Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-06-06T23:41:47.432Z Has data issue: false hasContentIssue false

The biology and technology of follicular oocyte development in vitro

Published online by Cambridge University Press:  02 March 2009

RG Gosden*
Affiliation:
Department of Physiology, University Medical School, Edinburgh, UK
NI Boland
Affiliation:
Department of Physiology, University Medical School, Edinburgh, UK
N Spears
Affiliation:
Department of Physiology, University Medical School, Edinburgh, UK
AA Murray
Affiliation:
Department of Physiology, University Medical School, Edinburgh, UK
M Chapman
Affiliation:
Department of Physiology, University Medical School, Edinburgh, UK
JC Wade
Affiliation:
Department of Physiology, University Medical School, Edinburgh, UK
NI Zohdy
Affiliation:
Department of Physiology, University Medical School, Edinburgh, UK
N Brown
Affiliation:
Department of Physiology, University Medical School, Edinburgh, UK
*
RG Gosden, Department of Physiology, University Medical School, Teviot Place, Edinburgh EH8 9AG, UK.

Extract

Fully mature oocytes are the rarest cells in the body. A premenopausal woman produces only one during each menstrual cycle and that survives for just a single day. Ovarian productivity is parsimonious in order that the ovulation rate matches the optimal capacity of the uterus for carrying conceptuses to full-term. But, in this new era of assisted reproductive medicine, there are many applications for which spare oocytes are needed (Table 1), and it is desirable to obtain more cells than are routinely available during superstimulated cycles. Since the great majority of ovarian oocytes undergo atresia (> 99.9%), the possibility of tapping the store of immature oocytes before they degenerate and maturing them in vitro is very attractive.

Type
Articles
Copyright
Copyright © Cambridge University Press 1993

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Eppig, JJ. Growth and development of mammalian oocytes in vitro. Arch Pathol Lab Med 1992; 116: 379–82.Google ScholarPubMed
2Gosden, RG, Boland, NI. Extracorporeal development of immature ovarian follicles. In: Templeton, AA, Drife, JO, eds. Infertility. London: Springer-Verlag, 1992: 263–75.Google Scholar
3Gosden, RG, Telfer, E. Scaling of follicular sizes in mammalian ovaries. J Zool 1987; 211: 157–68.Google Scholar
4Jones, EC, Krohn, PL. The effect of hypophysectomy on age changes in the ovaries of mice. J Endocrinol 1961; 21: 497508.Google Scholar
5Halpin, DMG, Jones, A, Fink, G, Charlton, HM. Postnatal ovarian follicle development of hypogonadal (hpg) and normal mice and associated changes in the hypothalamic-pituitary ovarian axis. J Reprod Fertil 1986; 77: 287–96.Google Scholar
6Moore, GPM, Lintern-Moore, S, Peters, H, Faber, M. RNA synthesis in the mouse oocyte. J Cell Biol 1974; 60: 416–22.Google Scholar
7Boland, NI, Gosden, RG. A clonal analysis of chimaeric mouse ovaries using DNA in situ hybridization. J Reprod Fertil 1993 (in press).Google Scholar
8Wassarman, PM. Zona pellucida glycoproteins. Ann Rev Biochem 1988; 57: 415–42.CrossRefGoogle ScholarPubMed
9Lee, VH, Dunbar, BS. Developmental expression of the rabbit 55-kDa zona pellucida protein and messenger RNA in ovarian follicles. Dev Biol 1993; 155: 371–82.Google Scholar
10Chiquoine, AD. The development of the zona pellucida of the mammalian ovum. Am J Anal 1960; 106: 149–69.Google Scholar
11Hope, J. The fine structure of the developing follicle of the rhesus ovary. J Ultrastruct Res 1965; 12: 592610.CrossRefGoogle ScholarPubMed
12Anderson, E, Albertini, DF. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol 1976; 71: 680–86.Google Scholar
