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New approaches to increasing oocyte yield from ruminants

Published online by Cambridge University Press:  18 August 2016

E. E. Telfer
Affiliation:
Institute of Ecology and Resource Management, School of Agriculture, University of Edinburgh, West Mains Road, Edinburgh EH9 3JG
R. Webb
Affiliation:
Division of Agriculture and Horticulture, School of Biological Sciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD
R. M. Moor
Affiliation:
Laboratory of Protein Function, Babraham Institute, Cambridge CB2 4AT
R. G. Gosden
Affiliation:
Centre for Reproduction, Growth and Development, Research School of Medicine, University of Leeds, Leeds LS2 9NS
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Abstract

Artificial insemination, superovulation and embryo transfer have had beneficial impacts on animal production but a limiting factor to realizing the full potential of these techniques and of other reproductive technologies is the availability of fertile oocytes. To overcome this problem, methods for maturing oocytes in vitro (IVM) have been developed. The production of bovine embryos by IVM is in commercial use but the rate of success and quality of embryos is low. The lack of success may be due to the quality of oocytes that are being matured and it would be preferable to utilize the abundant source of immature oocytes from preantral and primordial follicles by developing systems for in vitro growth (IVG). Several culture systems that utilize early growing follicles as a source of oocytes have been developed for laboratory species and these have been successful in producing live young. IVG in association with IVM and cryopreservation have the potential to maximize the genetic potential of high genetic merit females and shorten generation intervals. This paper presents the current status of technology for the in vitro growth and development of immature oocytes, in vitro maturation and cryopreservation of germ cells in domestic ruminants.

Type
Research Article
Copyright
Copyright © British Society of Animal Science 1999

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References

Bach varo va, R. 1985. Gene expression during oogenesis and oocyte development in the mammal. In Developmental biology: a comprehensive synthesis, vol. 1 (ed. Browder, L. W.), vol. 1, pp. 453524. Plenum, New York.Google Scholar
Behboodi, E., Anderson, G.B., Bondurant, R. H., Cargill, S. L., Kreuscher, B. R., Medrano, J. F. and Murray, J. D. 1995. Birth of large calves that developed from in vitro derived embryos. Theriogenology 44: 227232.CrossRefGoogle Scholar
Boland, N. I. and Gosden, R. G. 1994. Effects of epidermal growth-factor on the growth and differentiation of cultured mouse ovarian follicles. Journal of Reproduction and Fertility 101: 369374.CrossRefGoogle ScholarPubMed
Boland, N. L., 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 . Biology of Reproduction 48: 798806.CrossRefGoogle ScholarPubMed
Braw-Tal, R. and Yossefi, S. 1997. Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. journal of Reproduction and Fertility 109:165171.CrossRefGoogle ScholarPubMed
Buccione, R., Schroeder, A. C. and Eppig, J. J. 1990. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biology of Reproduction. 43: 543547.CrossRefGoogle ScholarPubMed
Bukovsky, A., Caudle, M. R., Keenan, J. A., Wimalasena, J. and Foster, J. S. 1995. Expression of cell-cycle regulatory proteins (P53, PRB) in the human female genital tract. journal of Assisted Reproduction and Genetics 12: 123131.CrossRefGoogle ScholarPubMed
