How to make a good oocyte: An update on in-vitro models to study follicle regulation

Human Reproduction Update

Volumn 9, Issue 6, 2003, Pages 541-555

  Thomas, Fiona H ^a   Walters, Kirsty A ^a   Telfer, Evelyn E ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Follicle development; In vitro culture; Oocyte development; Oocyte maturation

Indexed keywords

AUTOCRINE EFFECT; BIOLOGICAL MODEL; CELL MATURATION; CELL VIABILITY; CULTURE TECHNIQUE; DOMESTIC ANIMAL; FEMALE INFERTILITY; FERTILIZATION IN VITRO; HUMAN; IN VITRO STUDY; ISOLATION PROCEDURE; MEDICAL TECHNOLOGY; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; PARACRINE SIGNALING; PATIENT MONITORING; PREMATURE OVARIAN FAILURE; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; SOMATIC CELL; SPECIES DIFFERENCE;

ANIMALS; CELL AGING; EXTRACELLULAR MATRIX; FEMALE; GONADOTROPINS; GROWTH SUBSTANCES; HUMANS; OOCYTES; OVARIAN FOLLICLE; SOMATOMEDINS; TISSUE SURVIVAL; TRANSFORMING GROWTH FACTOR BETA;

EID: 0347287034     PISSN: 13554786     EISSN: None     Source Type: Journal    
DOI: 10.1093/humupd/dmg042     Document Type: Review

References (200)

1. Abir, R., Franks, S., Mobberley, M.A., Moore, P.A., Margara, R.A. and Winston, R.M. (1997) Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertil. Steril., 68, 682-688.
2. Adashi, E.Y., Resnick, C.E., Payne, D.W., Rosenfeld, R.G., Matsumoto, T., Hunter, M.K., Gargosky, S.E., Zhou, J. and Bondy, C.A. (1997) The mouse intraovarian insulin-like growth factor I system: departures from the rat paradigm. Endocrinology, 138, 3881-3890.
3. Alak, B.M., Coskun, S., Friedman, C.I., Kennard, E.A., Kim, M.H. and Seifer, D.B. (1998) Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro. Feril. Steril., 70, 1126-1130.
4. Albertini, D.F., Combelles, C.M., Benecchi, E. and Carabatsos, M.J. (2001) Cellular basis for paracrine regulation of ovarian follicle development. Reproduction, 121, 647-653.
5. Amsterdam, A., May, J.V. and Schomberg, D.W. (1988) Synergistic effect of insulin and follicle-stimulating hormone on biochemical and morphological differentiation of porcine granulosa cells in vitro. Biol. Reprod., 39, 379-390.
6. Anderson, E. and Albertini, D.F. (1976) Gap junctions between the oocyte and companion follicle cells in mammalian ovary. J. Cell Biol., 71, 680-686.
7. Armstrong, D.G. and Webb, R. (1997) Ovarian follicular dominance: the role of intraovarian growth factors and novel proteins. Rev. Reprod., 2, 139-146.
8. Armstrong, D.G., Baxter, G., Gutierrez, C.G., Hogg, C.O., Glazyrin, A.L., Campbell, B.K., Bramley, T.A. and Webb, R. (1998) Insulin-like growth factor binding protein-2 and -4 messenger ribonucleic acid expression in bovine ovarian follicles: effect of gonadotropins and developmental status. Endocrinology, 139, 2146-2154.
9. Armstrong, D.G., Gutierrez, C.G., Baxter, G., Glazyrin, A.L., Mann, G.E., Woad, K.J., Hogg, C.O. and Webb, R. (2000) Expression of mRNA encoding IGF-I, IGF-II and type 1 IGF receptor in bovine ovarian follicles. J. Endocrinol., 165, 101-113.
10. Armstrong, D.G., McEvoy, T.G., Baxter, G., Robinson, J.J., Hogg, C.O., Woad, K.J., Webb, R. and Sinclair, K.D. (2001) Effect of dietary energy and protein on bovine follicular dynamics and embryo production in vitro: associations with the ovarian insulin-like growth factor system. Biol. Reprod., 64, 1624-1632.
11. Armstrong, D.G., Baxter, G., Hogg, C.O. and Woad, K.J. (2002) Insulin-like growth factor (IGF) system in the oocyte and somatic cells of bovine preantral follicles. Reproduction, 123, 789-797.
12. Awotwi, E.K., Keeney, D.S., Hard, D.L. and Anderson, L.L. (1984) Effects of pulsatile infusion of luteinizing hormone-releasing hormone on luteinizing hormone secretion and ovarian function in hypophysial stalk-transected beef heifers. Biol. Reprod., 31, 989-999.
13. Baarends, W.M., Uilenbroek, J.T., Kramer, P., Hoogerbrugge, J.W., van Leeuwen, E.C., Themmen, A.P. and Grootegoed, J.A. (1995) Anti-mullerian hormone and anti-mullerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology, 136, 4951-4962.
14. Baker, J., Hardy, M.P., Zhou, J., Bondy, C., Lupu, F., Bellve, A.R. and Efstratiadis, A. (1996) Effects of an Igf1 gene null mutation on mouse reproduction. Mol. Endocrinol., 10, 903-918.
15. Baker, S.J., Srsen, V., Lapping, R. and Spears, N. (2001) Combined effect of follicle-follicle interactions and declining follicle-stimulating hormone on murine follicle health in vitro. Biol. Reprod., 65, 1304-1310.
16. Bao, B. and Garverick, H.A. (1998) Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review. J. Anim. Sci., 76, 1903-1921.
17. Bergh, C., Olsson, J.H. and Hillensjo, T. (1991) Effect of insulin-like growth factor I on steroidogenesis in cultured human granulosa cells. Acta Endocrinol. (Copenh.), 125, 177-185.