13Gilula, NB, Epstein, ML, Beers, WH. Cell-to-cell communication and ovulation. J Cell Biol 1978; 78: 5875.CrossRefGoogle ScholarPubMed
14Moor, RM, Smith, MW, Dawson, RMC. Measurement of intercellular coupling between oocytes and cumulus cells using in tracellular markers. Exp Cell Res 1980; 126: 1529.CrossRefGoogle Scholar
15Heller, DT, Schultz, RM. Ribonucleoside metabolism by mouse oocytes: metabolic cooperati vi ty between the fully grown oocyte and cumulus cells. J Exp Zool 1980; 214: 355–64.CrossRefGoogle Scholar
16Herlands, RL, Schultz, RM. Regulation of mouse oocyte growth: probable nutritional role for intercellular communication between follicle cells and oocytes in oocyte growth. J Exp Zool 1984; 229: 317–25.Google Scholar
17Collona, R, Cecconi, S, Tatone, C, Mangia, F, Buccione, R. Somatic cell-oocyte interactions in mouse oogenesis: stage-specific regulation of mouse oocyte protein phosphorylation by granulosa cells. Dev Biol 1989; 133: 305308.Google Scholar
18Gosden, RG, Byatt-Smith, JG. Oxygen concentration gradient across the ovarian follicular epithelium: models, predictions and implications. Hum Reprod 1986; 1: 6568.CrossRefGoogle ScholarPubMed
19Edwards, RG. Follicular fluid. J Reprod Fertil 1974; 37: 189219.CrossRefGoogle ScholarPubMed
20Gosden, RG, Hunter, RHF, Telfer, E, Torrance, C, Brown, N. Physiological factors underlying the formation of ovarian follicular fluid. J Reprod Fertil 1988; 823: 813–25.Google Scholar
21Shalgi, R, Kraicer, PF, Soferman, N. Gases and electrolytes of human follicular fluid. J Reprod Fertil 1972; 28: 335–40.CrossRefGoogle ScholarPubMed
22Knudsen, JF, Litkowski, LJ, Wilson, TL, Guthrie, HD, Batta, SK. Concentrations of hydrogen ions, oxygen, carbon dioxide and bicarbonate in porcine follicular fluid. J Endocrinol 1978; 79: 249–50.Google Scholar
23Grinsted, J, Blendstrup, K, Andreasen, MP, Byskov, AG. Temperature measurements of rabbit antral follicles. J Reprod Fertil 1980; 60: 149–55.CrossRefGoogle ScholarPubMed
24Hedin, L, Rodgers, RJ, Simpson, ER, Richards, JS. Changes in content of cytochrome P45017α', cytochrome P450SCC and 3-hydroxy-3-methylglutaryl CoA reductase in developing rat ovarian follicles and corpora lutea: correlation with theca cell steroidogenesis. Biol Reprod 1987; 37: 211–23.Google Scholar
25Wang, C, Hsueh, AJW, Erickson, GF. LH stimulation of estrogen secretion by cultured rat granulosa cells. Mol Cell Endocrinol 1979; 24: 1724.Google Scholar
26Pedersen, T. Follicle growth in the immature mouse ovary. Acta Endocrinol 1969; 62: 117–32.Google ScholarPubMed
27Gougeon, A. Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod 1986; 1:8187.CrossRefGoogle Scholar
28Cahill, LP, Mauleon, P. Influences of season, cycle and breed on follicular growth rates in sheep. J Reprod Fertil 1980; 58: 321–28.Google Scholar
29Greenwald, GS, Terranova, PF. Follicular selection and its control. In: Knobil, E, Neill, J eds. The physiology of reproduction, Volume 1. New York: Raven Press, 1988: 387445.Google Scholar
30Roy, SK, Greenwald, GS. Hormonal requirements for the growth and differentiation of hamster preantral follicles in long-term culture. J Reprod Fertil 1989; 87: 103–14.CrossRefGoogle ScholarPubMed
31Wang, X-N, Greenwald, GS. Hypophysectomy of the cyclic mouse. I. Effects on folliculogenesis, oocyte growth, and follicle-stimulating hormone and human chorionic gonadotropin receptors. Biol Reprod 1993; 48: 585–94.Google Scholar
32Tilly, JL, Kowalski, KI, Schomberg, DW, Hsueh, AJW. Apoptosis in atretic ovarian follicles is associated with selective decreases in messenger ribonucleic acid transcripts for gonadotropin receptors and cytochrome P450 aromatase. Endocrinology 1992; 131: 1670–76.Google Scholar
