M.M. Smad5 is required for mouse primordial germ cell development. Mech. Dev. 2001, 104:61-67.
23. Chen M., Tomkins D.J., Auerbach W., et al. Inactivation of FAC in mice produces inductible chromosomal instability and reduced fertility reminiscent of Fanconi anemia. Nat. Genet. 1996, 12:448-451.
24. Chen Y., Jefferson W.N., Newbold R.R., et al. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 2007, 148:3580-3590.
25. Choi Y., Ballow D.J., Xin Y., Rajkovic A. Lim homeobox gene, lhx8, is essential for mouse oocyte differentiation and survival. Biol. Reprod. 2008, 79:442-449.
26. Choi Y., Yuan D., Rajkovic A. Germ cell-specific transcriptional regulator sohlh2 is essential for early mouse folliculogenesis and oocyte-specific gene expression. Biol. Reprod. 2008, 79:1176-1182.
27. Clelland E., Kohli G., Campbell R.K., et al. Bone morphogenetic protein-15 in the zebrafish ovary: complementary deoxyribonucleic acid cloning, genomic organization, tissue distribution, and role in oocyte maturation. Endocrinology 2006, 147:201-209.
28. Clelland E.S., Tan Q., Balofsky A., et al. Inhibition of premature oocyte maturation: a role for bone morphogenetic protein 15 in zebrafish ovarian follicles. Endocrinology 2007, 148:5451-5458.
29. Correa R.V., Domenice S., Bingham N.C., et al. A microdeletion in the ligand binding domain of human steroidogenic factor 1 causes XY sex reversal without adrenal insufficiency. J. Clin. Endocrinol. Metab. 2004, 89:1767-1772.
30. Craig-Bennett A. The reproductive cycle of the three-spined stickleback, Gasterosteus aculeatus. Limm. Phil. Trans. B. 1930, 219:197-281.
31. Crisponi L., Deiana M., Loi A., et al. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat. Genet. 2001, 27:159-166.
32. Dadé S., Callebaut I., Paillisson A., et al. In silico identification and structural features of six new genes similar to MATER specifically expressed in the oocyte. Biochem. Biophys. Res. Commun. 2004, 324:547-553.
33. Dharma S.J., Modi D.N., Nandedkar T.D. Gene expression profiling during early folliculogenesis in the mouse ovary. Fertil. Steril. 2009, 91:2025-2036.
34. Di Pasquale E., Rossetti R., Marozzi A., et al. Identification of new variants of human BMP15 gene in a large cohort of women with premature ovarian failure. J. Clin. Endocrinol. Metab. 2006, 91:1976-1979.
35. Dipietromaria A., Benayoun B.A., Todeschini A.L., et al. Towards a functional classification of pathogenic FOXL2 mutations using transactivation reporter systems. Hum. Reprod. Genet. 2009, 18:3324-3333.
36. Dissen G.A., Garcia-Rudaz C., Ojeda S.R. Role of neurotrophic factors in early ovarian development. Semin. Reprod. Med. 2009, 27:24-31.
37. Dixit H., Deendayal M., Singh L. Mutational analysis of the mature peptide region of inhibin genes in Indian women with ovarian failure. Hum. Reprod. 2004, 19:1760-1764.
38. Dixit H., Rao L.K., Padmalatha V., et al. Mutational screening of the coding region of growth differentiation factor 9 gene in Indian women with ovarian failure. Menopause 2005, 12:749-754.
39. Dixit H., Rao L.K., Padmalatha V.V., et al. Missense mutations in the BMP15 gene are associated with ovarian failure. Hum. Genet. 2006, 119:408-415.
40. Durlinger A.L., Kramer P., Karels B., et al. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology 1999, 140:5789-5796.
41. Dyce P.W., Wen L., Li J. In vitro germline potential of stem cells derived from fetal porcine skin. Nat. Cell Biol. 2006, 8:384-390.
42. Edson M.A., Nagaraja A.K., Matzuk M.M. The mammalian ovary from genesis to revelation. Endocr. Rev. 2009, 30:624-712.
43. Eggan K., Jurga S., Gosden R. Ovulated oocytes in adult mice derive from non-circulating germ cells. Nature 2006, 441:1109-1114.
