Human ovarian follicular development: From activation of resting follicles to preovulatory maturation;Croissance folliculaire dans l'ovaire humain: de l'entrée en croissance du follicule primordial jusqu'à la maturation préovulatoire

Annales d'Endocrinologie

Volumn 71, Issue 3, 2010, Pages 132-143

  Gougeon, A ^a  

^a INSERM   (France)

Author keywords

Follicles; Gonadotropins; Granulosa; Growth factors; Oocyte; Ovary; Steroidogenesis; Theca interna

Indexed keywords

ESTRADIOL; FOLLITROPIN; GONADOTROPIN; LUTEINIZING HORMONE; PROGESTERONE;

ARTICLE; AUTOCRINE EFFECT; CELL DIFFERENTIATION; CELL GROWTH; CELL NUCLEUS; CELL PROLIFERATION; CELL SIZE; CUMULUS CELL; ESTROGEN SYNTHESIS; FOLLICULAR PHASE; FOLLITROPIN BLOOD LEVEL; GRANULOSA CELL; HORMONE SYNTHESIS; HUMAN; LUTEAL PHASE; OOCYTE; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE FLUID; PARACRINE SIGNALING; PROGESTERONE SYNTHESIS; THECA CELL;

AGING; ANTI-MULLERIAN HORMONE; CELL DIFFERENTIATION; CELL DIVISION; FEMALE; FOLLICLE STIMULATING HORMONE; GRANULOSA CELLS; HUMANS; MENSTRUAL CYCLE; OOCYTES; OVARIAN FOLLICLE; OVARY; OVULATION;

EID: 77952743231     PISSN: 00034266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ando.2010.02.021     Document Type: Article

References (139)

1. Eppig J.J., Wigglesworth K., Pendola F.L. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A 2002, 99:2890-2894.
2. Gougeon A., Chainy G.B.N. Morphometric studies of small follicles in ovaries of women at different ages. J Reprod Fertil 1987, 81:433-442.
3. Oktay K., Briggs D., Gosden R.G. Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J Clin Endocrinol Metab 1997, 82:3748-3751.
4. Baker T.G. Quantitative and cytological study of germ cells in human ovaries. Proc R Soc Ser B 1963, 158:417-433.
5. Forabosco A., Sforza C., de Pol A., Vizzotto L., Marzona L., Ferrario V. Morphometric study of the human neonatal ovary. Anat Rec 1991, 231:201-208.
6. 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.
7. Faddy M.J., Gosden R.G., Gougeon A., Richardson S.J., Nelson J.F. Accelerated disappearance of ovarian follicles in mid-life: Implications for forecasting menopause. Hum Reprod 1992, 7:1342-1346.
8. Meredith S., Dudenhoeffer G., Jackson K. Classification of small type B/C follicles as primordial follicles in mature rats. J Reprod Fertil 2000, 119:43-48.
9. van Wezel I.L., Rodgers R.J. Morphological characterization of bovine primordial follicles and their environment in vivo. Biol Reprod 1996, 55:1003-1011.
10. Ratts V.S., Flaws J.A., Kolp R., Sorenson C.M., Tilly J.L. Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 1995, 136:3665-3668.
11. Hsu S.Y., Lai R.J.M., Finegold M., Hsueh A.J.W. Targeted overexpression of bcl-2 in ovaries of transgenic mice leads to decreased follicle apoptosis, enhanced folliculogenesis, and increased germ cell tumorigenesis. Endocrinology 1996, 137:4837-4843.
12. Perez G.I., Robles R., Knudson C.M., Flaws J.A., Korsmeyer S.J., Tilly J.L. Prolongation of ovarian lifespan into advanced chronological age bybax-deficiency. Nat Genet 1999, 21:200-203.
13. Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev 1996, 17:121-155.
14. Kumar T.R., Wang Y., Lu N., Matzuk M.M. Follicle stimulating hormone is required for ovarian follicle maturation but not for male fertility. Nat Genet 1997, 15:201-204.
