Hostname: page-component-5c6d5d7d68-pkt8n Total loading time: 0 Render date: 2024-08-19T05:58:09.810Z Has data issue: false hasContentIssue false

The development of new embryo-based biotechnology procedures to aid reproductive function in cattle

Published online by Cambridge University Press:  27 February 2018

M.P. Boland
Affiliation:
University College Dublin, Ireland, Belfield, Dublin 4
P. Lonergan
Affiliation:
University College Dublin, Ireland, Belfield, Dublin 4
J.M. Sreenan
Affiliation:
Teagasc, Athenry, Co. Galway, Ireland
Get access

Abstract

Fertility in dairy cows has decreased during the past 50 years and current management procedures have done little to rectify this situation. Following intense selection for increased milk production, there are significantly more problems in establishing pregnancy at the appropriate time. In recent years, major strides have been made in the development of new embryo-based biotechnologies, including in vitro embryo production, ovum pick-up, cryopreservation of gametes and embryos, cloning and sexing of gametes. The objectives of this paper are to review current progress relating to embryo-based technologies in cattle.

Type
Invited Papers
Copyright
Copyright © British Society of Animal Science 2001

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

Aktas, H., Wheeler, M.B., Rosenkrans, C.F. Jr, First, N.L., Leibfried-Rutledge, M. L. 1996. Maintenance of bovine oocytes in prophase of meiosis I by high [cAMP]i. Journal of Reproduction and Fertility 105: 227235 Google Scholar
Armstrong, D.T., Kotaras, P.J., Earl, C.R. 1997. Advances in production of embryos in vitro from juvenile and prepubertal oocytes from the calf and lamb. Reproduction Fertility and Development 9: 333339 CrossRefGoogle ScholarPubMed
Avery, B., Madison, V., Greve, T. 1991. Sex and development in bovine in-vitro fertilized embryos. Theriogenology 35: 953963 CrossRefGoogle ScholarPubMed
Avery, B., Hay-Schmidt, A., Hyttel, P., Greve, T. 1998. Embryo development, oocyte morphology, and kinetics of meiotic maturation in bovine oocytes exposed to 6-dimethylaminopurine prior to in vitro maturation. Molecular Reproduction and Development 50: 334344 Google Scholar
Behboodi, E., Anderson, G.B., Bon Durant, R.H., Cargill, S.L., Kreuscheir, B.R., Medrano, J.F., Murray, J.D. 1995. Birth of large calves that developed from in vitro-derived bovine embryos. Theriogenology 44: 227232 CrossRefGoogle ScholarPubMed
Blondin, P., Sirard, M.A. 1995. Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Molecular Reproduction and Development 41: 5462 CrossRefGoogle ScholarPubMed
Bols, P.E.J., Van Soom, A., Ysebaert, M.T., Vandenheede, J.M.M., de Kruif, A. 1996. Effects of aspiration vacuum and needle diameter on cumulus oocyte complex morphology and development capacity of bovine oocytes. Theriogenology 45: 10011014 Google Scholar
Bols, P.E.J., Ysebaert, M.T., Van Soom, A., de Kruif, A. 1997. Effect of needle tip bevel and aspiration procedure on the morphology and developmental capacity of bovine compact cumulus oocyte complexes. Theriogenology 47: 12211236 Google Scholar
Booth, P.J., Vajta, G., Hoj, A., Holm, P., Jacobsen, H., Greve, T., Callesen, H. 1999. Full-term development of nuclear transfer calves produced from open-pulled straw (OPS) vitrified cytoplasts: work in progress. Theriogenology 51: 9991006 CrossRefGoogle ScholarPubMed
Bredbacka, P., Kankaanpaa, A., Peippo, J. 1995. PCR-sexing of bovine embryos: a simplified protocol. Theriogenology 44: 167176 Google Scholar
Brackett, B.G., Bousquet, D., Boice, M.L., Donawick, W.J., Evans, J.F., Dressel, M.A. 1982. Normal development following in vitro fertilization in the cow. Biology of Reproduction 27: 147158 Google Scholar