Canili, L. P. 1981. Folliculogenesis in the sheep as influenced by breed, season and oestrous cycle. Journal of Reproduction and Fertility 30: 135142.Google Scholar
Canili, L. P., Mariana, J. C. and Mauleon, P. 1979. Total follicle populations in ewes with high and low ovulation rates. Journal of Reproduction and Fertility 55: 2736.Google Scholar
Canili, L. P. and Mauleon, P. 1980. Influences of season, cycle and breed on follicular growth rates in sheep. Journal of Reproduction and Fertility 58: 321328.Google Scholar
Cain, L., Chatterjee, S. and Collins, T. J. 1995. In vitro folliculogenesis of rat preantral follicles. Endocrinology 136: 33693377.CrossRefGoogle ScholarPubMed
Carroll, J. and Gosden, R. G. 1993. Transplantation of frozen-thawed mouse primordial follicles. Human Reproduction 8: 11631167.CrossRefGoogle ScholarPubMed
Carroll, J., Whittingham, D. G. and Wood, M. J. 1991. Effect of dibutryl cyclic adenosine monophosphate on granulosa cell proliferation, oocyte growth and meiotic maturation in isolated mouse primary ovarian follicles cultured in collagen gels. Journal of Reproduction and Fertility 92: 197207.CrossRefGoogle Scholar
Carroll, J., Whittingham, D. G., Wood, M. J., Telfer, E. and Gosden, R. G. 1990. Extra-ovarian production of mature viable mouse oocytes from frozen primary follicles. Journal of Reproduction and Fertility 90: 321328.CrossRefGoogle ScholarPubMed
Cecconi, S., Rossi, G., DeFelici, M. and Colonna, R. 1996. Mammalian oocyte growth in vitro is stimulated by soluble factor(s) produced by preantral granulosa cells and sertoli cells. Molecular Reproduction and Development 44: 540546.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Chang, M. C. 1955. The maturation of rabbit oocytes in culture and their maturation, activation, fertilization and subsequent development in the Fallopian tubes. Journal of Experimental Zoology 128: 379405.CrossRefGoogle Scholar
Christmann, L., Jung, T. and Moor, R. M. 1994. MPF components and meiotic competence in growing pig oocytes. Molecular Reproduction and Development 38: 8590.CrossRefGoogle ScholarPubMed
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. Journal of Reproduction and Fertility 106: 329335.CrossRefGoogle ScholarPubMed
Cortvrindt, R., Smitz, J. and van Steirtegham, A. C. 1996. In vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepubertal mice in a simplified culture system. Human Reproduction 12: 26562666.CrossRefGoogle Scholar
Cran, D. G., Moor, R. M. and Hay, M. F. 1976. Permeability of ovarian follicles to electron-dense macromolecules. Acta Endocrinologica 82: 632636.Google ScholarPubMed
Cross, P. C. and Brinster, R. L. 1970. In vitro development of mouse oocytes. Biology of Reproduction. 3: 298307.CrossRefGoogle ScholarPubMed
Crozet, N., Ahmed, A. and Dubos, M. P. 1995. Developmental competence of goat oocytes from follicles of different size categories following maturation, fertilization and culture in vitro . Journal of Reproduction and Fertility 105: 293298.CrossRefGoogle Scholar
Daniel, S. A., Armstrong, D. T. and Gore-Langton, R.E. 1989. Growth and development of rat oocytes in vitro . Gamete Research 24:109121.CrossRefGoogle ScholarPubMed
Das, K., Stout, L. E., Hensleigh, H. C., Tagatz, G. E., Phipps, W. R. and Leung, B. S. 1991. Direct positive effect of epidermal growth factor on the cytoplasmic maturation of mouse and human oocytes. Fertility and Sterility 55: 10001004.Google Scholar
Dieleman, S. J., Kruip, T. A. M., Fontijne, P., Jong, W. H. R. de and Weyden, G. C. van der. 1983. Changes in oestradiol, progesterone and testosterone concentration in follicular fluid and in the micromorphology of preovulatory bovine follicles relative to the peak of luteinizing hormone. Journal of Endocrinology 97: 3142.CrossRefGoogle Scholar