15. Dierich A., Sairam M.R., Monaco L., Fimia G.M., Gansmuller A., LeMeur M., et al. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci U S A 1998, 95:13612-13617.
16. Matthews C.H., Borgato S., Beck-Peccoz, Adams M., Tone Y., Gambino G., et al. Primary amenorrhoea and infertility due to a mutation in the ß-subunit of follicle-stimulating hormone. Nat Genet 1993, 5:83-86.
17. Durlinger A.L., Gruijters M.J., Kramer P., Karels B., Ingraham H.A., Nachtigal M.W., et al. Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 2002, 143:1076-1084.
18. Nilsson E., Rogers N., Skinner M.K. Actions of anti-Müllerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction 2007, 134:209-221.
19. Carlsson I.B., Scott J.E., Visser J.A., Ritvos O., Themmen A.P., Hovatta O. Anti-Müllerian hormone inhibits initiation of growth of human primordial ovarian follicles in vitro. Hum Reprod 2006, 21:2223-2227.
20. Schmidt K.L., Kryger-Baggesen N., Byskov A.G., Andersen C.Y. Anti-Müllerian hormone initiates growth of human primordial follicles in vitro. Mol Cell Endocrinol 2005, 234:87-93.
21. Rajkumar K., Kerr D.E., Kirkwood R.N., Laarveld B. Inhibitory action of somatostatin-14 on hormone-stimulated cAMP induction in porcine granulosa and luteal cells. J Endocrinol 1992, 134:397-406.
22. Goddard I., Bauer S., Gougeon A., Lopez F., Giannetti N., Susini C., et al. Somatostatin inhibits stem cell factor messenger RNA expression by sertoli cells and stem cell factor-induced DNA synthesis in isolated seminiferous tubules. Biol Reprod 2001, 65:1732-1742.
23. Gougeon A., Delangle A., Arouche N., Stridsberg M., Gotteland J.P., Loumaye E. 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.
24. Castrillon D.H., Miao L., Kollipara R., Horner J.W., DePinho R.A. Suppression of ovarian follicle activation in mice by the transcription factor FOXO3a. Science 2003, 301:215-218.
25. Schmidt D., Ovitt C.E., Anlag K., Fehsenfeld S., Gredsted L., Treier A.C., et al. The murine winged-helix transcription factor FOXL2 is required for granulosa cell differentiation and ovary maintenance. Development 2004, 131:933-942.
26. Méduri G., Bachelot A., Duflos C., Bständig B., Poirot C., Genestie C., et al. FOXL2 mutations lead to different ovarian phenotypes in BPES patients: Case report. Hum Reprod 2010, 25:235-243.
27. Packer A.I., Hsu Y.C., Besmer P., Bachvarova R.F. The ligand of the c-kit receptor promotes oocyte growth. Dev Biol 1994, 161:194-205.
28. Huang E.J., Manova K., Packer A.I., Sanchez S., Bachvarova R.M., Besmer P. The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Dev Biol 1993, 157:100-109.
29. Yoshida H., Takakura N., Kataoka H., Kunisada T., Okamura H., Nishikawa S.I. Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Dev Biol 1997, 184:122-137.
30. Parrott J.A., Skinner M.K. Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 1999, 140:4262-4271.
31. Laitinen M., Rutanen E.M., Ritvos O. Expression of c-kit ligand mRNAs in human ovaries and regulation of their steady state levels by gonadotropins in cultured granulosa-luteal cells. Endocrinology 1995, 136:4407-4414.
32. Horie K., Fujita J., Takakura K., Kanzaki H., Suginami H., Iwai M., et al. The expression of c-kit protein in human adult and fetal tissues. Hum Reprod 1993, 8:1955-1962.
33. Gougeon A., Busso D. Morphologic and functional determinants of primordial and primary follicles in the monkey ovary. Mol Cell Endocrinol 2000, 163:33-41.