Bungartz, L., Niemann, H. 1993. Effects of a dominant follicle on ovarian responses of dairy cows following various superovulatory treatment schedules. Theriogenology 39: 198 Google Scholar
Butler, W.R., Callaman, J.J., Bean, S.W. 1996. Plasma and milk urea nitrogen in relation to pregnancy rate in lactating dairy cattle. Journal of Animal Science 74: 850865 CrossRefGoogle ScholarPubMed
Carvalho, R.V., Del Campo, M.R., Palasz, A.T., Plante, Y., Mapletoft, R.J. 1996. Survival rates and sex ratio of bovine IVF embryos frozen at different developmental stages on day 7. Theriogenology 45: 489498 Google Scholar
Cibelli, J.B., Stice, S.L., Golueke, P.J., Kane, J.J., Jerry, J., Blackwell, C, Ponce de Leon, F.A., Robl, J.M. 1998. Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science 280: 12561258 CrossRefGoogle ScholarPubMed
Collas, P., Barnes, F.L. 1994. Nuclear transplantation by microinjection of inner cell mass and granulosa cell nuclei. Molecular Reproduction and Development 38: 264267.CrossRefGoogle ScholarPubMed
Cortvrindt, R., Smitz, J., Van Steirteghem, A.C. 1996. In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Human Reproduction 11: 26562666 Google Scholar
Cran, D.G., Johnson, L.A., Miller, N.G., Cochrane, D., Polge, C. 1993. Production of bovine calves following separation of X- and Y-chromosome bearing spermatozoa and in vitro fertilisation. Veterinary Record 139: 494495 Google Scholar
Cran, D.G., Johnson, L.A., Polge, C. 1995. Sex selection in cattle: a field trial. Veterinary Record 132: 4041 Google Scholar
Damiani, P., Fissore, R.A., Cibelli, J.B., Robl, J.M., Duby, R.T. 1996. Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes. Molecular Reproduction and Development 45: 521-34Google Scholar
De Loos, F., Zeinstra, E., Bevers, M.M. 1994. Follicular wall maintains meiotic arrest in bovine oocytes cultured in vitro . Molecular Reproduction and Development 39: 162165 Google Scholar
Dinnyes, A., Dai, Y., Jiang, S., Yang, X. 1999. Solid surface vitrification (SSV) of matured bovine oocytes to generate parthenogenetic, in vitro fertilized, and somatic-cell nuclear transfer embryos. Molecular Reproduction and Development (in press)Google Scholar
Eppig, J.J., 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 Google Scholar
Eppig, J.J., O'Brien, M.J. 1996. Development in vitro of mouse oocytes from primordial follicles. Biology of Reproduction 54: 197200 Google Scholar
Eyestone, W.H. 1999. Production and breeding of transgenic cattle using in vitro embryo production technology. Theriogenology 51: 509517 Google Scholar
Fahey, J., Boland, M.P., O'Callaghan, D. 1998. Effect of dietary urea on embryo development in superovulated donor ewes and on embryo survival following transfer in recipient ewes. Proceedings of the Annual Meeting of the British Society for Animal Science, Abstract 182CrossRefGoogle Scholar
Foote, R.H. 1977. Sex ratios in cattle under various conditions. Theriogenology 8: 349356 CrossRefGoogle Scholar
Fouladi-Nashta, A.A., Waddington, D., Campbell, K.H.S. 1998. Maintenance of bovine oocytes in meiotic arrest and subsequent development in vitro: a comparative evaluation of antral follicle culture with other methods. Biology of Reproduction 59: 255262 Google Scholar
Fulka, J. Jr, Leibfried-Rutledge, M.L., First, N.L. 1991. Effect of 6-dimethylaminopurine on germinal vesicle breakdown of bovine oocytes. Molecular Reproduction and Development 29: 379384 Google Scholar
Gath, V., Lonergan, P., Boland, M.P., O'Callaghan, D. 1999. Effects of diet type on establishment of pregnancy and embryo development in beef heifers. Theriogenology 51: 224 Google Scholar
Gordon, I. 1983. Controlled breeding inform animals. Pergamon PressGoogle Scholar
Gordon, I. 1994. Laboratory production of cattle embryos. CAB International, University Press, Cambridge Google Scholar