18. Besmer, P., Manova, K., Duttlinger, R., Huang, E.J., Packer, A., Gyssler, C. and Bachvarova, R.F. (1993) The kit-ligand (steel factor) and its receptor c-kit/W: pleiotropic roles in gametogenesis and melanogenesis. Development (Suppl.), 125-137.
19. Billig, H., Furuta, I. and Hsueh, A.J. (1993) Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology, 133, 2204-2212.
20. Billig, H., Furuta, I. and Hsueh, A.J. (1994) Gonadotropin-releasing hormone directly induces apoptotic cell death in the rat ovary: biochemical and in situ detection of deoxyribonucleic acid fragmentation in granulosa cells. Endocrinology, 134, 245-252.
21. Bodensteiner, K.J., Clay, C.M., Moeller, C.L. and Sawyer, H.R. (1999) Molecular cloning of the ovine Growth/Differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol. Reprod., 60, 381-386.
22. Boland, N.I., Humpherson, P.G., Leese, H.J. and Gosden, R.G. (1993) Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro. Biol. Reprod., 48, 798-806.
23. Braw-Tal, R. and Yossefi, S. (1997) Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J. Reprod. Fertil., 109, 165-171.
24. Buccione, R., Schroeder, A.C. and Eppig, J.J. (1990) Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol. Reprod., 43, 543-547.
25. Cameron, V.A., Nishimura, E., Mathews, L.S., Lewis, K.A., Sawchenko, P.E. and Vale, W.W. (1994) Hybridization histochemical localization of activin receptor subtypes in rat brain, pituitary, ovary, and testis. Endocrinology, 134, 799-808.
26. Campbell, B.K., Scaramuzzi, R.J. and Webb, R. (1996) Induction and maintenance of oestradiol and immunoreactive inhibin production with FSH by ovine granulosa cells cultured in serum-free media. J. Reprod Fertil., 106, 7-16.
27. Cecconi, S., Barboni, B., Coccia, M. and Mattioli, M. (1999) In vitro development of sheep preantral follicles. Biol. Reprod., 60, 594-601.
28. Chun, S.Y., Billig, H., Tilly, J.L., Furuta, I., Tsafriri, A. and Hsueh, A.J. (1994) Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor I. Endocrinology, 35, 1845-1853.
29. Clark, D.E., Tisdall, D.J., Fidler, A.E. and McNatty, K.P. (1996) Localization of mRNA encoding c-kit during the initiation of folliculogenesis in ovine fetal ovaries. J. Reprod. Fertil., 106, 329-335.
30. Colonna, R., Cecconi, S., Tatone, C., Mangia, F. and Buccione, R. (1989) Somatic cell-oocyte interactions in mouse oogenesis: stage-specific regulation of the mouse oocytye protein phosphorylation by granulosa cells. Dev. Biol., 133, 305-308.
31. Cortvrindt, R. and Smitz, J. (2001) In vitro follicle growth: achievements in mammalian species. Reprod. Domest. Anim., 36, 3-9.
32. Cortvrindt, R., Smitz, J. and Van Steirteghem, A.C. (1996) A morphological and functional study of the effect of slow freezing followed by complete in-vitro maturation of primary mouse ovarian follicles. Hum. Reprod., 11, 2648-2655.
33. CwyfanHughes, S.C., Mason, H.D., Franks, S. and Holly, J.M.P. (1997) Modulation of the insulin-like growth factor binding proteins by follicle size in the human ovary. J. Endocrinol., 154, 35-43.
34. Dale, L. and Wardle, F.C. (1999) A gradient of BMP activity specifies dorsal-ventral fates in early Xenopus embryos. Semin. Cell Dev. Biol., 10, 319-326.
35. Danforth, D.R., Arbogast, L.K., Ghosh, S., Dickerman, A., Rofagha, R., Friedman, C.I. (2003) Vascular endothelial growth factor stimulates preantral follicle growth in the rat ovary. Biol. Reprod., 68, 1736-1741.
36. Dong, J., Albertini, D.F., Nishimori, K., Kumar, T.R., Lu, N. and Matzuk, M.M. (1996) Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature, 383, 531-535.
37. Dube, J.L., Wang, P., Elvin, J., Lyons, K.M., Celeste, A.J. and Matzuk, M.M. (1998) The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol., 12, 1809-1817.
38. Dufour, J., Cahill, L.P. and Mauleon, P. (1979) Short- and long-term effects of hypophysectomy and unilateral ovariectomy on ovarian follicular populations in sheep. J. Reprod. Fertil., 57, 301-309.
39. Durlinger, A.L., Kramer, P., Karels, B., de Jong, F.H., Uilenbroek, J.T., Grootegoed, J.A. and Themmen, A.P. (1999) Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology, 140, 5789-5796.
40. Durlinger, A.L., Gruijters, M.J., Kramer, P., Karels, B., Ingraham, H.A., Nachtigal, M.W., Uilenbroek, J.T., Grootegoed, J.A. and Themmen, A.P. (2002) Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 143, 1076-1084.
41. Eckert, J. and Niemann, H. (1998) mRNA expression of leukaemia inhibitory factor (LIF) and its receptor subunits glycoprotein 130 and LIF-receptor-beta in bovine embryos derived in vitro or in vivo. Mol. Hum. Reprod., 4, 957-965.
42. Eckery, D.C., Moeller, C.L., Nett, T.M. and Sawyer, H.R. (1997) Localization and quantification of binding sites for follicle-stimulating hormone, luteinizing hormone, growth hormone, and insulin-like growth factor I in sheep ovarian follicles. Biol. Reprod., 57, 507-513.
43. Elvin, J.A., Yan, C., Wang, P., Nishimori, K. and Matzuk, M.M. (1999) Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol. Endocrinol., 13, 1018-1034.