33Armstrong, DT, Dorrington, JH. Oestrogen biosynthesis in the ovaries and testes. In: Thomas, JA, Singhai, RA eds. Regulatory mechanisms affecting gonadal hormone action, Volume 2. Baltimore: University Park Press, 1979: 217–58.Google Scholar
34Richards, JS, Jahnsen, T, Hedin, L et al. Ovarian follicular development: from physiology to molecular biology. Ree Prog Harm Res 1987; 43: 231–70.Google Scholar
35Wu, T-CJ, Wang, L, Wan, Y-JY. Expression of estrogen receptor gene in mouse oocyte and during embryogenesis. Mol Reprod Dev 1992; 33: 407–12.CrossRefGoogle ScholarPubMed
36Murray, AA, Boland, NI, Wade, JC, Gosden, RG. Unpublished observations.Google Scholar
37Eppig, JJ. Mouse oocyte development in vitro with various culture systems. Dev Biol 1977; 60: 371–88.Google Scholar
38Hsueh, AJW. Paracrine mechanisms involved in granulosa cell differentiation. Clin Endocr Metab 1986; 15: 117–34.Google Scholar
39Ackland, JF, Schwartz, NB, Mayo, KE, Dodson, RE. Non-steroidal signals originating in the gonads. Physiol Rev 1992; 72: 731–87.Google Scholar
40Findlay, JK. An update on the roles of inhibin, activin, and follistatin as local regulators of folliculogenesis. Biol Reprod 1993; 48: 1523.Google Scholar
41Venderhyden, BC, Telfer, EE, Eppig, JJ. Mouse oocytes promote proliferation of granulosa cells from preantral and an trai follicles in vitro. Biol Reprod 1992; 46: 1196–204.CrossRefGoogle Scholar
42Vanderhyden, BC. Species differences in the regulation of cumulus expansion by an oocyte-secreted factor(s). J Reprod Fertil 1993; 98: 219–27.Google Scholar
43Edwards, RG. Maturation in vitro of mouse, sheep, cow, pig, Rhesus monkey and human ovarian oocytes. Nature 1965; 208: 349–51.Google Scholar
44Sorensen, RA, Wassarman, PM. Relationship between growth and meiotic maturation of the mouse oocyte. Dev Biol 1976; 50: 531–36.CrossRefGoogle ScholarPubMed
45Block, E. Quantitative morphological investigations of the follicular system in women. Variations at different ages. Acta Anat 1952: 14: 108–23.Google Scholar
46Faddy, MJ, Telfer, E, Gosden, RG. The kinetics of preantral follicle development in ovaries of CBA/Ca mice during the first 14 weeks of life. Cell Tissue Kinetics 1987; 20: 551–60.Google Scholar
47Hay, MF, Moor, RM, Cran, DG, Dott, HM. Regeneration of atretic follicles in vitro. J Reprod Fertil 1979; 55: 195207.CrossRefGoogle ScholarPubMed
48Faddy, MJ, Gosden, RG, Gougeon, A, Richardson, SJ, Nelson, JF. Accelerated disappearance of ovarian follicles in mid-life – implications for forecasting menopause. Hum Reprod 1992; 7: 1342–46.Google Scholar
49Gosden, RG, Telfer, E. Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships. J Zool 1987; 211: 169–75.Google Scholar
50Martinovitch, PN. The development in vitro of the mammalian gonad-ovary and ovogenesis. Proc R Soc Land [Biol] 1938; 125: 232–49.Google Scholar
51Ryle, M. Morphological responses to pituitary gonadotrophins by mouse ovaries in vitro. J Reprod Fertil 1969; 20: 307312.CrossRefGoogle ScholarPubMed
52Baker, TG, Neal, P. Gonadotrophin-induced maturation of mouse Graafian follicles in organ culture. In: Biggers, JD, Schuetz, AW eds. Oogenesis. Baltimore: University Park Press, 1972; 377–96.Google Scholar
53Roy, SK, Greenwald, GS. An enzymatic method for dissociation of intact follicles from the hamster ovary: histological and quantitative aspects. Biol Reprod 1985; 32: 203–15.Google Scholar
54Torrance, C, Telfer, E, Gosden, RG. Quantitative study of the development of isolated mouse preantral follicles in collagen gel culture. J Reprod Fertil 1989; 87: 367–74.CrossRefGoogle ScholarPubMed
55Poste, G. Tissue dissociation with proteolytic enzymes. Exp Cell Res 1971; 65: 359–67.CrossRefGoogle ScholarPubMed