44. Eggert B. Die Geschlechtsorgane der Gobiiformes und Blenniformes. Zwiss. Zool. 1931, 139:249-558.
45. Elis S., Dupont J., Couty I., et al. Expression and biological effects of bone morphogenetic protein-15 in the hen ovary. J. Endocrinol. 2007, 194:485-497.
46. Ennis S., Ward D., Murray A. Nonlinear association between CGG repeat number and age of menopause in FMR1 premutation carriers. Eur. J. Hum. Genet. 2006, 14:253-255.
47. Faddy M.J., Gosden R.G., Gougeon A., et al. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum. Reprod. 1992, 7:1342-1346.
48. Farini D., La Sala G., Tedesco M., De Felici M. Chemoattractant action and molecular signaling pathways of Kit ligand on mouse primordial germ cells. Dev. Biol. 2007, 306:572-583.
49. Franchi L.L., Mandle A.M., Zuckerman S. The development of the ovary and the process of oogenesis. The ovary 1962, 1-88. Academic Press, New York. Jones (Ed.).
50. Fuchs E., Tumbar T., Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 2004, 116:769-778.
51. Goudet G., Mugnier S., Callebaut I., Monget P. Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol. Reprod. 2008, 78:796-806.
52. Gougeon A., Delangle A., Arouche N., et al. Kit ligand and the somatostatin receptor antagonist, BIM-23627, stimulate in vitro resting follicle growth in the neonatal mouse ovary. Endocrinology 2010, 151:1299-1309.
53. Gougeon A., Ecochard R., Thalabard J.C. Age-related changes of the population of human ovarian follicles: increase in the disappearance rate of non-growing and early-growing follicles in aging women. Biol. Reprod. 1994, 50:653-663.
54. Greenbaum M.P., Iwamori N., Agno J.E., Matzuk M.M. Mouse TEX14 is required for embryonic germ cell intercellular bridges but not female fertility. Biol. Reprod. 2009, 80:449-457.
55. Greenbaum M.P., Yan W., Wu M.H., et al. TEX14 is essential for intercellular bridges and fertility in male mice. Proc. Natl. Acad. Sci. USA 2006, 103:4982-4987.
56. Greenfeld C.R., Pepling M.E., Babus J.K., et al. BAX regulates follicular endowment in mice. Reproduction 2007, 133:865-876.
57. Grier H.J., Uribe M.C., Parenti L.R. Germinal epithelium, folliculogenesis, and postovulatory follicles in ovaries of rainbow trout, Oncorhynchus mykiss (Walbaum, 1792) (Teleostei, protacanthopterygii, salmoniformes). J. Morphol. 2007, 268:293-310.
58. Hahn K.L., Johnson J., Beres B.J., et al. Lunatic fringe null female mice are infertile due to defects in meiotic maturation. Development 2005, 132:817-828.
59. Hann H.W. The history of the germ cell of Cottus bairdii Girard. J. Morph. 1927, 43:427-497.
60. Hao J., Yamamoto M., Richardson T.E., et al. Sohlh2 knockout mice are male-sterile because of degeneration of differentiating type A spermatogonia. Stem Cells 2008, 26:1587-1597.
61. Hayashi K., Kobayashi T., Umino T., et al. SMAD1 signaling is critical for initial commitment of germ cell lineage from mouse epiblast. Mech. Dev. 2002, 118:99-109.
62. Hirshfield A.N., DeSanti A.M. Patterns in ovarian cell proliferation in rats during the embryonic period and the first three weeks post-partum. Biol. Reprod. 1995, 53:1208-1221.
63. Holt J.E., Jackson A., Roman S.D. CXCR4/SDF1 interaction inhibits the primordial to primary follicle transition in the neonatal mouse ovary. Dev. Biol. 2006, 293:449-460.
64. Huang E.J., Manova K., Packer A.I., et al. The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Dev. Biol. 1993, 157:100-109.
65. Jalabert B. Particularities of reproduction and oogenesis in teleost fish compared to mammals. Reprod. Nut. Dev. 2005, 45:261-279.
66. John G.B., Gallardo T.D., Shirley L.J., Castrillon D.H. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev. Biol. 2008, 321:197-204.