Gordon, I. 1996. Controlled Reproduction in Cattle and Buffaloes. CAB International, University Press, Cambridge Google Scholar
Gordon, I., Boland, M.P., McGovern, H., Lynn, G. 1987. Effect of season on superovulatory responses and embryo quality in Holstein cattle in Saudi Arabia. Theriogenology 27: 231 Google Scholar
Hasler, J.F., Hurtgen, P.J., Jin, Z.Q., Stokes, J.E. 1997. Survival of IVF-derived bovine embryos frozen in glycerol or ethylene glycol. Theriogenology 48: 563579 CrossRefGoogle ScholarPubMed
Hasler, J.F. 1998. The current status of oocyte recovery in vitro embryo production and embryo transfer in domestic animals with an emphasis on the bovine. Journal of Animal Science 1998, 76 (Suppl.3): 5274 Google Scholar
Holm, P., Walker, S.K., Seamark, R.F. 1996. Embryo viability, duration of gestation and birthweight in sheep after transfer of in vitro matured and in vivo fertilized zygotes cultured in vitro or in vivo. Journal of Reproduction and Fertility 107: 175181 Google Scholar
Imai, K., Nagai, T., Kobayashi, S., Tsujino, T., Kojima, T. 1999. Effects of butyrolactone-1 on GVBD in bovine oocytes and their subsequent maturation, fertilization and development in vitro . Theriogenology 51: 377 CrossRefGoogle Scholar
Johnson, L.A. 1997. Advances in gender selection in swine. Journal of Reproduction and Fertility Supplement 52: 255266 Google Scholar
Khatir, H., Lonergan, P., Carolan, C, Mermillod, P. 1996. Prepubertal bovine oocyte: a negative model for studying oocyte developmental competence. Molecular Reproduction and Development 45: 231239 Google Scholar
King, K.K., Seidel, G.E., Elsden, R.P. 1985. Bovine embryo transfer pregnancies. 1. Abortion rates and characteristics of calves. Journal of Animal Science 61: 747762 CrossRefGoogle ScholarPubMed
Kotsuji, F., Kubo, M., Tominaga, T. 1994. Effect of interactions between granulosa and thecal cells on meiotic arrest in bovine oocytes. Journal of Reproduction and Fertility 100: 151156 Google Scholar
Kubota, C, Yang, X., Dinnyes, A., Todoroki, J., Yamakuchi, H., Mizoshita, K., Inohae, S., Tabara, N. 1998. In vitro and in vivo survival of frozen-thawed bovine oocytes after IVF, nuclear transfer and parthenogenetic activation. Molecular Reproduction and Development 51: 281286.Google Scholar
Lazzari, G., Duchi, R., Landriscina, R, Colombo, N., Galli, C. 1996. Developmental capacity of IVM-IVF calf oocytes from eCG stimulated donors of 2-3 months of age. Journal of Reproduction and Fertility, Abstract Series 17: 41 Google Scholar
Levesque, J.T., Sirard, M.A. Effects of different kinases and phosphatases on nuclear and cytoplasmic maturation of bovine oocytes. Molecular Reproduction and Development 42: 114121 Google Scholar
Leibo, S.P. 1984 A one-step method for the direct non-surgical transfer of frozen-thawed bovine embryos. Theriogenology 21: 767790 Google Scholar
Lim, J.M., Fukui, Y., Ono, H. 1992. Developmental competence of bovine oocytes frozen at various maturation stages followed by in vitro maturation and fertilization. Theriogenology 37: 351361.Google Scholar
Lohuis, M.M. 1995. Potential benefits of bovine embryo manipulation technologies to genetic improvement programs. Theriogenology 43: 5160.Google Scholar
Lonergan, P., Monaghan, P., Rizos, D., Boland, M.P., Gordon, I. 1994. Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization and culture in vitro . Molecular Reproduction and Development 37: 4853.Google Scholar
Lonergan, P., Khatir, H., Carolan, C, Mermillod, P. 1997. Bovine blastocyst production in vitro after inhibition of meiotic resumption for 24 h. Journal of Reproduction and Fertility 109: 355365.Google Scholar