34. Dissen G.A., Garcia-Rudaz C., Ojeda S.R. Role of neurotrophic factors in early ovarian development. Semin Reprod Med 2009, 27:24-31.
35. Nilsson E., Dole G., Skinner M.K. Neurotrophin NT3 promotes ovarian primordial to primary follicle transition. Reproduction 2009, 138:697-707.
36. Abir R., Fisch B., Jin S., Barnnet M., Ben-Haroush A., Felz C., et al. Presence of NGF and its receptors in ovaries from human fetuses and adults. Mol Hum Reprod 2005, 11:229-236.
37. Salas C., Julio-Pieper M., Valladares M., Pommer R., Vega M., Mastronardi C., et al. Nerve growth factor-dependent activation of trkA receptors in the human ovary results in synthesis of follicle-stimulating hormone receptors and estrogen secretion. J Clin Endocrinol Metab 2006, 91:2396-2403.
38. Nilsson E.E., Skinner M.K. Kit ligand and basic fibroblast growth factor interactions in the induction of ovarian primordial to primary follicle transition. Mol Cell Endocrinol 2004, 214:19-25.
39. Kezele P.R., Nilsson E.E., Skinner M.K. Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biol Reprod 2005, 73:967-973.
40. Nilsson E.E., Kezele P., Skinner M.K. Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol Cell Endocrinol 2002, 188:65-73.
41. Kezele P.R., Nilsson E.E., Skinner M.K. Insulin but not insulin-like growth factor-1 promotes the primordial to primary follicle transition. Mol Cell Endocrinol 2002, 192:37-43.
42. 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.
43. Nilsson E.E., Detzel C., Skinner M.K. Platelet-derived growth factor modulates the primordial to primary follicle transition. Reproduction 2006, 131:1007-1015.
44. Oktay K., Karlikaya G., Akman O., Ojakian G.K., Oktay M. Interaction of extracellular matrix and activin-A in the initiation of follicle growth in the mouse ovary. Biol Reprod 2000, 63:457-461.
45. Vendola K., Zhou J., Wang J., Famuyiwa O.A., Bievre M., Bondy C.A. Androgens promote oocyte insulin-like growth factor I expression and initiation of follicle development in the primate ovary. Biol Reprod 1999, 61:353-357.
46. Ben-Haroush A., Abir R., Ao A., Jin S., Kessler-Icekson G., Feldberg D., et al. Expression of basic fibroblast growth factor and its receptors in human ovarian follicles from adults and fetuses. Fertil Steril 2005, 84(Suppl. 2):1257-1268.
47. Yamamoto S., Konishi I., Nanbu K., Komatsu T., Mandai M., Kuroda H., et al. Immunohistochemical localization of basic fibroblast growth factor (bFGF) during folliculogenesis in the human ovary. Gynecol Endocrinol 1997, 11:223-230.
48. Ackert C.L., Gittens J.E., O'Brien M.J., Eppig J.J., Kidder G.M. Intercellular communication via connexin 43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev Biol 2001, 233:258-270.
49. Simon A.M., Goodenough D.A., Li E., Paul D.L. Female infertility in mice lacking connexin 37. Nature 1997, 385:525-528.
50. Gougeon A. Rate of follicular growth in the human ovary. Follicular maturation and ovulation 1982, 155-163. Excerpta Medica, Amsterdam. R. Rolland, E.V. van Hall, S.G. Hillier, K.P. McNatty, J. Schoemaker (Eds.).
51. Donnez J., Dolmans M.M., Demylle D., Jadoul P., Pirard C., Squifflet J., et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet 2004, 364:1405-1410.
52. Meduri G., Charnaux N., Driancourt M.A., Combettes L., Granet P., Vannier B., et al. Follicle-stimulating hormone receptors in oocytes?. J Clin Endocrinol Metab 2002, 87:2266-2276.