67. Johnson J., Canning J., Kaneko T., et al. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004, 428:145-150.
68. Johnson J., Bagley J., Skaznik-Wikiel M., et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell 2005, 122:303-315.
69. Kevenaar M.E., Meerasahib M.F., Kramer P., et al. Serum anti-mullerian hormone levels reflect the size of the primordial follicle pool in mice. Endocrinology 2006, 147:3228-3234.
70. Kezele P., Skinner M.K. Regulation of ovarian primordial follicle assembly and development by estrogen and progesterone: endocrine model of follicle assembly. Endocrinology 2003, 144:3329-3337.
71. Kocer A., Reichmann J., Best D., Adams I.R. Germ cell sex determination in mammals. Mol. Hum. Reprod. 2009, 15:205-213.
72. Koomen M., Cheng N.C., van de Vrugt H.J. Reduced fertility and hypersensitivity to mitomycin C characterize Fancg/Xrcc9 null mice. Hum. Mol. Genet. 2002, 11:273-281.
73. Kovanci E., Rohozinski J., Simpson J.L., et al. Growth differentiating factor-9 mutations may be associated with premature ovarian failure. Fertil. Steril. 2007, 87:143-146.
74. Kuroda H., Terada N., Nakayama H., et al. Infertility due to growth arrest of ovarian follicles in Sl/Slt mice. Dev. Biol. 1988, 126:71-79.
75. 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.
76. Lawson K.A., Dunn N.R., Roelen B.A., et al. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes. Dev. 1999, 13:424-436.
77. Lee W.S., Otsuka F., Moore R.K., Shimasaki S. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol. Reprod. 2001, 65:994-999.
78. Liao B.-Y., Zhang J. Null mutations in human and mouse orthologs frequently result in different phenotypes. Proc. Natl. Acad. Sci. 2008, 105:6987-6992.
79. Liang L., Soyal S.M., Dean J. FIGα, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 1997, 124:4939-4947.
80. Liu L., Rajareddy S., Reddy P., et al. Infertility caused by retardation of follicular development in mice with oocyte-specific expression of Foxo3a. Development 2007, 134:199-209.
81. Lourenco D., Brauner R., Lin L., et al. Mutations in NR5A1 associated with ovarian insufficiency. N. Engl. J. Med. 2009, 360:1200-1210.
82. Lubzens E., Young G., Bobe J., Cerdà J. Oogenesis in teleosts: how fish eggs are formed?. Gen. Comp. Endocrinol. 2010, 165:367-389.
83. Luo X., Ikeda Y., Parker K.L. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 1994, 77:481-490.
84. Luoh S.W., Bain P.A., Polakiewicz R.D., et al. Zfx mutation results in small animal size and reduced germ cell number in male and female mice. Development 1997, 124:2275-2284.
85. MacLean G., Li H., Metzger D., et al. Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology 2007, 148:4560-4567.
86. McMahon H.E., Hashimoto O., Mellon P.L., Shimasaki S. Oocyte-specific overexpression of mouse bone morphogenetic protein-15 leads to accelerated folliculogenesis and an early onset of acyclicity in transgenic mice. Endocrinology 2008, 149:2807-2815.
87. Marozzi A., Porta C., Vegetti W., et al. Mutation analysis of the inhibin alpha gene in a cohort of Italian women affected by ovarian failure. Hum. Reprod. 2002, 17:1741-1745.
88. Meduri G., Touraine P., Beau I., et al. Delayed puberty and primary amenorrhea associated with a novel mutation of the human follicle-stimulating hormone receptor: clinical, histological, and molecular studies. J. Clin. Endocrinol. Metab. 2003, 88:3491-3498.
89. Miyamoto N., Yoshida M., Kuratani S., et al. Defects of urogenital development in mice lacking Emx2. Development 1997, 124:1653-1664.
90. Morrison S.J., Shah N.M., Anderson D.J. Regulatory mechanisms in stem cell biology. Cell 1997, 88:287-298.
91. Naillat F., Prunskaite-Hyyryläinen R., Pietilä I., et al. Wnt4/5a signalling coordinates cell adhesion and entry into meiosis during presumptive ovarian follicle development. Hum. Mol. Genet. 2010, 19:1539-1550.