Lonergan, P., Khatir, H., Piumi, F., Rieger, D., Humblot, P., Boland, M.P. 1999. Effect of time interval from insemination to first cleavage on the developmental characteristics, sex and pregnancy rates following transfer of bovine preimplantation embryos. Journal of Reproduction and Fertility 117: 159167 Google Scholar
Lopez-Gatius, F., Camon-Urgel, J. 1988. Increase of pregnancy rate in dairy cattle after preovulatory follicle palpation and deep cornual insemination. Theriogenology, 45: 417425 Google Scholar
Martino, A., Songansen, N., Leibo, S.P. (1996a) Development into blastocysts of bovine oocytes cryopreserved by ultra-rapid cooling of very small samples. Biology of Reproduction 54: 10591069 Google Scholar
Martino, A., Pollard, J., Leibo, S.P. (1996b) Effect of chilling bovine oocytes on their developmental competence. Molecular Reproduction and Development 45: 503512 3.0.CO;2-X>CrossRefGoogle ScholarPubMed
McKenna, T., Lenz, R.W., Fenton, S.E., Ax, R.L. 1990. Nonreturn rates of dairy cattle following uterine body or cornual insemination. Journal of Dairy Science 73: 17791783 Google Scholar
Mihm, M., Baguisi, A., Boland, M.P., Roche, J.F. 1994. Association between the duration of dominance of the ovulatory follicle and pregnancy rate in beef heifers. Journal of Reproduction and Fertility 102: 123130 Google Scholar
Motlik, J. 1998. Interplay between CDC2 kinase and MAP kinase pathway during maturation of mammalian oocytes. Theriogenology 49: 461469 Google Scholar
Murray, J.D. 1999. Genetic modification of animals in the next century Theriogenology 51: 149159 Google Scholar
Niemann, H. 1991. Cryopreservation of ova and embryos from livestock: current status and research needs. Theriogenology 35: 109124 Google Scholar
Nolan, R, O'Callaghan, D., Duby, R.T., Lonergan, P., Boland, M.P. 1998. Influence of short-term nutrient changes on follicle growth and embryo production following superovulation in beef heifers. Theriogenology 50: 12631274.Google Scholar
Osaki, S., Matsumura, K., Yamamoto, K., Miyano, T., Miyake, M., Kato, S. 1997. Fertilization of bovine oocytes grown in vitro . Reproduction Fertility Development: 781787.Google Scholar
Oussaid, B., Lonergan, P., Khatir, H., Monniaux, D., , Beckers, J.F., Cognie, Y., Mermillod, P. 1999. Effect of GnRH antagonist-induced prolonged follicular phase on follicular atresia and oocyte developmental competence in superovulated heifers. Journal of Reproduction and Fertility (in press).Google Scholar
Palasz, A.T., Mapletoft, R. J. 1996. Cryopreservation of mammalian embryos and oocytes: recent advances. Biotechnology Advances 14: 127149 Google Scholar
Pieterse, M.C., Kappen, K.A., Kruip, T.A.M., Taverne, M.A.M. 1991. Transvaginal ultrasound guided follicular aspiration of bovine oocytes. Theriogenology 35: 1924.Google Scholar
Pollard, J.W., Leibo, S.P. 1994. Chilling sensitivity of mammalian embryos. Theriogenology 41: 101106 Google Scholar
Qvist, R., Blackwell, L.F., Bourne, H., Brown, J.B. 1990. Development of mouse ovarian follicles from primary to preovulatory stages in vitro . Journal of Reproduction and Fertility 89: 169180 CrossRefGoogle ScholarPubMed
Rall, W.F., Wood, M.J. 1992. High in vitro and in vivo survival of day 3 mouse embryos vitrified or frozen in a non-toxic solution of glycerol and albumin. Journal of Reproduction and Fertility 101: 681688 CrossRefGoogle Scholar
Reichenbach, H.D., Liebrich, J., Berg, U., Brem, G. 1992. Pregnancy rates and births after unilateral or bilateral transfer of bovine embryos produced in vitro . Journal of Reproduction and Fertility 95: 363370 Google Scholar
Reinders, J.M.C., Wurth, Y.A., Kruip, T.A.M. 1995. From embryo to calf after transfer of in vitro produced bovine embryos. Theriogenology 43: 306 Google Scholar