Donnelly, K. and Telfer, E. E. 1994. Growth of porcine preantral ovarian follicles in different culture systems. Journal of Reproduction and Fertility, Abstract Series 13: 76 (abstr.).Google Scholar
Downs, S. M. and Daniel, S. A. 1988. Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin. Journal of Experimental Zoology 245: 8696.CrossRefGoogle ScholarPubMed
Edwards, R. G. 1965. Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208: 349351.CrossRefGoogle ScholarPubMed
Eppig, J. J. 1977. Mouse oocyte development in vitro with various culture systems. Developmental Biology 60: 371388.CrossRefGoogle ScholarPubMed
Eppig, J. J. 1979. A comparison between oocyte growth in coculture with granulosa cell-oocyte junctional contact maintained in vitro . Journal of Experimental Zoology 209: 345353.CrossRefGoogle ScholarPubMed
Eppig, J. J. 1994. Further reflections on culture systems for the growth of oocytes in vitro . Human Reproduction 9: 969976.CrossRefGoogle ScholarPubMed
Eppig, J. J. and O’Brien, M.J. 1996. Development in vitro of mouse oocytes from primordial follicles. Biology of Reproduction 54:197207.CrossRefGoogle ScholarPubMed
Eppig, J. J. and O’Brien, M.J. 1998. Comparison of preimplantation developmental competence after mouse oocyte growth development in vitro and in vivo . Theriogenology 49: 415422.CrossRefGoogle ScholarPubMed
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. Molecular Reproduction and Development 34: 450456.CrossRefGoogle ScholarPubMed
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 . Biology of Reproduction 41: 268276.CrossRefGoogle ScholarPubMed
Eppig, J. J. and Telfer, E. E. 1993. Isolation and culture of oocytes. Methods in Enzymology 225: 7784.CrossRefGoogle ScholarPubMed
Erickson, B. H. 1966. Development and senescence of the postnatal bovine ovary. Journal of Animal Science 25: 800805.CrossRefGoogle ScholarPubMed
Faddy, M. J., Telfer, E. E. and Gosden, R. G. 1987. The kinetics of preantral follicle development in ovaries of CBA/Ca mice during the first 14 weeks of life. Cell and Tissue Kinetics 20: 551560.Google ScholarPubMed
Fair, T., Hyttel, P. and Greve, T. 1995. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Molecular Reproduction and Development 42: 437442.CrossRefGoogle ScholarPubMed
Figueiredo, J. R., Hulshof, S. C. J., Hurk, R. van den, Nusgens, B., Bevers, M. M., Ectors, F. J. and Beckers, J. F. 1994. Preservation of oocyte and granulosa cell morphology in bovine preantral follicles cultured in vitro . Theriogenology 41:13331346.CrossRefGoogle ScholarPubMed
Figueiredo, J. R., Hulshof, S. C. J., Thiry, M., Hurk, R. van den, Bevers, M. M., Nusgens, B. and Beckers, J. F. 1995. Extracellular matrix proteins and basement membrane: their identification in bovine ovaries and significance for the attachment of cultured preantral follicles. Theriogenology 43: 845858.CrossRefGoogle ScholarPubMed
Fortune, J.E. 1994. Ovarian follicular growth and development in mammals. Biology of Reproduction 50: 225232.CrossRefGoogle ScholarPubMed
Fortune, J. E., Kito, S., Wandji, S.-A. and Sršen, V. 1998. Activation of bovine and baboon primordial follicles in vitro . Thcriogenology 49: 441449.CrossRefGoogle ScholarPubMed
Funahashi, H., Mclntush, E. W., Smith, M. F. and Day, B. N. 1997. Effect of tissue inhibitor of metalloproteinase (TIMP-1) on early development of swine oocytes matured and fertilized in vitro . Theriogenology 47: 277.CrossRefGoogle Scholar
Galii, C. and Lazzari, G. 1996. Practical aspects IVM/IVF in cattle. Animal Reproduction Science 42: 371379.CrossRefGoogle Scholar