53. Patsoula E., Loutradis D., Drakakis P., Michalas L., Bletsa R., Michalas S. Messenger RNA expression for the follicle-stimulating hormone receptor and luteinizing hormone receptor in human oocytes and pre-implantation-stage embryos. Fertil Steril 2003, 79:1187-1193.
54. Klinger F.G., De Felici M. In vitro development of growing oocytes from fetal mouse oocytes: stage-specific regulation by stem cell factor and granulosa cells. Dev Biol 2002, 244:85-95.
55. Joyce I.M., Clark A.T., Pendola F.L., Eppig J.J. Comparison of recombinant growth differentiation factor-9 and oocyte regulation of KIT ligand messenger ribonucleic acid expression in mouse ovarian follicles. Biol Reprod 2000, 63:1669-1675.
56. Otsuka F., Shimasaki S. A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis. Proc Natl Acad Sci U S A 2002, 99:8060-8065.
57. Carabatsos M.J., Elvin J., Matzuk M.M., Albertini D.F. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol 1998, 204:373-384.
58. Dong J., Albertini D.F., Nishimori K., Kumar T.R., Lu N., Matzuk M.M. Growth differentiation factor-9 is required during ovarian early folliculogenesis. Nature 1996, 383:531-535.
59. Ito M., Harada T., Tanikawa M., Fujii A., Shiota G., Terakawa N. Hepatocyte growth factor and stem cell factor involvement in paracrine interplays of theca and granulosa cells in the human ovary. Fertil Steril 2001, 75:973-979.
60. Erickson G.F., Case E. Epidermal growth factor antagonizes ovarian theca-interstitial cytodifferentiation. Mol Cell Endocrinol 1983, 31:71-76.
61. Erickson G.F., Magoffin D.A., Dyer C.A., Hofeditz C. The ovarian androgen producing cells: a review of structure/function relationships. Endocr Rev 1985, 6:371-399.
62. Magoffin D.A., Weitsman S.R. Insulin-like growth factor-l regulation of luteinizing hormone (LH) receptor messenger ribonucleic acid expression and LH-stimulated signal transduction in rat ovarian theca-interstitial cells. Biol Reprod 1994, 51:766-775.
63. Shima K., Kitayama S., Nakano R. Gonadotropin binding sites in human ovarian follicles and corpora lutea during the menstrual cycle. Obstet Gynecol 1987, 69:800-806.
64. Magoffin D.A., Weitsman S.R. Effect of insulin-like growth factor-1 on cholesterol side-chain cleavage cytochrome P450 mRNA expression in ovarian theca-interstitial cells stimulated to differentiate in vitro. Molec Cell Endocrinol 1993, 96:45-51.
65. Bergh C., Olsson J.H., Selleskog U., Hillensjo T. Steroid production in cultured thecal cell obtained from human ovarian follicles. Hum Reprod 1993, 8:519-524.
66. Jayaprakasan K., Hilwah N., Kendall N.R., Hopkisson J.F., Campbell B.K., Johnson I.R., et al. Does 3D ultrasound offer any advantage in the pretreatment assessment of ovarian reserve and prediction of outcome after assisted reproduction treatment?. Hum Reprod 2007, 22:1932-1941.
67. Beau I., Touraine P., Meduri G., Gougeon A., Desroches A., Matuchansky C., et al. A novel phenotype related to partial loss of function mutations of the follicle-stimulating hormone receptor. J Clin Invest 1998, 102:1-8.
68. Yokota H., Yamada K., Liu X., Kobayashi J., Abe Y., Mizunuma H., et al. Paradoxical action of activin A on folliculogenesis in immature and adult mice. Endocrinology 1997, 138:4572-4576.
69. Roy S.K. Epidermal growth factor and transforming growth factor-ß modulation of FSH-induced DNA synthesis in hamster preantral and early antral follicles. Biol Reprod 1993, 48:552-557.