44. Eppig, J.J. (1994) Further reflections on culture systems for the growth of oocytes in vitro. Hum. Reprod. 9, 974-976.
45. Eppig, J.J. and O'Brien, M.J. (1996) Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod., 54, 197-207.
46. Eppig, J.J. and Schroeder, A.C. (1989) Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol. Reprod., 41, 268-276.
47. Eppig, J.J. and Telfer, E.E. (1993) Isolation and culture of oocytes. Methods Enzymol., 225, 77-84.
48. Eppig, J.J., Peters, A.H., Telfer, E.E. and Wigglesworth, K. (1993) Production of cumulus expansion enabling factor by mouse oocytes grown in vitro: preliminary characterization of the factor. Mol. Reprod. Dev., 34, 450-456.
49. Eppig, J.J., O'Brien, M.J., Pendola, F.L. and Watanabe, S. (1998) Factors affecting the developmental competence of mouse oocytes grown in vitro: follicle-stimulating hormone and insulin. Biol. Reprod., 59, 1445-1453.
50. Erickson, B.H. (1966) Development and senescence of the postnatal bovine ovary. J. Anim. Sci., 25, 800-805.
51. Findlay, J.K. (1993) An update on the roles of inhibin, activin, and follistatin as local regulators of folliculogenesis. Biol. Reprod., 48, 15-23.
52. Findlay, J.K., Drummond, A.E., Dyson, M., Baillie, A.J., Robertson, D.M. and Ethier, J.F. (2001) Production and actions of inhibin and activin during folliculogenesis in the rat. Mol. Cell. Endocrinol., 180, 139-144.
53. Francis, G.L., Ross, M., Ballard, F.J., Milner, S.J., Senn, C., McNeil, K.A., Wallace, J.C., King, R. and Wells, J.R. (1992) Novel recombinant fusion protein analogues of insulin-like growth factor (IGF)-I indicate the relative importance of IGF-binding protein and receptor binding for enhanced biological potency. J. Mol. Endocrinol., 8, 213-223.
54. Galloway, S.M., McNatty, K.P., Cambridge, L.M., Laitinen, M.P., Juengel, J.L., Jokiranta, T.S., McLaren, R.J., Luiro, K., Dodds, K.G., Montgomery, G.W. et al. (2000) Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nature Genet., 25, 279-283.
55. Giudice, L.C. (1992) Insulin-like growth factors and ovarian follicular development. Endocr. Rev., 13, 641-669.
56. Gomez, E., Tarin, J.J. and Pellicer, A. (1993) Oocyte maturation in humans: the role of gonadotropins and growth factors. Fertil. Steril., 60, 40-46.
57. Gong, J.G., Campbell, B.K., Bramley, T.A., Gutierrez, C.G., Peters, A.R. and Webb, R. (1996) Suppression in the secretion of follicle-stimulating hormone and luteinizing hormone, and ovarian follicle development in heifers continuously infused with a gonadotropin-releasing hormone agonist. Biol. Reprod., 55, 68-74.
58. Gore-Langton, R.E. and Daniel, S.A. (1990) Follicle-stimulating hormone and estradiol regulate antrum-like reorganization of granulosa cells in rat preantral follicle cultures. Biol. Reprod., 43, 65-72.
59. Gosden, R.G. and Telfer, E. (1987a) Scaling of follicular sizes in mammalian ovaries. J. Zool., 211, 157-168.
60. Gosden, R.G. and Telfer, E. (1987b) Numbers of folicles and oocytes in mammalian ovaries and their allometric relationships. J. Zool., 211, 169-175.
61. Gosden, R.G., Baird, D.T., Wade, J.C. and Webb, R. (1994) Restoration of fertility to oophorectomized sheep by ovarian autografts stored at -196 degrees C. Hum. Reprod, 9, 597-603.
62. Gougeon, A. and Busso, D. (2000) Morphologic and functional determinants of primordial and primary follicles in the monkey ovary. Mol. Cell. Endocrinol., 163, 33-42.
63. Gutierrez, C.G., Campbell, B.K., Armstrong, D.G. and Webb, R. (1997a) Insulin-like growth factor-I (IGF-I) production by bovine granulosa cells in vitro and peripheral IGF-I measurement in cattle serum: an evaluation of IGF-binding protein extraction protocols. J. Endocrinol., 153, 231-240.
64. Gutierrez, C.G., Campbell, B.K. and Webb, R. (1997b) Development of a long-term bovine granulosa cell culture system: induction and maintenance of estradiol production, response to follicle-stimulating hormone, and morphological characteristics. Biol. Reprod., 56, 608-616.
65. Gutierrez, C.G., Ralph, J.H., Telfer, E.E., Wilmut, I. and Webb, R. (2000) Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod., 62, 1322-1328.
66. Hakuno, N., Koji, T., Yano, T., Kobayashi, N., Tsutsumi, O., Taketani, Y. and Nakane, P.K. (1996) Fas/APO-1/CD95 system as a mediator of granulosa cell apoptosis in ovarian follicle atresia. Endocrinology, 137, 1938-1948.
67. Hayashi, M., McGee, E.A., Min, G., Klein, C., Rose, U.M., van Duin, M. and Hsueh, A.J. (1999) Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology, 140, 1236-1244.
68. Hayes, S.A., Zarnegar, M., Sharma, M., Yang, F., Peehl, D.M., ten Dijke, P. and Sun, Z. (2001) SMAD3 represses androgen receptor-mediated transcription. Cancer Res., 61, 2112-2118.
69. Heldin, C.H., Miyazono, K. and ten Dijke, P. (1997) TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature, 390, 465-471.
70. Himeno, N., Kawamura, N., Okamura, H., Mori, T., Fukumoto, M. and Midorikawa, O. (1984) [Collagen synthetic activity in rabbit ovary during ovulation and its blockage by indomethacin.] Nippon Sanka Fujinka Gakkai Zasshi, 36, 1930-1934.