92. Nakamura S., Kobayashi K., Nishimura T., Higashijima S., Tanaka M. Identification of germline stem cells in the ovary of the teleost medaka. Science 2010, 328:1561-1563.
93. Nakamura S., Kobayashi K., Nishimura T., Tanaka M. Ovarian germline stem cells in the teleost fish, medaka (Oryzias latipes). Int. J. Biol. Sci. 2011, 7:403-409.
94. Nilsson E., Rogers N., Skinner M.K. Actions of anti-mullerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction 2007, 134:209-221.
95. Nilsson E.E., Skinner M.K. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol. Reprod. 2003, 69:1265-1272.
96. Ohinata Y., Payer B., O'Carroll D., et al. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 2005, 436:207-213.
97. Pangas S.A., Choi Y., Ballow D.J., et al. Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. Proc. Natl. Acad. Sci. USA 2006, 103:8090-8095.
98. Park C.-E., Cha K.-Y., Kim K., Lee K.-A. Expression of cell cycle regulatory genes during primordial-primary follicle transition in the mouse ovary. Fertil. Steril. 2005, 83:410-418.
99. Parrott J.A., Skinner M.K. Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 1999, 140:4262-4271.
100. Persani L., Rossetti R., Cacciatore C., Fabre S. Genetic defects of ovarian TGFb-like factors and premature ovarian failure. J. Endocrinol. Invest. 2011, 34:244-251.
101. Qin Y., Choi Y., Zhao H., et al. NOBOX homeobox mutation causes premature ovarian failure. Am. J. Hum. Genet. 2007, 81:576-581.
102. Rajareddy S., Reddy P., Du C., et al. P27kip1 (cyclin-dependent kinase inhibitor 1B) controls ovarian development by suppressing follicle endowment and activation and promoting follicle atresia in mice. Mol. Endocrinol. 2007, 21:2189-2202.
103. Rajkovic A., Pangas S.A., Ballow D., et al. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 2004, 305:1157-1159.
104. Ratts V.S., Flaws J.A., Kolp R., et al. Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the postnatal female mouse gonad. Endocrinology 1995, 136:3665-3668.
105. Reddy P., Adhikari D., Zheng W., et al. PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum. Mol. Genet. 2009, 18:2813-2824.
106. Reddy P., Liu L., Adhikari D., et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008, 319:611-613.
107. 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.
108. Rico C., Fabre S., Médigue C., et al. Anti-mullerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow. Biol. Reprod. 2009, 80:50-59.
109. Robles R., Morita Y., Mann K.K., et al. The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. Endocrinology 2000, 141:450-453.
110. Rodríguez-Marí A., Cañestro C., Bremiller R.A., et al. Sex reversal in zebrafish fancl mutants is caused by Tp53-mediated germ cell apoptosis. PLoS Genet. 2010, 6:e1001034.
111. Rossetti R., Di Pasquale E., Marozzi A., et al. BMP15 mutations associated with primary ovarian insufficiency cause a defective production of bioactive protein. Hum. Mutat. 2009, 30:804-810.
112. Ruggiu M., Speed R., Taggart M., et al. The mouse Daz1a gene encodes a cytoplasmic protein essential for gametogenesis. Nature 1997, 389:73-77.
113. Rybak A., Fuchs H., Smirnova L., et al. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem cell commitment. Nat. Cell. Biol. 2008, 10:987-993.
114. Schmidt D., Ovitt C.E., Anlag K., et al. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 2004, 131:933-942.
115. Shelling A.N., Burton K.A., Chand A.L., et al. Inhibin: a candidate gene for premature ovarian failure. Hum. Reprod. 2000, 15:2644-2649.
116. Skinner M.K. Regulation of primordial follicle assembly and development. Hum. Reprod. Update 2005, 11:461-471.
117. Smith P., O W.-S., Hudson N.L., et al. Effects of the Booroola gene (FecB) on body weight, ovarian development and hormone concentrations during fetal life. J. Reprod. Fertil. 1993, 98:41-54.
118. Soyal S.M., Amleh A., Dean J. FIGα, a germ cell-specific transcription factor required for ovarian follicle formation. Development 2000, 127:4645-4654.