Gordon, J. 1994. Laboratory production of cattle embryos. CAB International, Wallingford.Google Scholar
Gosden, R. G. 1992. Ovarian germ cell manipulation and transplantation. AgBiotech News and Information 4: 337340.Google Scholar
Gosden, R. G., Baird, D. T., Wade, J. C. and Webb, R. 1994a. Restoration of fertility to oophorectomised sheep by ovarian autografe stored at -196°C. Human Reproduction 9: 597603.CrossRefGoogle Scholar
Gosden, R. G., Boulton, M. I., Grant, K. and Webb, R. 1994b. Follicular development from ovarian xenografts in seid mice. Journal of Reproduction and Fertility 101: 619623.CrossRefGoogle Scholar
Gosden, R. G. and Telfer, E. 1987a. Scaling of follicular sizes in mammalian ovaries. Journal of Zoology 211:157168.CrossRefGoogle Scholar
Gosden, R. G. and Telfer, E. 1987b. Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships. Journal of Zoology 211: 169175.CrossRefGoogle Scholar
Greenwald, G. S. and Moor, R. M. 1989. Isolation and preliminary characterization of pig primordial follicles. Journal of Reproduction and Fertility 87: 561571.CrossRefGoogle ScholarPubMed
Grob, H. S. 1964. Enzymatic dissection of the mammalian ovary. Science 146: 7374.CrossRefGoogle ScholarPubMed
Guiterrez, C., Ralph, J.H., Telfer, E. E., Wilmut, I. and Webb, R. 1999. In vitro development of bovine follicles. Biology of Reproduction In press.Google Scholar
Guiterrez, C., Ralph, J. H., Wilmut, I. and Webb, R. 1997. Follicle growth and antrum formation of bovine preantral follicles in long-term in vitro culture. Journal of Reproduction and Fertility Abstract Series 19: 18 (abstr.).Google Scholar
Harade, Mv Miyano, T., Matsumura, K., Osaki, S., Miyake, M. and Kato, S. 1997. Bovine oocytes from early antral follicles grow to meiotic competence in vitro: effects of FSH and hypoxanthine. Theriogenology 48: 743755.Google Scholar
Harp, R., Leibach, J., Black, J., Keldahl, C. and Karow, A. 1994. Cryopreservation of murine ovarian tissue. Cryobiology 31: 336343.CrossRefGoogle ScholarPubMed
Hasler, J. F., Henderson, W.B., Hurtgen, P. J., Jin, Z. Q., McCauley, A. D., Mower, S. A., Neeley, B., Shuey, L. S., Stokes, J. E. and Trimmer, S. A. 1995. Production, freezing and transfer of bovine IVF embryos and subsequent calving results. Theriogenology 43: 141152.CrossRefGoogle Scholar
Hirao, Y., Nagai, T., Kubo, M., Miyano, T. and Kato, S. 1994. In vitro growth and maturation of pig oocytes. Journal of Reproduction and Fertility 100: 333339.CrossRefGoogle ScholarPubMed
Hirshfield, A. N. 1991. Development of follicles in the mammalian ovary. International Reviews of Cytology 124: 43101.CrossRefGoogle ScholarPubMed
Howe, C. C. and Solter, D. 1979. Cytoplasmic and nuclear protein synthesis in preimplantation mouse embryos. Journal of Embryology and Experimental Morphology 52: 209225.Google ScholarPubMed
Hulshof, S.C. J., Figueiredo, J. R., Beckers, J. F., Bevers, M. M., Donk, J. A. van der and Hurk, R. van den. 1995. Effects of fetal bovine serum, FSH and 17ß-estradiol on the culture of bovine preantral follicles. Theriogenology 44: 217226.CrossRefGoogle Scholar
Hurk, R. van den, Bevers, M. M. and Beckers, J. F. 1997. In-vivo and in-vitro development of preantral follicles. Theriogenology 47: 7382.CrossRefGoogle Scholar
Hyttel, P., Fair, T., Caliesen, H. and Greve, T. 1997. Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47: 2332.CrossRefGoogle Scholar
Jewgenow, K. and Pitra, C. 1991. A method for isolation of preantral follicles from cattle ovaries. Reproduction in Domestic Animals 6: 281289.CrossRefGoogle Scholar