56Greenwald, GS, Moor, RM. Isolation and preliminary characterization of pig primordial follicles. J Reprod Fertil 1989; 87: 561–71.Google Scholar
57Lazzari, G, Galli, C, Moor, RM. Centrifugal elutriation of porcine oocytes isolated from the ovaries of newborn piglets. Anal Biochem 1992; 200: 3135.CrossRefGoogle ScholarPubMed
58Roy, SK, Treacy, BJ. Isolation and long-term culture of human preantral follicles. Fertil Steril 1993; 59: 783–90.Google Scholar
59Taha, TA, Schellander, K. Isolation and culture of primary follicles from cattle ovaries. 12th International Congress on Animal Reproduction. The Netherlands: The Hague, 1992: abstract 85.Google Scholar
60Eppig, JJ. Growth and development of mammalian oocytes in vitro. Arch Pathol Lab Med 1992; 116: 379–82.Google ScholarPubMed
61Telfer, E, Torrance, C, Gosden, RG. Morphological study of cultured preantral ovarian follicles of mice after transplantation under the kidney capsule. J Reprod Fertil 1990; 89: 565–71.Google Scholar
62Daniel, SAJ, Armstrong, DT, Gore-Langton, RE. Growth and development of rat oocytes in vitro. Gamete Res 1989; 24: 109–21.Google Scholar
63Hirao, Y, Nagai, T, Kubo, M, Miyano, T, Miyake, M, Kalo, S. In vitro growth and maturation of pig oocytes. J Reprod Fertil 1993 (in press).CrossRefGoogle Scholar
64Eppig, JJ, Peters, AHFM, Telfer, EE, Wigglesworth, K. Production of cumulus expansion enabling factor by mouse oocytes grown in vitro: preliminary characterization of the factor. Mol Reprod Dev 1993; 34: 450–56.Google Scholar
65Eppig, JJ, Schroeder, AC. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation and fertilization in vitro. Biol Reprod 1989; 41: 268–76.Google Scholar
66Eppig, J. Maintenance of meiotic arrest and the induction of oocyte maturation in mouse oocyte-granulosa cell complexes developed in vitro from preantral follicles. Biol Reprod 1991; 45: 824–30.CrossRefGoogle ScholarPubMed
67Eppig, JJ, Schroeder, AC, van de Sandt, JJM, Ziomek, CA, Bavister, BD. Developmental capacity of mouse oocytes that grow and mature in culture: the effect of modification of the protocol. Theriogenology 1990; 33: 89100.Google Scholar
68Eppig, JJ, Wigglesworth, K, O'Brien, MJ. Comparison of embryonic developmental competence of mouse oocytes grown with and without serum. Mol Reprod Dev 1992; 32: 3340.Google Scholar
69Schroeder, AC, Schultz, RM, Kopf, GS, Taylor, GR, Bicker, RB, Eppig, JJ. Fetuin inhibits zona hardening and conversion of ZP2 to ZP2f during spontaneous mouse oocyte maturation in vitro in the absence of serum. Biol Reprod 1990; 43: 891–97.Google Scholar
70Hirao, Y, Miyano, T, Kato, S. Fertilization of in vitro grown mouse oocytes. Theriogenology 1990; 34: 1071–77.Google Scholar
71Canipari, R, Palombi, F, Riminucci, M, Mangia, F. Early programming of maturation competence in mouse oogenesis. Dev Blol 1984; 102: 519–24.CrossRefGoogle ScholarPubMed
72Diggers, JD, Whittingham, DG, Donahue, RP. The pattern of energy metabolism in the mouse oocyte and zygote. Proc Nati Acad Sci USA 1967; 58: 560–67.Google Scholar
73Brinster, RL. Oxidation of pyruvate and glucose by oocytes of the mouse and Rhesus monkey. J Reprod Fertil 1971; 24: 157–91.Google Scholar
74Hardy, K, Hooper, MAK, Handyside, AH, Rutherford, AJ, Winston, RML, Leese, HJ. Non-invasive measurement of pyruvate and glucose uptake by individual human oocytes and preimplantation embryos. Hum Reprod 1989; 4: 188–91.Google Scholar
75Donahue, RP, Stern, S. Follicular cell support of oocyte maturation. Production of pyruvate in vitro. J Reprod Fertil 1968; 17: 395–98.Google Scholar
76Bachvarova, R, Baran, MM, Tejblum, A. Development of naked growing mouse oocytes in vitro. J Exp Zool 1980; 211: 159–69.Google Scholar