119. Spradling A., Drummond-Barbosa D., Kai T. Stem cells find their niche. Nature 2001, 414:98-104.
120. Toyoda S., Miyazaki T., Miyazaki S. Sohlh2 affects differentiation of KIT positive oocytes and spermatogonia. Dev. Biol. 2009, 325:238-248.
121. Tremblay K.D., Dunn N.R., Robertson E.J., et al. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 2001, 128:3609-3621.
122. Trombly D.J., Woodruff T.K., Mayo K.E. Suppression of Notch signaling in the neonatal mouse ovary decreases primordial follicle formation. Endocrinology 2009, 150:1014-1024.
123. Tsuda M., Sasaoka Y., Kiso M., et al. Conserved role of nanos proteins in germ cell development. Science 2003, 301:1239-1241.
124. Uda M., Ottolenghi C., Crisponi L., et al. Foxl2 disruption causes mouse ovarian failure by pervasive blockade of follicle development. Hum. Mol. Genet. 2004, 13:1171-1181.
125. Visser J.A., de Jong F.H., Laven J.S., Themmen A.P. Anti-Mullerian hormone: a new marker for ovarian function. Reproduction 2006, 131:1-9.
126. Viswanathan S.R., Daley G.Q., Gregory R.I. Selective blockade of microRNA processing by Lin28. Science 2008, 320:97-100.
127. Virant-Klun I., Zech N., Rozman P., et al. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation 2008, 76:843-856.
128. Wallace R.A., Selman K. Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J. Electron Microsc. Tech. 1990, 16(3):175-201.
129. Watkins W.J., Umbers A.J., Woad K.J., et al. Mutational screening of FOXO3A and FOXO1A in women with premature ovarian failure. Fertil. Steril. 2006, 86:1518-1521.
130. Watt F.M., Hogan B.L. Out of Eden: stem cells and their niches. Science 2000, 287:1427-1430.
131. West J.A., Viswanathan S.R., Yabuuchi A., et al. A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 2009, 460:909-913.
132. Wilhelm D., Englert C. The Wilms tumor suppressor WT1 regulates early gonad development by activation of Sf1. Genes Dev. 2002, 16:1839-1851.
133. Wong J.C., Alon N., Mckerlie C., et al. Targeted disruption of exons 1 to 6 of the Fanconi Anemia group A gene leads to growth retardation, strain-specific microphthalmia, meiotic defects and primordial germ cell hypoplasia. Hum. Mol. Genet. 2003, 12:2063-2076.
134. Xie T., Kawase E., Kirilly D., Wong M.D. Intimate relationship with their neighbors: Tales of stem cells in Drosophila reproductive systems. Dev. Dyn. 2005, 232:775-790.
135. Yamaji M., Seki Y., Kurimoto K., et al. Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 2008, 40:1016-1022.
136. Yao K., Ge W. Kit System in the Zebrafish Ovary: Evidence for functional divergence of two isoforms of Kit (Kita and Kitb) and Kit ligand (Kitlga and Kitlgb) during folliculogenesis. Biol. Reprod. 2010, 82:1216-1226.
137. Ying Y., Liu X.M., Marble A., et al. Requirement of BMP8b for the generation of primordial germ cells in the mouse. Mol. Endocrinol. 2000, 14:1053-1063.
138. Ying Y., Zhao G.Q. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev. Biol. 2001, 232:484-492.
139. Yoon S.-J., Kim K.-H., Chung H.-M., et al. Gene expression profiling of early follicular development in primordial, primary, and secondary follicles. Fertil. Steril. 2006, 85:193-203.
140. Youngren K.K., Coveney D., Peng X., et al. The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 2005, 435:360-364.
141. Zachos N.C., Billiar R.B., Albrecht E.D., Pepe G.J. Developmental regulation of baboon fetal ovarian maturation by estrogen. Biol. Reprod. 2002, 67:1148-1156.
142. Zhang J., Niu C., Ye L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003, 425:836-841.
143. Zou K., Yuan Z., Luo H., et al. Production of offspring from a germinal stem cell line derived from neonatal ovaries. Nat. Cell. Biol. 2009, 11:631-636.