Johnson, L. D., Albertini, D. F., McGinnis, L. K. and Biggers, J. D. 1995. Chromatin organization, meiotic status and meiotic competence acquisition in mouse oocytes from cultured ovarian follicles. Journal of Reproduction and Fertility 104: 277284.CrossRefGoogle ScholarPubMed
Kruip, T. A. M. and Boni, R. 1994. Repeated follicular oocyte recovery for bovine embryo production in vitro . In Progress in embryo technology and genetic engineering in cattle and sheep breeding, pp. 117126.Google Scholar
Lazzari, G. and Galli, C. 1996. In vitro embryo production and its application to cattle breeding. 12e reunion Association Europeene de Transfert Embryonnaire, Lyon, 13-14 September, pp. 7382.Google Scholar
Lonergan, P., Carolan, C., Langendonckt, A. van, Donnay, I., Khatir, H. and Mermillod, P. 1996. Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro . Biology of Reproduction 54: 14201429.CrossRefGoogle ScholarPubMed
Lonergan, P., Monaghan, P., Rizos, D., Boland, M. P. and Gordon, D. 1994. Effects of follicle size on bovine oocyte quality and developmental competence following maturation, fertilisation and culture in vitro . Molecular Reproduction and Development 37: 4853.CrossRefGoogle ScholarPubMed
Looney, C. R., Lindsey, B. R., Gonseth, C. L. and Johnson, D. L. 1994. Commercial aspects of oocyte retrieval and in vitro fertilization (IVF) for embryo production in the problem cow. Theriogenology 41: 67-72. Lussier, J.G., Matton, P. and Dufour, J. J. 1987. Growth rates of follicles in the ovary of the cow. Journal of Reproduction and Fertility 81: 301307.CrossRefGoogle Scholar
Martinovitch, P. N. 1938. The development in vitro of the mammalian gonad. Ovary and oogenesis. Proceedings of the Royal Society of London, B 125: 232249.Google Scholar
Moor, R. M., Nagai, T. and Gandolfi, F. 1990. Somatic cell interactions in early mammalian development. In Ovulation to implantation (ed. Evers, J. L. H. and Heineman, M. J.), proceedings of the 7th Reinier de Graaf symposium, Maastricht, The Netherlands, pp. 177193. Elsevier Science Publishers.Google Scholar
Moor, R. M. and Trounson, A. O. 1977. Hormonal and follicular factors affecting maturation of sheep oocytes in vitro and their subsequent developmental capacity. Journal of Reproduction and Fertility 49: 101109.CrossRefGoogle ScholarPubMed
Nayudu, P. L. and Osborn, S. M. 1992. Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro . Journal of Reproduction and Fertility 95: 349362.CrossRefGoogle ScholarPubMed
Newton, H., Picton, H. and Gosden, R. G. 1999. In vitro growth of oocyte-granulosa cell complexes isolated from cryopreserved ovine tissue. Journal of Reproduction and Fertility In press.CrossRefGoogle ScholarPubMed
Nicosia, S. V., Evangelista, I. and Batta, S. K. 1975. Rabbit ovarian follicles. I. Isolation techniques and characterisation at different stages of development. Biology of Reproduction 13: 423447.CrossRefGoogle ScholarPubMed
Nuttinck, F., Mermillod, P., Massip, A. and Dessy, F. 1994. Characterization of in vitro growth of bovine preantral ovarian follicles: a preliminary study. Theriogenology 39: 811821.CrossRefGoogle Scholar
Oktay, K., Nugent, D., Newton, H., Salha, O., Chatterjee, P. and Gosden, R. G. 1997. Isolation and characterization of primordial follicles from fresh and cryopreserved human ovarian tissue. Fertility and Sterility 67: 481486.CrossRefGoogle ScholarPubMed
Parrott, D. M. 1960. The fertility of mice with orthotopic grafts derived from frozen tissue. Journal of Reproduction and Fertility 1: 230241.CrossRefGoogle Scholar
Pedersen, T. 1970. Determination of follicle growth rate in the ovary of the immature mouse. Journal of Reproduction and Fertility 121: 8193.CrossRefGoogle Scholar