77Downs, SM, Schroeder, AC, Eppig, JJ. Developmental capacity of mouse oocytes following maintenance of meiotic arrest in vitro. Gamete Res 15: 305–16.Google Scholar
78Masui, Y, Clarke, HJ. Oocyte maturation. Ini Rev Cytol 1979; 57: 186282.Google Scholar
79Moor, RM, Crosby, IM. Protein requirements for germinal vesicle breakdown in ovine oocytes. J Embryol Exp Morph 1986; 94: 207220.Google Scholar
80Motlik, J, Croset, N, Fulka, J. Meiotic competence in vitro of pig oocytes isolated from early antral follicles. J Reprod Fertil 1984; 72: 323–28.Google Scholar
81Moor, RM, Mattioli, M, Ding, J, Nagai, T. Maturation of pig oocytes in vivo and in vitro. J Reprod Fertil 1990; 40 (suppl): 197210.Google Scholar
82Thibault, C, Szollosi, D, Gerard, M. Mammalian oocyte maturation. Reprod Nutr Dev 1987; 27: 865–96.CrossRefGoogle ScholarPubMed
83Rabahi, F, Monniaux, D, Pisselet, C, Durand, P. Control of in vitro maturation of bovine cumulus-oocyte complex by preovulatory granulosa cells. Mol Reprod Dev 1993; 34: 431–42.CrossRefGoogle ScholarPubMed
84Cha, KY, Koo, JJ, Ko, JJ, Choi, DH, Han, SY, Yoon, TK. Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil Steril 1991; 55: 109–13.Google Scholar
85Thibault, C. Are follicular maturation and oocyte maturation independent processes? J Reprod Fertil 1977;51: 115.Google Scholar
86Schroeder, AC, Eppig, JJ. The development capacity of mouse oocytes that matured spontaneously in vitro is normal. Dev Biol 1984; 102: 493–97.CrossRefGoogle Scholar
87Vanderhyden, BC, Armstrong, DT. Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol Reprod 1989; 40: 720–28.Google Scholar
88Staigmiller, RB, Moor, RM. Effect of follicle cells on the maturation and developmental competence of ovine oocytes matured outside the follicle. Gamete Res 1984; 9: 221–29.Google Scholar
89Yoshida, M, Ishizaki, Y, Kawagishi, H. Blastocyst formation by pig embryos resulting from in vitro fertilization of oocytes matured in vitro. J Reprod Fertil 1990; 88: 18.Google Scholar
90Goto, K, Kajihara, Y, Kosaka, S, Koba, M, Nakanishi, Y, Ogawa, K. Pregnancies after co-culture of cumulus cells with bovine embryos derived from in vitro fertilization of in vitro matured follicular oocytes. J Reprod Fertil 1988; 83: 753–58.Google Scholar
91Johnston, LA, Donaghue, AM, O'Brien, SJ, Wildt, DE. Rescue and maturation of follicular oocytes collected from nondomestic felid species. Biol Reprod 1991; 45: 898906.Google Scholar
92Qvist, R, Blackwell, LF, Bourne, H, Brown, JB. Development of mouse ovarian follicles from primary to preovulatory stages in vitro. J Reprod Fertil 1990; 89: 169–80.Google Scholar
93Nayudu, PL, Osborn, SM. Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. J Reprod Fertil 1992; 95: 349–62.CrossRefGoogle ScholarPubMed
94Boland, NI, Humpherson, PG, Leese, HJ, Gosden, RG. The pattern of laclate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro. Biol Reprod 1993; 48: 798806.Google Scholar
95Peters, H. The development of the mouse ovary from birth to maturity. Acta Endocrinol 1969; 62: 98116.Google Scholar
96Brown, JB. Pituitary control of ovarian function –concepts derived from gonadotrophin therapy. Aust N Z J Obstet Gynaecol 1978; 18: 4754.Google Scholar
97Hillier, SG. Regulation of follicular oestrogen biosynthesis: a survey of current concepts. J Endocrinol 1981; 89 (suppl): 319.Google Scholar
98Hillier, SG. Sex steroid metabolism and follicular development in the ovary. In: Clark, JR ed. Oxford reviews of reproductive biology, Volume 7. Oxford: Clarendon Press, 1985: 168222.Google Scholar
99Daniel, SAJ, Armstrong, DT. Androgens in the ovarian microenvironment. Semin Reprod Endocrinol 1986; 4: 89100.CrossRefGoogle Scholar
100Boland, NI. Experimental investigation of follicle development in mammalian ovaries [Thesis]. Edinburgh: University of Edinburgh, 1992.Google Scholar