71. Hirao, Y., Nagai, T., Kubo, M., Miyano, T., Miyake, M. and Kato, S. (1994) In vitro growth and maturation of pig oocytes. J. Reprod. Fertil., 100, 333-339.
72. Hirobe, S., He, W.W., Lee, M.M. and Donahoe, P.K. (1992) Mullerian inhibiting substance messenger ribonucleic acid expression in granulosa and Sertoli cells coincides with their mitotic activity. Endocrinology, 131, 854-862.
73. Hirshfield, A.N. (1991) Development of follicles in the mammalian ovary. Int. Rev. Cytol., 124, 43-101.
74. Hovatta, O., Silye, R., Abir, R., Krausz, T. and Winston, R.M. (1997) Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum. Reprod., 12, 1032-1036.
75. Hovatta, O., Wright, C., Krausz, T., Hardy, K. and Winston, R.M. (1999) Human primordial, primary and secondary ovarian follicles in long-term culture: effect of partial isolation. Hum. Reprod., 14, 2519-2524.
76. Hreinsson, J.G., Scott, J.E., Rasmussen, C., Swahn, M.L., Hsueh, A.J. and Hovatta, O. (2002) Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J. Clin. Endocrinol. Metab., 87, 316-321.
77. Huang, E.J., Manova, K., Packer, A.I., Sanchez, S., Bachvarova, R.F. and Besmer, P. (1993) The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Dev. Biol., 157, 100-109.
78. Huet, C., Pisselet, C., Mandon-Pepin, B., Monget, P. and Monniaux, D. (2001) Extracellular matrix regulates ovine granulosa cell survival, proliferation and steroidogenesis: relationships between cell shape and function. J. Endocrinol., 169, 347-360.
79. Hughes, F.M. Jr and Gorospe, W.C. (1991) Biochemical identification of apoptosis (programmed cell death) in granulosa. cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology, 129, 2415-2422.
80. Hulshof, S., Figueiredo, J., Beckers, J., Bevers, M., Van der Donk, J. and Van den Hurk, R. (1995) Effect of recombinant FSH, 17beta-oestradiol and their combination on bovine preantral follicles in vitro. Theriogenology, 44, 217-226.
81. Hulshof, S., Figueiredo, J., Beckers, J., Bevers, M., Vanderstichele, H. and Van den Hurk, R. (1997) Bovine preantral follicles and activin:Immunohistochemistry for activin and activin receptor and the effect of bovine activin in vitro. Theriogenology 48, 133-142.
82. Itoh, T., Kacchi, M., Abe, H., Sendai, Y. and Hoshi, H. (2002) Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biol. Reprod., 67, 1099-1105.
83. Joyce, I.M., Clark, A.T., Pendola, F.L. and Eppig, J.J. (2000) Comparison of recombinant growth differentiation factor-9 and oocyte regulation of KIT ligand messenger ribonucleic acid expression in mouse ovarian follicles. Biol. Reprod., 63, 1669-1675.
84. Juneja, S.C., Barr, K.J., Enders, G.C. and Kidder, G.M. (1999) Defects in the germ line and gonads of mice lacking connexin43. Biol. Reprod., 60, 1263-1270.
85. Kaipia, A., Chun, S.Y., Eisenhauer, K. and Hsueh, A.J. (1996) Tumor necrosis factor-alpha and its second messenger, ceramide, stimulate apoptosis in cultured ovarian follicles. Endocrinology, 137, 4864-4870.
86. Kaipia, A. and Hsueh, A.J. (1997) Regulation of ovarian follicle atresia. Annu. Rev. Physiol., 59, 349-363.
87. Kerr, J.F., Wyllie, A.H. and Currie, A.R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer, 26, 239-257.
88. Klinger, F.G. and De Felici, M. (2002) In vitro development of growing oocytes from fetal mouse oocytes: stage-specific regulation by stem cell factor and granulosa cells. Dev. Biol., 244, 85-95.
89. Knight, P.G. and Glister, C. (2001) Potential local regulatory functions of inhibins, activins and follistatin in the ovary. Reproduction, 121, 503-512.
90. Langhout, D.J., Spicer, L.J. and Geisert, R.D. (1991) Development of a culture system for bovine granulosa cells: effects of growth hormone, estradiol, and gonadotropins on cell proliferation, steroidogenesis, and protein synthesis. J. Anim. Sci., 69, 3321-3334.
91. Leeuwenberg, B.R., Hurst, P.R. and McNatty, K.P. (1995) Expression of IGF-I mRNA in the ovine ovary. J. Mol. Endocrinol., 15, 251-258.
92. Liu, H.C., He, Z. and Rosenwaks, Z. (2002) In vitro culture and in vitro maturation of mouse preantral follicles with recombinant gonadotropins. Fertil. Steril., 77, 373-383.
93. Liu, X., Andoh, K., Yokota, H., Kobayashi, J., Abe, Y., Yamada, K., Mizunuma, H. and Ibuki, Y. (1998) Effects of growth hormone, activin, and follistatin on the development of preantral follicle from immature female mice. Endocrinology, 139, 2342-2347.
94. Liu, X., Andoh, K., Abe, Y., Kobayashi, J., Yamada, K., Mizunuma, H. and Ibuki, Y. (1999) A comparative study on transforming growth factor-beta and activin A for preantral follicles from adult, immature, and diethylstilbestrol-primed immature mice. Endocrinology, 140, 2480-2485.
95. Luck, M.R., Jeyaseelan, I. and Scholes, R.A. (1995) Ascorbic acid and fertility. Biol. Reprod., 52, 262-266.
96. Luck, M.R. and Zhao, Y. (1993) Identification and measurement of collagen in the bovine corpus luteum and its relationship with ascorbic acid and tissue development. J. Reprod. Fertil., 99, 647-652.