Rens, W., Welch, G.R., Johnson, L.A. 1999. Improved flow cytometric sorting of X- and Y-chromosome bearing sperm: substantial increase in yield of sexed semen. Molecular Reproduction and Development 52: 5056 Google Scholar
Revel, F., Mermillod, P., Peynot, N., Renard, J.P., Heyman, Y. 1995. Low developmental capacity of in vitro matured and fertilized oocytes from calves compared to that of cows. Journal of Reproduction and Fertility 103: 115120 Google Scholar
Richard, F.J., Sirard, M.A. 1996a. Effects of follicular cells on oocyte maturation II: thecal cell inhibition of bovine oocyte maturation in vitro . Biology of Reproduction 54: 2228 Google Scholar
Richard, F.J., Sirard, M.A. 1996b. Effects of follicular cells on oocyte maturation I: effects of follicular hemisections on bovine oocyte maturation in vitro. Biology of Reproduction 54: 1621 Google Scholar
Rieger, D. 1984. The measurement of metabolic activity as an approach to evaluating viability and diagnosing sex in early embryos. Theriogenology 21: 138149 Google Scholar
Robl, J.M. 1999. Development and application of technology for large scale cloning of cattle. Theriogenology 51: 499508 Google Scholar
Schellender, K., Peli, J., Schmoll, F., Brem, G. 1994 Effects of different cryoprotectants and carbohydrates on freezing of matured and unmatured bovine oocytes. Theriogenology 42: 909915 Google Scholar
Seidel, G.E., Allen, C.H., Johnson, L.A., Holland, M.D., Brink, Z., Welch, G.R., Graham, J.K., Cattell, M.B. 1997. Uterine insemination of heifers with very low numbers of nonfrozen and sexed spermatozoa. Theriogenology 48: 12551264 CrossRefGoogle Scholar
Senger, P.J., Becker, W.C., Davidge, S.T., Hillers, J.K., Reeves, J.J. 1988. Influence of cornual insemination on conception in cattle. Journal of Animal Science 66: 30103016 Google Scholar
Shea, B.F. 1999. Determining the sex of bovine embryos using polymerase chain reaction results: a six-year retrospective study. Theriogenology 51: 841854 Google Scholar
Sinclair, K.D., Dunne, L.D., Maxfield, E.K., Maltin, C.A., Young, L.E., Wilmut, I., Robinson, J.J., Broadbent, P.J. 1998. Fetal growth and development following temporary exposure of day-3 ovine embryos to an advanced uterine environment. Reproduction Fertility and Development 10: 263269 CrossRefGoogle Scholar
Sinclair, K.D., McEvoy, T.G., Maxfield, E.K., Maltin, C.A., Young, L.E., Wilmut, I., Broadbent, P.J., Robinson, J.J. 1999. Aberrant fetal growth and development after in vitro culture of sheep zygotes. Journal of Reproduction and Fertility 116: 177186 Google Scholar
Sirard, M.A. 1990. Temporary inhibition of meiosis resumption in vitro by adenylate cyclase stimulation in immature bovine oocytes. Theriogenology 33: 757767 Google Scholar
Sirard, M.A., Bilodeau, S. 1990. Granulosa cells inhibit the resumption of meiosis in bovine oocytes in vitro . Biology of Reproduction 43: 777783 Google Scholar
Sirard, M.A., Picard, L., Dery, M., Coenen, K., Blondin, P. 1999. The time interval between FSH administration and ovarian aspiration influences the development of cattle oocytes. Theriogenology 51: 699708 Google Scholar
Stice, S.L., Keefer, CL. 1993. Multiple generation bovine embryo cloning. Biology of Reproduction 48: 715719 Google Scholar
Telfer, E.E. 1996. The development of methods for isolation and culture of preantral follicles from bovine and porcine ovaries. Theriogenology 45: 101110 Google Scholar
Telfer, E.E., Webb, R., Moor, R.M., Gosden, R.G. 1999. New approaches to increasing oocyte yield from ruminants. Animal Science 68: 285298 Google Scholar
Thibier, M., Nibart, M. 1995. The sexing of bovine embryos in the field. Theriogenology 43: 7180 Google Scholar
Thompson, J.G., Gardner, D.K., Pugh, P.A., McMillan, W.H., Tervit, H.R. 1995. Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biology of Reproduction 53: 13851391 Google Scholar