70. Liu X., Andoh K., Abe Y., Kobayashi J., Yamada K., Mizunuma H., et al. A comparative study on transforming growth factor-beta and activin A for preantral follicles from adult, immature, and diethylstilbestrol-primed immature mice. Endocrinology 1999, 140:2480-2485.
71. Parrott J.A., Vigne J.L., Chu B.Z., Skinner M.K. Mesenchymal-epithelial interactions in the ovarian follicle involve keratinocyte and hepatocyte growth factor production by thecal cells and their action on granulosa cells. Endocrinology 1994, 135:569-575.
72. Hayashi M., McGee E.A., Min G., Klein C., Rose U.M., van Duin M., et al. Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 1999, 140:1236-1244.
73. Otsuka F., Yao Z., Lee T., Yamamoto S., Erickson G.F., Shimasaki S. Bone morphogenetic protein-15. Identification of target cells and biological functions. J Biol Chem 2000, 275:39523-39528.
74. Osuga Y., Koga K., Tsutsumi O., Yano T., Kugu K., Momoeda M., et al. Evidence for the presence of keratinocyte growth factor (KGF) in human ovarian follicles. Endocr J 2001, 48:161-166.
75. Abir R., Fisch B., Zhang X.Y., Felz C., Kessler-Icekson G., Krissi H., et al. Keratinocyte growth factor and its receptor in human ovaries from fetuses, girls and women. Mol Hum Reprod 2009, 15:69-75.
76. Osuga Y., Tsutsumi O., Momoeda M., Okagaki R., Matsumi H., Hiroi H., et al. Evidence for the presence of hepatocyte growth factor expression in human ovarian follicles. Mol Hum Reprod 1999, 5:703-707.
77. Ying S.Y. Inhibins, activins, and follistatins: gonadal proteins modulating the secretion of follicle-stimulating hormone. Endocr Rev 1988, 9:267-293.
78. Westergaard L.G., Andersen C.Y. Epidermal growth factor (EGF) in human preovulatory follicles. Hum Reprod 1989, 4:257-260.
79. Aaltonen J., Laitinen M.P., Vuojolainen K., Jaatinen R., Horelli-Kuitunen N., Seppa L., 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.
80. Palter S.F., Tavares A.B., Hourvitz A., Veldhuis J.D., Adashi E.Y. Are estrogens of import to primate/human ovarian folliculogenesis?. Endocr Rev 2001, 22:389-424.
81. Vendola K.A., Zhou J., Adesanya O.O., Weil S.J., Bondy C.A. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest 1998, 101:2622-2629.
82. Hild-Petito S., Brenner R.M., Stouffer R.L. Localization of androgen receptor in the follicle and corpus luteum of the primate ovary during the menstrual cycle. Biol Reprod 1991, 44:561-568.
83. Weil S., Vendola K., Zhou J., Bondy C.A. Androgen and follicle-stimulating hormone interactions in primate ovarian follicle development. J Clin Endocrinol Metab 1999, 84:2951-2956.
84. Shiina H., Matsumoto T., Sato T., Igarashi K., Miyamoto J., Takemasa S., et al. Premature ovarian failure in androgen receptor-deficient mice. Proc Natl Acad Sci U S A 2006, 103:224-229.
85. Hsueh A.J., McGee E.A., Hayashi M., Hsu S.Y. Hormonal regulation of early follicle development in the rat ovary. Mol Cell Endocrinol 2000, 163:95-100.
86. Nakamura M., Nakamura K., Igarashi S., Tano M., Miyamoto K., Ibuki Y., et al. Interaction between activin A and cAMP in the induction of FSH receptor in cultured rat granulosa cells. J Endocrinol 1995, 147:103-110.
87. Mizunuma H., Liu X., Andoh K., Abe Y., Kobayashi J., Yamada K., et al. Activin from secondary follicles causes small preantral follicles to remain dormant at the resting stage. Endocrinology 1999, 140:37-42.
88. Durlinger A.L., Gruijters M.J., Kramer P., Karels B., Kumar T.R., Matzuk M.M., et al. Anti-Müllerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology 2001, 142:4891-4899.