97. Lussier, J.G., Matton, P. and Dufour, J.J. (1987) Growth rates of follicles in the ovary of the cow. J. Reprod. Fertil., 81, 301-307.
98. Manova, K., Huang, E.J., Angeles, M., De Leon, V., Sanchez, S., Pronovost, S.M., Besmer, P. and Bachvarova, R.F. (1993) The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in the oocyte growth and in proliferation of spermatogonia. Dev. Biol., 157, 85-99.
99. Markstrom, E., Svensson, E.C., Shao, R., Svanberg, B. and Billig, H. (2002) Survival factors regulating ovarian apoptosis - dependence on follicle differentiation. Reproduction, 123, 23-30.
100. Martimbeau, S. and Tilly, J.L. (1997) Physiological cell death in endocrine-dependent tissues: an ovarian perspective. Clin. Endocrinol. (Oxf.), 46, 241-254.
101. Martinovitch, P.N. (1938) The development in vitro of the mammalian gonad. Ovary and oogenesis. Proc. R. Soc. Lond., B125, 232-249.
102. Mason, H.D., Cwyfan-Hughes, S.C., Heinrich, G., Franks, S. and Holly, J.M.P. (1996) Insulin-like growth factor (IGF) I and II, IGF-binding proteins, and IGF-binding protein proteases are produced by theca and stroma of normal and polycystic human ovaries. J. Clin. Endocrinol. Metab., 81, 276-284.
103. Mason, H.D., Willis, D., Holly, J.M., Cwyfan-Hughes, S.C., Seppala, M. and Franks, S. (1992) Inhibitory effect of insulin-like growth factor-binding proteins on steroidogenesis by human granulosa cells in culture. Mol. Cell. Endocrinol., 89, 1-4.
104. Mather, J.P., Moore, A. and Li, R.H. (1997) Activins, inhibins, and follistatins: further thoughts on a growing family of regulators. Proc. Soc. Exp. Biol. Med., 215, 209-222.
105. Matzuk, M.M. and Lamb, D.J. (2002) Genetic dissection of mammalian fertility pathways. Nat. Cell. Biol., 4 (Suppl.), s41-49.
106. May, J.V. and Schomberg, D.W. (1981) Granulosa cell differentiation in vitro: effect of insulin on growth and functional integrity. Biol. Reprod., 25, 421-431.
107. McCaffery, F.H. (2001) The development of bovine preantral follicles in vitro. PhD thesis, University of Edinburgh.
108. McCaffery, F.H., Leask, R., Riley, S.C. and Telfer, E.E. (2000) Culture of bovine preantral follicles in a serum-free system: markers for assessment of growth and development. Biol. Reprod., 63, 267-273.
109. McCaffery, F.H., Campbell, B.K. and Telfer, E.E. (2001) The effect of IGF-I on the development of bovine preantral follicles in vitro. Biol. Reprod., 64 (Suppl. 1), Abstract 9.
110. McGee, E.A. (2000) The regulation of apoptosis in preantral ovarian follicles. Biol. Signals Recept., 9, 81-86.
111. McGee, E.A., Smith, R., Spears, N., Nachtigal, M.W., Ingraham, H. and Hsueh, A.J. (2001) Mullerian inhibitory substance induces growth of rat preantral ovarian follicles. Biol. Reprod., 64, 293-298.
112. McGrath, S.A., Esquela, A.F. and Lee, S.J. (1995) Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol., 9, 131-136.
113. McNatty, K.P., Heath, D.A., Lundy, T., Fidler, A.E., Quirke, L., O'Connell, A., Smith, P., Groome, N. and Tisdall, D.J. (1999) Control of early ovarian follicular development. J. Reprod. Fertil., 54 (Suppl.), 3-16.
114. Mizunuma, H., Liu, X., Andoh, K., Abe, Y., Kobayashi, J., Yamada, K., Yokota, H., Ibuki, Y. and Hasegawa, Y. (1999) Activin from secondary follicles causes small preantral follicles to remain dormant at the resting stage. Endocrinology, 140, 37-42.
115. Moley, K.H. and Schreiber, J.R. (1995) Ovarian follicular growth, ovulation and atresia. Endocrine, paracrine and autocrine regulation. Adv. Exp. Med. Biol., 377, 103-119.
116. Monget, P. and Bondy, C. (2000) Importance of the IGF system in early folliculogenesis. Mol. Cell. Endocrinol., 163, 89-93.
117. Monniaux, D. and de Reviers, M.M. (1989) Quantitative autoradiographic study of FSH binding sites in prepubertal ovaries of three strains of rats. J. Reprod. Fertil., 85, 151-162.
118. Morbeck, D.E., Flowers, W.L. and Britt, J.H. (1993) Response of porcine granulosa cells isolated from primary and secondary follicles to FSH, 8-bromo-cAMP and epidermal growth factor in vitro. J. Reprod. Fertil., 99, 577-584.
119. Morita, Y. and Tilly, J.L. (1999) Oocyte apoptosis: like sand through an hourglass. Dev. Biol., 213, 1-17.
120. Motro, B. and Bernstein, A. (1993) Dynamic changes in ovarian c-kit and Steel expression during the estrous reproductive cycle. Dev. Dyn., 197, 69-79.
121. Motta, P.M., Makabe, S., Naguro, T. and Correr, S. (1994) Oocyte follicle cells association during development of human ovarian follicle. A study by high resolution scanning and transmission electron microscopy. Arch. Histol. Cytol., 57, 369-394.
122. Murray, A.A., Gosden, R.G., Allison, V. and Spears, N. (1998) Effect of androgens on the development of mouse follicles growing in vitro. J. Reprod. Fertil., 113, 27-33.