Ushijima, H., Yamakawa, H., Nagashima, H. 1999. Cryopreservation of bovine pre-morula stage in vitro matured/in vitro fertilized embryos after delipidation and before use in nucleus transfer. Biology of Reproduction 60: 534539 Google Scholar
Utsumi, K., Iritani, A. 1993. Embryo sexing by male specific antibody and by PCR using male specific (SRY) primer. Molecular Reproduction and Development 36: 238241 CrossRefGoogle ScholarPubMed
Van Soom, A., de Kruif, A. 1996. Oocyte maturation, sperm capacitation and pre-implantation development in the bovine: implications for in vitro production of embryos. Reproduction in Domestic Animal 31: 687701 CrossRefGoogle Scholar
Van Wagtendonk-de Leeuw, A.M., den Daas, J.H.G, Kruip, T.A.M., Rail, W.F. 1995. Comparison of the efficacy of conventional slow freezing and rapid cryopreservation methods for bovine embryos. Cryobiology 32: 157167 Google Scholar
Van Wagtendonk-de Leeuw, A.M., den Daas, J.H.G., Rail, W.F. 1997. Field trial to compare pregnancy rates of bovine embryo cryopreservation methods: vitrification and one-step dilution versus slow freezing and three-step dilution. Theriogenology 48: 10711084 Google Scholar
Vajta, G., Booth, P.J., Holm, P., Greve, T., Callesen, H. 1997. Successful vitrification of early stage bovine in vitro produced embryos with the open pulled straw (OPS) method. Cryo-letters 18: 191195 Google Scholar
Vajta, G., Holm, P., Kuwayama, M., Booth, P.J., Jacobsen, H., Greve, T., Callesen, H. 1998. Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Molecular Reproduction and Development 51: 3558 Google Scholar
Voelkel, S.A., Hu, Y.X. 1992. Direct transfer of frozen-thawed bovine embryos. Theriogenology 37: 687697 Google Scholar
Walker, S.K., Hartwich, K.M., Seamark, R.F. 1996. The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenology 45: 111120 Google Scholar
Wandji, S.A., Srsen, V., Voss, A.K., Eppig, J.J., Fortune, J.E. 1996. Initiation in vitro of growth of bovine primordial follicles. Biology of Reproduction 55: 942948 Google Scholar
Ward, F.A., Enright, B.P., Lonergan, P., Boland, M.P. 1999. Ovum pick-up (OPU): Effect of aspiration vacuum on cumulus oocyte complex morphology and oocyte developmental capacity. 15th Annual Meeting of the European Embryo Transfer Society, Lyon Google Scholar
Webb, R., Gosden, R.G., Telfer, E.E., Moor, R.M. 1999. Factors affecting folliculogenesis in ruminants. Animal Science 68: 257284 Google Scholar
Wells, D.N., Misica, P.M., Tervit, H.R. 1999. Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biology of Reproduction 60: 9961005 Google Scholar
White, K.L., Anderson, G.B., BonDurant, R.H. 1987. Expression of a male specific factor on various stages of preimplantation bovine embryos. Biology of Reproduction 37: 867873 Google Scholar
Williams, T.J. 1986. A technique for sexing mouse embryos by a visual colorimetric assay of the X-linked enzyme, glucose-6-phosphate dehydrogenase. Theriogenology 25: 733739 Google Scholar
Winterberger-Torres, S., Popescu, C. 1980. Transfer of cow blastocysts after sexing. Theriogenology 14: 309318 Google Scholar
Wilmut, I., Rowson, L.E.A. 1973. Experiments on the low temperature preservation of cow embryos. Veterinary Record 92: 686690 Google Scholar
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J., Campbell, K.H.S. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature 385: 810813 Google Scholar
Wrenzycki, C, Hermann, D., Carnwath, J.W., Niemann, H. 1996. Expression of the gap junction gene connexin 43 (Cx43) in preimplantation bovine embryos derived in vitro or in vivo. Journal of Reproduction and Fertility 108: 1724 Google Scholar
Young, L.E., Sinclair, K.D., Wilmut, I. 1998. Large offspring syndrome in cattle and sheep. Reviews of Reproduction 3: 155163.Google Scholar