89. Weenen C., Laven J.S., Von Bergh A.R., Cranfield M., Groome N.P., Visser J.A., 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.
90. Sasano H., Okamoto M., Mason J.I., Simpson E.R., Mendelson C.R., Sasano N., et al. Immunolocalization of aromatase, 17α-hydroxylase and side-chain cleavage cytochrome P-450 in the human ovary. J Reprod Fertil 1989, 85:163-169.
91. Sasano H., Mori T., Sasano N., Nagura H., Mason J.I. Immunolocalization of 3ß-hydroxysteroid dehydrogenase in human ovary. J Reprod Fertil 1990, 89:743-751.
92. Tilly J.L., LaPolt P.S., Hsueh A.J.W. Hormonal regulation of follicle-stimulating hormone receptor messenger ribonucleic acid levels in cultured rat granulosa cells. Endocrinology 1992, 130:1296-1302.
93. Elvin J.A., Yan C., Matzuk M.M. Oocyte-expressed TGF-beta superfamily members in female fertility. Mol Cell Endocrinol 2000, 159:1-5.
94. Steinkampf M.P., Mendelson C.R., Simpson E.R. Effects of epidermal growth factor and insulin-like growth factor I on the levels of mRNA encoding aromatase cytochrome P-450 of human ovarian granulosa cells. Mol Cell Endocrinol 1988, 59:93-99.
95. Taniguchi F., Harada T., Deura I., Iwabe T., Tsukihara S., Terakawa N. Hepatocyte growth factor promotes cell proliferation and inhibits progesterone secretion via PKA and MAPK pathways in a human granulosa cell line. Mol Reprod Dev 2004, 68:335-344.
96. Monget P., Bondy C. Importance of the IGF system in early folliculogenesis. Mol Cell Endocrinol 2000, 163:89-93.
97. McNatty K.P., Hillier S.G., van den Boogaard A.M.J., Trimbos-Kemper T.C.M., Reichert L.E., van Hall E.V. Follicular development during the luteal phase of the human menstrual cycle. J Clin Endocrinol Metab 1983, 56:1022-1031.
98. Koering M.J. Cyclic changes in ovarian morphology during the menstrual cycle in Macaca mulatta. Am J Anat 1969, 126:73-101.
99. Pache T.D., Wladimiroff J.W., de Jong F.H., Hop W.C., Fauser B.C.J.M. Growth patterns of non dominant ovarian follicles during the normal menstrual cycle. Fertil Steril 1990, 54:638-642.
100. Gougeon A., Lefèvre B. Evolution of the diameters of the largest healthy and atretic follicles during the human menstrual cycle. J Reprod Fertil 1983, 69:497-502.
101. Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod 1986, 1:81-87.
102. Gougeon A., Testart J. Influence of human menopausal gonadotropin on the recruitment of human ovarian follicles. Fertil Steril 1990, 54:848-852.
103. Kumar T.R., Wiseman A.L., Kala G., Kala S.V., Matzuk M.M., Lieberman M.W. Reproductive defects in gamma-glutamyl transpeptidase-deficient mice. Endocrinology 2000, 141:4270-4277.
104. Mason H.D., Carr L., Leake R., Franks S. Production of transforming growth factor-alpha by normal and polycystic ovaries. J Clin Endocrinol Metab 1995, 80:2053-2056.
105. el-Roeiy A., Chen X., Roberts V.J., Shimasakai S., Ling N., LeRoith D., et al. Expression of the genes encoding the insulin-like growth factors (IGF-I and ll), the IGF and insulin receptors, and IGF-binding proteins 1-6 and the localization of their gene products in normal and polycystic ovary syndrome ovaries. J Clin Endocr Metab 1994, 78:1488-1496.
106. Mason H.D., Margara R., Winston R.M.L., Beard R.W., Reed M.J., Franks S. Inhibition of oestradiol production by epidermal growth factor in human granulosa cells of normal and polycystic ovaries. Clin Endocrinol 1990, 33:511-517.