123. Murray, A.A., Molinek, M.D., Baker, S.J., Kojima, F.N., Smith, M.F., Hillier, S.G. and Spears, N. (2001) Role of ascorbic acid in promoting follicle integrity and survival in intact mouse ovarian follicles in vitro. Reproduction, 121, 89-96.
124. Nayudu, P.L. and Osborn, S.M. (1992) Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. J. Reprod. Fertil., 95, 349-362.
125. Nayudu, P.L., Fehrenbach, A., Kiesel, P., Vitt, U.A., Pancharatna, K. and Osborn, S. (2001) Progress toward understanding follicle development in vitro: appearances are not deceiving. Arch. Med. Res., 32, 587-594.
126. Newton, H., Picton, H. and Gosden, R.G. (1999) In vitro growth of oocyte-granulosa cell complexes isolated from cryopreserved ovine tissue. J. Reprod. Fertil., 115, 141-150.
127. Nilsson, E.E., Kezele, P. and Skinner, M.K. (2002) Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol. Cell. Endocrinol., 188, 65-73.
128. Nuttinck, F., Collette, L., Massip, A. and Dessy, F. (1996) Histologic and autoradiographic study of the in vitro effects of FGF-2 and FSH on isolated bovine preantral follicles: preliminary investigation. Theriogenology, 45, 1235-1245.
129. Obata, Y., Kono, T. and Hatada, I. (2002) Maturation of mouse fetal germ cells in vitro. Nature, 418, 497-498.
130. O'Brien, M.J., Pendola, J.K. and Eppig, J.J. (2003) A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod., 68, 1682-1686.
131. Olsson, J.H., Carlsson, B. and Hillensjo, T. (1990) Effect of insulin-like growth factor I on deoxyribonucleic acid synthesis in cultured human granulosa cells. Fertil. Steril., 54, 1052-1057.
132. Otsuka, F., Yao, Z., Lee, T., Yamamoto, S., Erickson, G.F. and Shimasaki, S. (2000) Bone morphogenetic protein-15. Identification of target cells and biological functions. J. Biol. Chem., 275, 39523-39528.
133. Packer, A.I., Hsu, Y.C., Besmer, P. and Bachvarova, R.F. (1994) The ligand of the c-kit receptor promotes oocyte growth. Dev. Biol., 161, 194-205.
134. Padh, H. (1991) Vitamin C: newer insights into its biochemical functions. Nutr. Rev., 49, 65-70.
135. Parrott, J.A. and Skinner, M.K. (1999) Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology, 140, 4262-4271.
136. Pawshe, C.H., Rao, K.B. and Totey, S.M. (1998) Effect of insulin-like growth factor I and its interaction with gonadotropins on in vitro maturation and embryonic development, cell proliferation, and biosynthetic activity of cumulus-oocyte complexes and granulosa cells in buffalo. Mol. Reprod. Dev., 49, 277-285.
137. Peluso, J.J., Luciano, A.M., Pappalardo, A. and White, B.A. (1995) Cellular and molecular mechanisms that mediate insulin-dependent rat granulosa cell mitosis. Biol. Reprod., 52, 124-130.
138. Pfeffer, F., Casanueva, E., Kamar, J., Guerra, A., Perichart, O. and Vadillo-Ortega, F. (1998) Modulation of 72-kilodalton type IV collagenase (matrix metalloproteinase-2) by ascorbic acid in cultured human amnion-derived cells. Biol. Reprod., 59, 326-329.
139. Pinnell, S.R. (1985) Regulation of collagen biosynthesis by ascorbic acid: a review. Yale J. Biol. Med., 58, 553-559.
140. Poretsky, L., Cataldo, N.A., Rosenwaks, Z. and Guidice, L.C. (1999) The insulin-related ovarian regulatory system in health and disease. Endocr. Rev., 20, 535-582.
141. Prochazka, P., Mbaye, A., Kanka, J., Nagova, E. and Malek, S. (2002) Expression of growth differentiation factor-9 (GDF-9) in porcine ovarian follicles. Reprod. Abstr. Ser. 29, Abstract 39.
142. Raftery, L.A. and Sutherland, D.J. (1999) TGF-beta family signal transduction in Drosophila development: from Mad to Smads. Dev. Biol., 210, 251-268.
143. Ralph, J.H. (1996) Factors affecting follicle and oocyte development in cattle. PhD thesis, University of Edinburgh.
144. Ralph, J.H., Telfer, E.E. and Wilmut, I. (1995) Bovine cumulus cell expansion does not depend on the presence of an oocyte secreted factor. Mol. Reprod. Dev., 42, 248-253.
145. Roberts, A.J. and Skinner, M.K. (1991) Transforming growth factor-alpha and -beta differentially regulate growth and steroidogenesis of bovine thecal cells during antral follicle development. Endocrinology, 129, 2041-2048.
146. Roberts, V.J., Barth, S., el Roeiy, A. and Yen, S.S. (1993) 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., 77, 1402-1410.
147. Rodgers, R.J. and Irving Rodgers, H.F. (2002) Extracellular matrix of the bovine ovarian membrana. granulosa. Mol. Cell. Endocrinol., 191, 57-64.
148. Rose, U.M., Hanssen, R.G. and Kloosterboer, H.J. (1999) Development and characterization of an in vitro ovulation model using mouse ovarian follicles. Biol. Reprod., 61, 503-511.
149. Roy, S.K. (1993a) Epidermal growth factor and transforming growth factor-beta modulation of follicle-stimulating hormone-induced deoxyribonucleic acid synthesis in hamster preantral and early antral follicles. Biol. Reprod., 48, 552-557.