101Hoff, JF, Quigley, ME, Yen, SSC. Hormonal dynamics at mid-cycle: a re-evaluation. J Clin Endocrinol Metab 1983; 57: 792–96.Google Scholar
102Oliver, JE, Aitman, TJ, Powell, JF, Wilson, CA, Clayton, RN. Insulin-like growth factor I gene expression in the rat ovary is confined to the granulosa cells of developing follicles. Endocrinology 1989; 124: 2671–79.Google Scholar
103Mattison, DR, Thorgeirsson, SS. Smoking and industrial pollution and their effects on menopause and ovarian cancer. Lancet 1978; i: 187–88.Google Scholar
104Lambertson, CJ, Greenbaum, DF, Wright, KH, Wallach, EE. In vitro studies of ovulation in the perfused rabbit ovary. Fertil Steril 1976; 27: 178–87.Google Scholar
105Koos, RD, Jaccarino, FJ, Magaril, RA, Le Maire, WJ. Perfusion of the rat ovary in vitro: methodology, induction of ovulation, and pattern of steroidogenesis. Biol Reprod 1984; 30: 1135–41.Google Scholar
106Moor, RM, Hay, MF, Mclntosh, JEA, Caldwell, BV. Effect of gonadotrophins on the production of steroids by sheep ovarian follicles cultured in vitro. J Endocrinol 1973; 58: 599611.Google Scholar
107Baker, TG, Hunter, RHF, Neal, P. Studies on the maintenance of porcine Graafian follicles in organ culture. Experientia 1975; 31: 133–5.Google Scholar
108Tsafriri, A, Lindner, HR, Zor, U, Lamprecht, SA. In vitro induction of meiotic maturation in follicle-enclosed rat oocytes by LH, cyclic AMP and prostaglandin E2. J Reprod Fertil 1972; 31: 3950.CrossRefGoogle Scholar
109Lindner, HR, Tsafriri, A, Lieberman, ME et al. Gonadotrophin action on cultured Graafian follicles: induction of maturation division of the mammalian oocyte and differentiation of the luteal cell. Rec Prog Horm Res 1974; 30: 79138.Google ScholarPubMed
110Nilsson, L. Acute effects of gonadotrophins and prostaglandins on the metabolism of isolated ovarian follicles from PMSG-treated immature rats. Acta Endocrinol 1974; 77: 540–58.Google Scholar
111Chen, C. Pregnancy after human oocyte cryopreservation. Lancet 1986; i: 884–86.Google Scholar
112Van Uem, JFHM, Siebzehnrubl, ER, Shuh, B et al. Birth after cryopreservation of unfertilized oocytes. Lancet 1987: i: 752–53.Google Scholar
113Pickering, SJ, Johnson, MH. The influence of cooling on the organization of the meiotic spindle of the mouse oocyte. Hum Reprod 1987; 2: 207–16.Google Scholar
114Glenister, PH, Wood, MJ, Kirby, C, Whittingham, DG. Incidence of chromosome anomalies in first cleavage mouse embryos obtained from frozen-thawed oocytes fertilized in vitro. Gamete Res 1987; 16: 205–16.Google Scholar
115Carroll, J, Warnes, G, Matthews, C. Increase in digyny explains polyploidy after in vitro fertilization of frozen-thawed mouse oocytes. J Reprod Pert 1989; 85: 489–94.Google Scholar
116Carroll, J, Wood, MJ, Whittingham, DG. Normal fertilization and development of frozen-thawed mouse oocytes: protective action of certain macro-molecules. Biol Reprod 1993;48: 606–12.Google Scholar
117Carroll, J, Depypere, H, Matthews, CD. Freeze-thaw-induced changes in the zona pellucida explains decreased rates of fertilization in frozen-thawed mouse oocytes. J Reprod Fertil 1990; 90: 547–53.Google Scholar
118Carroll, J, Whittingham, DG, Wood, MJ, Telfer, E, Gosden, RG. Extraovarian production of mature viable mouse oocytes from frozen primary follicles. J Reprod Fertil 1990; 90: 321–27.Google Scholar
119Carroll, J, Gosden, RG. Transplantation of frozen-thawed mouse primordial ovarian follicles. Hum Reprod 1993; 8: 1163–67.Google Scholar
120Schroeder, AC, Champlin, AK, Morbraaten, LE, Eppig, JJ. Developmental capacity of mouse oocytes cryopreserved before and after maturation in vitro. J Reprod Fertil 1990; 89: 4350.Google Scholar