Peters, H. 1969. The development of the mouse ovary from birth to maturity. Acta Endocrinologica 62: 98116.Google ScholarPubMed
Pincus, G. and Enzmann, E. V. 1935. The comparative behaviour of mammalian eggs in vivo and in vitro . Journal of Experimental Medicine 62: 665675.CrossRefGoogle ScholarPubMed
Rajakoski, E. 1960. The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical and left-right variations. Acta Endocrinologica 52: 768.Google Scholar
Ralph, J. H. 1996. Factors affecting follicle and oocyte development in cattle. Ph.D. thesis, University of Edinburgh. Google Scholar
Ralph, J. H., Telfer, E. E. and Wilmut, I. 1995a. Bovine cumulus cell expansion does not depend on the presence of an oocyte secreted factor. Molecular Reproduction and Development 42: 248253.CrossRefGoogle Scholar
Ralph, J. H., Wilmut, I. and Telfer, E. E. 1995b. In vitro growth of bovine preantral follicles and the influence of FSH on follicular and oocyte diameters. Journal of Reproduction and Fertility, Abstract Series 15: 6 (abstr.).Google Scholar
Ralph, J. H., Wilmut, I. and Telfer, E. E. 1996. The effect of FSH on bovine preantral to early antral ovarian follicle growth in vitro . Biology of Reproduction 1: 58.Google Scholar
Roy, S. K. and Greenwald, G. S. 1985. An enzymatic method for dissociation of intact follicles from the hamster ovary: histological and quantitative aspects. Biology of Reproduction 32: 203215.CrossRefGoogle ScholarPubMed
Roy, S. K. and Greenwald, G. S. 1989. Hormonal requirements for the growth and differentiation of hamster preantral follicles in long-term culture. Journal of Reproduction and Fertility 87: 103114.CrossRefGoogle ScholarPubMed
Roy, S. K. and Greenwald, G. S. 1996. Methods of separation and in vitro culture of pre-antral follicles from mammalian ovaries. Human Reproduction Update 2: 236245.CrossRefGoogle ScholarPubMed
Satoh, T., Kobayashi, K., Yamashita, S., Kikuchi, M., Sendal, Y. and Hoshi, I. I. 1994. Tissue inhibitor of metalloproteinases (TIMP-1) produced by granulosa and oviduct cells enhances in vitro development of bovine embryo. Biology of Reproduction 50: 835844.CrossRefGoogle ScholarPubMed
Scaramuzzi, R. J., Turnbull, K. E. and Nancarrow, C. D. 1980. Growth of Graafian follicles in cows following luteolysis induced by the prostaglandin F2a analogue, cloprostenol. Australian Journal of Biological Sciences 33: 6369.CrossRefGoogle Scholar
Schultz, R. M. and Wassarman, P. M. 1977. Biochemical studies of mammalian oogenesis: protein synthesis during oocyte growth and maturation in the mouse. Journal of Cell Science 24: 167194.CrossRefGoogle ScholarPubMed
Seamark, R. F., Moor, R. M. and Mclntosh, J. E. A. 1974. Steroid hormone production by sheep ovarian follicles culture in vitro . Journal of Reproduction and Fertility 41: 143158.CrossRefGoogle Scholar
Smith, G. W., Moor, R. M. and Smith, M.F. 1992. Identification of a 30,000 Mr polypeptide secreted by ovine granulosa cells and luteal tissue as a tissue inhibitor of metalloproteinases. Biology of Reproduction 48: 125132.CrossRefGoogle Scholar
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. Human Reproduction 9: 527532.CrossRefGoogle ScholarPubMed
Telfer, E., Ansell, J. D., Taylor, H. and Gosden, R. G. 1988. The number of clonai precursors of the follicular epithelium in the mouse ovary. Journal of Reproduction and Fertility 84: 105110.CrossRefGoogle Scholar
Telfer, E., Torrance, C. and Gosden, R. G. 1990. Morphological study of cultured preantral ovarian follicles of mice after transplantation under the kidney capsule. Journal of Reproduction and Fertility 89: 565571.CrossRefGoogle ScholarPubMed