150. Roy, S.K. (1993b) Transforming growth factor-beta potentiation of follicle-stimulating hormone-induced deoxyribonucleic acid synthesis in hamster preantral follicles is mediated by a latent induction of epidermal growth factor. Biol. Reprod., 48, 558-563.
151. Roy, S.K. and Greenwald, G.S. (1989) Hormonal requirements for the growth and differentiation of hamster preantral follicles in long-term culture. J. Reprod. Fertil., 87, 103-114.
152. Roy, S.K. and Terada, D.M. (1999) Activities of glucose metabolic enzymes in human preantral follicles: in vitro modulation by follicle-stimulating hormone, luteinizing hormone, epidermal growth factor, insulin-like growth factor I, and transforming growth factor beta1. Biol. Reprod., 60, 763-768.
153. Roy, S.K. and Treacy, B.J. (1993) Isolation and long-term culture of human preantral follicles. Fertil. Steril., 59, 783-790.
154. Saha, S., Shimizu, M., Geshi, M. and Izaike, Y. (2000) In vitro culture of bovine preantral follicles. Anim. Reprod. Sci., 63, 27-39.
155. Saumande, J. (1991) Culture of bovine granulosa cells in a chemically defined serum-free medium: the effect of insulin and fibronectin on the response to FSH. J. Steroid Biochem. Mol. Biol., 38, 189-196.
156. Schams, D., Berisha, B., Kosmann, M., Einspanier, R. and Amselgruber, W.M. (1999) Possible role of growth hormone, IGFs, and IGF-binding proteins in the regulation of ovarian function in large farm animals. Domest. Anim. Endocrinol., 17, 279-285.
157. Schroeder, A.C. and Eppig, J.J. (1989) Developmental capacity of mouse oocytes that undergo maturation in vitro: effect of the hormonal state of the oocyte donor. Gamete Res., 24, 81-92.
158. Schultz, R.M. and Wassarman, P.M. (1977) Biochemical studies of mammalian oogenesis: Protein synthesis during oocyte growth and meiotic maturation in the mouse. J. Cell Sci., 24, 167-194.
159. Simon, A.M., Goodenough, D.A., Li, E. and Paul, D.L. (1997) Female infertility in mice lacking connexin 37. Nature, 385, 525-529.
160. Smitz, J. and Cortvrindt, R. (1998) Follicle culture after ovarian cryostorage. Maturitas, 30, 171-179.
161. Spears, N., Boland, N.I., Murray, A.A. and Gosden, R.G. (1994) Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile. Hum. Reprod., 9, 527-532.
162. Spears, N., de Bruin, J.P. and Gosden, R.G. (1996) The establishment of follicular dominance in co-cultured mouse ovarian follicles. J. Reprod. Fertil., 106, 1-6.
163. Spears, N., Murray, A.A., Allison, V., Boland, N.I. and Gosden, R.G. (1998) Role of gonadotrophins and ovarian steroids in the development of mouse follicles in vitro. J. Reprod. Fertil., 113, 19-26.
164. Telfer, E.E., Ansell, J.D., Taylor, H. and Gosden, R.G. (1988) The numbers of clonal precursors in the follicular epithelium of the mouse ovary. J. Reprod. Fertil., 84, 105-110.
165. Telfer, E., Torrance, C. and Gosden, R.G. (1990) Morphological study of cultured preantral ovarian follicles of mice after
166. Telfer, E.E., Binnie, J.P., McCaffery, F.H. and Campbell, B.K. (2000) In vitro development of oocytes from porcine and bovine primary follicles. Mol. Cell. Endocrinol., 163, 117-123.
167. Thomas, F.H., Leask, R., Srsen, V., Riley, S.C., Spears, N. and Telfer, E.E. (2001) Effect of ascorbic acid on health and morphology of bovine preantral follicles during long-term culture. Reproduction, 122, 487-495.
168. Thomas, F.H., Campbell, B.K., Baird, D. and Telfer, E.E. (2002) Oocyte development and granulosa cell differentiation in ovine preantral follicles in vitro: Effect of androstenedione and activin A. Reprod. Abstr. Ser. 29, Abstract 4.
169. Tilly, J.L. and Tilly, K.I. (1995) Inhibitors of oxidative stress mimic the ability of follicle-stimulating hormone to suppress apoptosis in cultured rat ovarian follicles. Endocrinology, 136, 242-252.
170. Tilly, J.L., Kowalski, K.I., Johnson, A.L. and Hsueh, A.J. (1991) Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology, 129, 2799-2801.
171. Tilly, J.L., Billig, H., Kowalski, K.I. and Hsueh, A.J. (1992) Epidermal growth factor and basic fibroblast growth factor suppress the spontaneous onset of apoptosis in cultured rat ovarian granulosa cells and follicles by a trosine kinase-dependent mechanism. Mol. Endocrinol., 6, 1942-1950.
172. Tisdall, D.J., Quirke, L.D., Smith, P. and McNatty, K.P. (1997) Expression of the ovine stem cell factor gene during folliculogenesis in late fetal and adult ovaries. J. Mol. Endocrinol., 18, 127-135.
173. Tonetta, S.A. and diZerega, G.S. (1989) Intragonadal regulation of follicular maturation. Endocr. Rev., 10, 205-229.
174. Torrance, C., Telfer, E. and Gosden, R.G. (1989) Quantitative study of the development of isolated mouse pre-antral follicles in collagen gel culture. J. Reprod. Fertil., 87, 367-374.
175. VandenHurk, R., Bevers, M.M. and Beckers, J. (1997) In vivo and in vitro development of preantral follicles. Theriogenology, 47, 73-82.
176. VandenHurk, R., Spek, E.R., Hage, W.J., Fair, T., Ralph, J.H. and Schotanus, K. (1998) Ultrastructure and viability of isolated bovine preantral follicles. Hum. Reprod. Update, 4, 833-841.