107. Kwintkiewicz J., Giudice L.C. The interplay of insulin-like growth factors, gonadotropins, and endocrine disruptors in ovarian follicular development and function. Semin Reprod Med 2009, 27:43-51.
108. Nahum R., Thong K.J., Hillier S.G. Metabolic regulation of androgen production by human thecal cells in vitro. Hum Reprod 1995, 10:75-81.
109. Kobayashi M., Nakano R., Ooshima A. Immunocytochemical localization of pituitary gonadotrophins and gonadal steroids confirms the " two-cell, two-gonadotrophin" hypothesis of steroidogenesis in the human ovary. J Endocrinol 1990, 126:483-488.
110. Soules M.R., Steiner R.A., Clifton D.K., Cohen N.L., Aksel S., Bremner W.J. Progesterone modulation of pulsatile luteinizing hormone secretion in normal women. J Clin Endocrinol Metab 1984, 58:378-383.
111. Solovyeva E.V., Hayashi M., Margi K., Barkats C., Klein C., Amsterdam A., et al. Growth differentiation factor-9 stimulates rat theca-interstitial cell androgen biosynthesis. Biol Reprod 2000, 63:1214-1218.
112. Goodman A.L., Hodgen G.S. The ovarian triad of the primate menstrual cycle. Recent Prog Horm Res 1983, 39:1-73.
113. Macklon N.S., Fauser B.C. Follicle development during the normal menstrual cycle. Maturitas 1998, 30:181-188.
114. Klein N.A., Battaglia D.E., Fujimoto V.Y., Davis G.S., Bremner W.J., Soules M.R. Reproductive aging: accelerated ovarian follicular development associated with a monotropic follicle-stimulating hormone rise in normal older women. J Clin Endocrinol Metab 1996, 81:1038-1045.
115. McNatty K.P. Ovarian follicular development from the onset of luteal regression in humans and sheep. Follicular maturation and ovulation 1982, 1-18. Excerpta Medica, Amsterdam. R. Rolland, E.V. van Hall, S.G. Hillier, K.P. McNatty, J. Schoemaker (Eds.).
116. Mason H.D., Cwyfan-Hughes S., Holly J.M., Franks S. Potent inhibition of human ovarian steroidogenesis by insulin-like growth factor binding protein-4 (IGFBP-4). J Clin Endocrinol Metab 1998, 83:284-287.
117. Hourvitz A., Widger A.E., Filho F.L., Chang R.J., Adashi E.Y., Erickson G.F. Pregnancy-associated plasma protein-A gene expression in human ovaries is restricted to healthy follicles and corpora lutea. J Clin Endocrinol Metab 2000, 85:4916-4920.
118. Lawrence J.B., Oxvig C., Overgaard M.T., Sottrup-Jensen L., Gleich G.J., Hays L.G., et al. The insulin-like growth factor (IGF)-dependent IGF binding protein-4 protease secreted by human fibroblasts is pregnancy-associated plasma protein-A. Proc Natl Acad Sci U S A 1999, 96:3149-3153.
119. Baker J., Hardy M.P., Zhou J., Bondy C., Lupu F., Bellvé A., et al. Effect of an igf1 gene null mutation on mouse reproduction. Mol Endocrinol 1996, 10:903-918.
120. Matzuk M.M., Dionne L., Guo Q., Kumar T.R., Lebovitz R.M. Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology 1998, 139:4008-4011.
121. Amsterdam A., Rotmensch S. Structure-function relationships during granulosa cell differentiation. Endocr Rev 1987, 8:309-337.
122. Hillier S.G., Yong E.L., Illingworth P.J., Baird D.T., Schwall R.H., Mason A.J. Effect of recombinant inhibin on androgen synthesis in cultured human thecal cells. Mol Cell Endocrinol 1991, 75:R1-R6.