Telfer, E. E. 1996. The development of methods for isolation and culture of preantral follicles from bovine and porcine ovaries. Theriogenology 45:101110.CrossRefGoogle Scholar
Telfer, E. E. 1998. In vitro models for oocyte development. Theriogenology 49: 451460.CrossRefGoogle ScholarPubMed
Telfer, E. E., Binnie, J. P. and Jordan, L. B. 1998a. Effect of follicle size on the onset of apoptotic cell death in cultured bovine ovarian follicles. Theriogenology 49: 357.CrossRefGoogle Scholar
Telfer, E. E., Binnie, J. P. and Jordan, L. B. 1998b. Relationship between developmental stage and apoptotic cell death in cultured bovine ovarian follicles. Journal of Reproduction and Fertility, Abstract Series 21: 8 (abstr.).Google Scholar
Thibault, C. and Gerard, M. 1973. Cytoplasmic and nuclear maturation of rabbit oocytes in vitro . Annales de Biologie Animale, Biochimie, Biophysique 13: 145156.CrossRefGoogle Scholar
Thompson, J. G. 1997. Comparison between in vivo derived and in vitro produced pre-elongation embryos from domestic ruminants. Reproduction, Fertility and Development 9: 341354.CrossRefGoogle ScholarPubMed
Torrance, C., Telfer, E. and Gosden, R. G. 1989. Quantitative study of the development of isolated mouse pre-antral follicles in collagen gel culture. Journal of Reproduction and Fertility 87: 367374.CrossRefGoogle ScholarPubMed
Turnbull, K.E., Braden, A. W. H. and Mattner, P. E. 1977. The pattern of follicular growth and atresia in the ovine ovary. Australian Journal of Biological Sciences 30: 229241.CrossRefGoogle ScholarPubMed
Vanderhyden, B. C., Carón, 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. Developmental Biology 140: 307317.CrossRefGoogle ScholarPubMed
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 . Biology of Reproduction 46: 11961204.CrossRefGoogle ScholarPubMed
Vincent, C. and Johnson, M. H. 1992. Cooling, cryoprotectants and the cytoskeleton of the mammalian oocyte. Oxford Reviews in Reproductive Biology 14: 73100.Google ScholarPubMed
Walker, S. K., Hartwich, K. M. and Seamark, R. F. 1996. The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenology 45: 111120.CrossRefGoogle Scholar
Walker, S. K., Heard, T. M. and Seamark, R. F. 1992. In vitro culture of sheep embryos without co-culture: successes and perspectives. Theriogenology 37: 111126.CrossRefGoogle Scholar
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: 817832.CrossRefGoogle ScholarPubMed
Wandji, S. A., Eppig, J. J. and Fortune, J. E. 1996b. Initiation in vitro of growth of primordial follicles. Biology of Reproduction 55: 942948.CrossRefGoogle ScholarPubMed
Webb, R., Gosden, R. G., Telfer, E. E. and Moor, R. M. 1999. Factors affecting folliculogenesis in ruminants. Animal Science 68: 257284.CrossRefGoogle Scholar
Willadsen, S. M., Janzen, R. E., McAlister, R. J., Shea, B. F., Hamilton, G. and McDermand, D. 1991. The viability of late morulae and blastocysts produced by nuclear transplantation in cattle. Theriogenology 35: 161170.CrossRefGoogle Scholar
Wu, T. C. J., Wang, L. and Wan, Y. J. Y. 1993. Detection and estrogen-receptor messenger-ribonucleic acid in human oocytes and cumulus oocyte complexes using reverse transcriptase polymerase chain reaction. Fertility and Sterility 59: 5459.Google ScholarPubMed
Wurth, Y. 1994. Bovine embryo production in vitro: influencing factors. CIP-GEGEVENS Koninklijke Bibliotheek, Den Haag, The Netherlands.Google Scholar
Yoshida, H., Takakura, N., Kataoka, H., Kunisada, T., Okamura, H. and Nishikawa, S. 1997. Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Developmental Biology 184:122137.CrossRefGoogle ScholarPubMed