177. VandenHurk, R., Abir, R., Telfer, E.E. and Bevers, M.M. (2000) Primate and bovine immature oocytes and follicles as sources of fertilizable oocytes. Hum. Reprod. Update, 6, 457-474.
178. Vanderhyden, B.C., Caron, P.J., Buccione, R. and Eppig, J.J. (1990) Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol., 140, 307-317.
179. Vanderhyden, B.C., Telfer, E.E. and Eppig, J.J. (1992) Mouse oocytes promote proliferation of granulosa cells from preantral and antral follicles in vitro. Biol. Reprod., 46, 1196-1204.
180. vanEijk, M.J., Mandelbaum, J., Salat-Baroux, J., Belaisch-Allart, J., Plachot, M., Junca, A.M. and Mummery, C.L. (1996) Expression of leukaemia inhibitory factor receptor subunits LIFR beta and gp130 in human oocytes and preimplantation embryos. Mol. Hum. Reprod., 2, 355-360.
181. Vitt, U.A., Hayashi, M., Klein, C. and Hsueh, A.J. (2000) 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., 62, 370-377.
182. Wandji, S.A., Pelletier, G. and Sirard, M.A. (1992) Ontogeny and cellular localization of 125I-labeled insulin-like growth factor-I, 125I-labeled follicle-stimulating hormone, and 125I-labeled human chorionic gonadotropin binding sites in ovaries from bovine fetuses and neonatal calves. Biol. Reprod., 47, 814-822.
183. Wandji, S.A., Eppig, J.J. and Fortune, J.E. (1996a) FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles. Theriogenology, 45, 817-832.
184. Wandji, S.A., Srsen, V., Voss, A.K., Eppig, J.J. and Fortune, J.E. (1996b) Initiation in vitro of growth of bovine primordial follicles. Biol. Reprod., 55, 942-948.
185. Wandji, S.A., Srsen, V., Nathanielsz, P.W., Eppig, J.J. and Fortune, J.E. (1997) Initiation of growth of baboon primordial follicles in vitro. Hum. Reprod., 12, 1993-2001.
186. Wandji, S.A., Wood, T.L., Crawford, J., Levison, S.W. and Hammond, J.M. (1998) Expression of mouse ovarian insulin growth factor system components during follicular development and atresia. Endocrinology, 139, 5205-5214.
187. Webb, R.J., Marshall, F., Swann, K. and Carroll, J. (2002) Follicle-stimulating hormone induces a gap junction-dependent dynamic change in (cAMP) and protein kinase A in mammalian oocytes. Dev. Biol., 246, 441-454.
188. Wilson, T., Wu, X.Y., Juengel, J.L., Ross, I.K., Lumsden, J.M., Lord, E.A., Dodds, K.G., Walling, G.A., McEwan, J.C., O'Connell, A.R. et al. (2001) Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol. Reprod., 64, 1225-1235.
189. Wright, C.S., Hovatta, O., Margara, R., Trew, G., Winston, R.M., Franks, S. and Hardy, K. (1999) Effects of follicle-stimulating hormone and serum substitution on the in-vitro growth of human ovarian follicles. Hum. Reprod., 14, 1555-1562.
190. Wright, C.S., Becker, D.L., Lin, J.S., Warner, A.E. and Hardy, K. (2001) Stage-specific and differential expression of gap junctions in the mouse ovary: connexin-specific roles in follicular regulation. Reproduction, 121, 77-88.
191. Wu, J., Emery, B.R. and Carrell, D.T. (2001) In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles. Biol. Reprod., 64, 375-381.
192. Wyllie, A.H. (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284, 555-556.
193. Yoshida, H., Takakura, N., Kataoka, H., Kunisada, T., Okamura, H. and Nishikawa, S.I. (1997) Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Dev. Biol., 184, 122-137.
194. Yoshimura, Y., Ando, M., Nagamatsu, S., Iwashita, M., Adachi, T., Sueoka, K., Miyazaki, T., Kuji, N. and Tanaka, M. (1996) Effects of insulin-like growth factor-I on follicle growth, oocyte maturation, and ovarian steroidogenesis and plasminogen activator activity in the rabbit. Biol. Reprod., 55, 152-160.
195. Yuan, W., Lucy, M.C. and Smith, M.F. (1996) Messenger ribonucleic acid for insulin-like growth factors-I and -II, insulin-like growth factor-binding protein-2, gonadotropin receptors, and steroidogenic enzymes in porcine follicles. Biol. Reprod., 55, 1045-1054.
196. Yutaka, M., Manganaro, T., Tao, X.-J., Martimbeau, S., Donahoe, P. and Tilly, J. (1999) Requirement of phosphatidylinositol-3′-kinase in cytokine-mediated germ cell survival during fetal oogenesis in the mouse. Endocrinology, 140, 941-949.
197. Zeleznik, A. and Hillier, S.G. (1996) The ovary: endocrine function. In Hillier, S.G., Kitchener, H.C. and Neilson, J.P. (eds), Scientific Essentials of Reproductive Medicine. W.B.Saunders, Philadelphia, pp. 133-147.
198. Zhang, P., Hreinsson, J.G., Telfer, E. and Hovatta, O. (2002) Few instead of many: human follicle collection from follicular aspirates at oocyte retrieval. Hum. Reprod., 17, 3190-3192.
199. Zhao, J., Dorland, M., Taverne, M.A., van der Weijden, G.C., Bevers, M.M. and Van den, H.R. (2000) In vitro culture of rat pre-antral follicles with emphasis on follicular interactions. Mol. Reprod. Dev., 55, 65-74.
200. Zhou, J., Bievre, M. and Bondy, C.A. (2000) Reduced GLUT1 expression in Igf1-/- null oocytes and follicles. Growth Horm. IGF Res., 10, 111-117.