123. Roberts V.J., Barth S., El-Roeiy A., Yen S.S.C. Expression of inhibin/activin subunits and follistatin messenger ribonucleic acids and proteins in ovarian follicles and the corpus luteum during the human menstrual cycle. J Clin Endocrinol Metab 1993, 77:1402-1410.
124. Hernandez E.R., Hurwitz A., Vera A., Pellicer A., Adashi E.Y., LeRoith D., et al. Expression of the genes encoding the insulin-like growth factors and their receptors in the human ovary. J Clin Endocrinol Metab 1992, 74:419-425.
125. Gougeon A. Steroid 3ß-ol-dehydrogenase activity in the largest healthy and atretic follicles in the human ovary during the menstrual cycle. Ann Biol Anim Biochim Biophys 1977, 17:1087-1094.
126. Filicori M., Cognigni G.E., Taraborrelli S., Spettoli D., Ciampaglia W., Tabarelli De Fatis C., et al. Luteinizing hormone activity in menotropins optimizes folliculogenesis and treatment in controlled ovarian stimulation. J Clin Endocrinol Metab 2001, 86:337-343.
127. Zeleznik A.J., Schuler H.M., Reichert L.E. Gonadotropin-binding sites in the rhesus monkey ovary: role of the vasculature in the selective distribution of human chorionic gonadotropin to the preovulatory follicle. Endocrinology 1981, 109:356-362.
128. Wulff C., Wiegand S.J., Saunders P.T., Scobie G.A., Fraser H.M. Angiogenesis during follicular development in the primate and its inhibition by treatment with truncated Flt-1-Fc (vascular endothelial growth factor Trap[A40]). Endocrinology 2001, 142:3244-3254.
129. Chaffkin L.M., Luciano A.A., Peluso J.J. Progesterone as an autocrine/paracrine regulator of human granulosa cell proliferation. J Clin Endocrinol Metab 1992, 75:1404-1408.
130. Hernandez-Gonzalez I., Gonzalez-Robayna I., Shimada M., Wayne C.M., Ochsner S.A., White L., et al. Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: does this expand their role in the ovulation process?. Mol Endocrinol 2006, 20:1300-1321.
131. Edson M.A., Nagaraja A.K., Matzuk M.M. The mammalian ovary from genesis to revelation. Endocr Rev 2009, 30:624-712.
132. Freimann S., Ben-Ami I., Dantes A., Ron-El R., Amsterdam A. EGF-like factor epiregulin and amphiregulin expression is regulated by gonadotropins/cAMP in human ovarian follicular cells. Biochem Biophys Res Commun 2004, 324:829-834.
133. Park J.Y., Su Y.Q., Ariga M., Law E., Jin S.L., Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 2004, 303:682-684.
134. Hizaki H., Segi E., Sugimoto Y., Hirose M., Saji T., Ushikubi F., et al. Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proc Natl Acad Sci U S A 1999, 96:10501-10506.
135. Gueripel X., Brun V., Gougeon A. Oocyte bone morphogenetic protein 15, but not growth differentiation factor 9, is increased during gonadotropin-induced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol Reprod 2006, 75:836-843.
136. Assou S., Anahory T., Pantesco V., Le Carrour T., Pellestor F., Klein B., et al. The human cumulus - oocyte complex gene-expression profile. Hum Reprod 2006, 21:1705-1719.
137. Brailly S., Gougeon A., Milgrom E., Bomsel Helmreich O., Papiernik E. Androgens and progestins in the human ovarian follicle: differences in the evolution of preovulatory, healthy nonovulatory, and atretic follicles. J Clin Endocrinol Metab 1981, 53:128-134.
138. Westergaard L. Follicular atresia in relation to oocyte morphology in non-pregnant and pregnant women. J Reprod Fertil 1985, 74:113-118.
139. Westergaard L.G., McNatty K.P., Christensen I.J. Steroid concentrations in fluid from human ovarian antral follicles during pregnancy. J Endocrinol 1985, 107:133-136.