Skip to main content
Download PDF
  • Published:

Growth of Preimplatation Bovine Embryos

Acta Veterinaria Scandinavica volume 35, pages 307–320 (1994)Cite this article

Abstract

Development of mammalian embryos in vitro is functionally and temporally inferior to embryo development as it occurs inside the female reproductive tract. The deficiencies of cultured embryos range from slow cleavage rates to complete developmental arrests or blocks, occurring at particular stages in many species. A variety of approaches have been used to overcome the blocks, including most extensively the coculture of preimplantation embryos with various somatic cells. However, even with coculture, development of embryos in vitro is still not equivalent to that in vivo. In most laboratories, only 25–40% of inseminated oocytes develop into morulae and blastocysts in spite of numerous variations on the basic technique. A better understanding of the factors governing embryonic growth is required before we can hope to achieve results comparable with those occurring in vivo.

Sammendrag

In vitro utvikling av pattedyrembryo er både funksjonelt og tidsmessig dårligere enn embryo som utvikler seg naturlig i de hunnlige kjønnsveier. Manglene ved dyrkede embryoner varierer fra lav delingshastighet til fullstendig delingsstopp, som inntrer på bestemte stadier hos mange arter. Forskjellige metoder har blitt brukt for å forhindre denne såkalte blokkering, inklusive kultur av embryo med forskjellige somatiske celler. Til tross for bruk av slike systemer er in vitro utvikling av embryo forsatt ikke sammenlignbart med in vivo utvikling. Til tross for en rekke variasjoner i de benyttede teknikker flater nivået av utviklede morulae/blastocyster ved 25–40% av inseminerte oocytter i de fleste laboratorier. Det kreves en bedre forståelse av faktorene som styrer embryoets vekst før vi kan håpe å oppnå resultater som kan sammenlignes med forhold in vivo.

References

  • Aoyagi Y, Fukui Y, Iwazumi Y, Urakama M, Minegishi Y, Ono H Effects of culture system on development of in vitro fertilized bovina ova into blastocysts. Theriogenology 1989, 31, 168.

    Article  Google Scholar 

  • Avery B Impact of asynchronous ovulations on the expression of sex-dependent growth rate in bovine preimplantation embryos J. Reprod. Fert. 1989, 87, 627–631.

    Article  CAS  Google Scholar 

  • Avery B, Madison V, Greve T Sex and development in bovine in vitro fertilized embryos. Theriogenology 1991, 35, 953–963.

    Article  CAS  PubMed  Google Scholar 

  • Barnes FL Characterization of the onset of embryonic control and early development in the bovine embryo. Ph.D. Thesis, University of Wisconsin-Madison 1988.

    Google Scholar 

  • Barnes FL, Eyestone WH Early cleavage and the maternal transition in bovine embryos. Theriogenology 1990, 33, 141–152.

    Article  Google Scholar 

  • Bavister BD, Rose-Hellekant TA, Pinyopummintr T Development of in vitro matured/in vitro fertilized bovine embryos into morulae and blastocysts in defined culture media. Theriogenology 1992, 37, WA46.

    Article  Google Scholar 

  • Berg U, Reichenbach HD, Liebrich J, Brem G Sex ratio of calves born after transfer of in vitro produced embryos. Theriogenology 1992, 37, 191.

    Article  Google Scholar 

  • Betteridge KJ, Flechon JE The anatomy and physiology of preattachment bovine embryos. Theriogenology 1988, 29, 155–187.

    Article  Google Scholar 

  • Camous S, Heyman Y, Meziou W, Menezo Y Cleavage beyond the block stage and survival after transfer of early bovine embryos cultured with trophoblastic vesicles. J. Reprod. Fert. 1984, 72, 479–485.

    Article  CAS  Google Scholar 

  • Canseco RS, Sparks AET, Pearson RE, Gwazdauskas FC Effect of microdrop size and number of embryos per microdrop on early murine embryo development. Serono Symposium on Preimplantation Embryo Development. 1991, Abstract Volume, 29.

    Google Scholar 

  • Crosby IM, Gandolfi F, Moor RM Control of protein synthesis during early cleavage of sheep embryos. J. Reprod. Fert. 1988, 82, 769–775.

    Article  CAS  Google Scholar 

  • Dominiko T, First NL Kinetics of bovine oocyte maturation allows selection for developmental competence and is affected by gonadotropins. Theriogenology 1992, 37, 203.

    Article  Google Scholar 

  • Dubicella T, Anderson P Cell shape and membrane changes in the eight-cell mouse embryo. Prerequisites for morphogenesis of the blastocyst. Dev. Biol. 1975, 47, 45.

    Article  Google Scholar 

  • Duby RT, Dobrinsky JR, Robl JM, Overstrom EW, Boland MP, Bagusi A, Lonergan P, Roche JF Development rate, esterase activity and death of cells in in vitro and in vivo produced bovine embryos. Theriogenology 1993, 39, 210.

    Article  Google Scholar 

  • Eyestone WH, First NL Cell cycle analysis of early bovine embryos. Theriogenology 1988, 29, 243.

    Article  Google Scholar 

  • Eyestone WH, First NL Co-culture of early cattle embryos to the blastocyst stage with oviducal tissue or in conditioned medium. J. Reprod. Fert. 1989, 85, 715–720.

    Article  CAS  Google Scholar 

  • Flood MR, Gage TL, Bunch TD Effect of various growth-promoting factors on preimplantation bovine embryo development in vitro. Theriogenology 1993, 39, 823–833.

    Article  CAS  PubMed  Google Scholar 

  • Frei RE, Schultz GA, Church RB Qualitative and quantitative changes in protein synthesis occur at the 8–16 cell stage of embryogenesis in the cow. J. Reprod. Fert. 1989, 86, 637–641.

    Article  CAS  Google Scholar 

  • Fukui Y, Ono H In vitro development to blastocyst of in vitro matured and fertilized bovine oocytes. Vet. Rec. 1988, 722, 282–283.

    Article  Google Scholar 

  • Fukui Y, McGowan LT, James RW, Pugh PA, Tervit HR Factors affecting the in-vitro development to blastocysts of bovine oocytes matured and fertilized in vitro. J. Reprod. Fert. 1991, 92, 125–131.

    Article  CAS  Google Scholar 

  • Gandolfi F, Brevini TAL, Modina S, Lauria A Detection and characterization of a growth factor in bovine oviduct secretions. J. Reprod. Fert. 1991, Abstract Series 7, Abstract 6.

    Google Scholar 

  • Goto 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. Fert. 1988, 83, 753–758.

    Article  CAS  Google Scholar 

  • Goto K, Kinoshita A, Takuma Y, Ooe N, Ogawa K In vitro development of bovine oocytes collected from ovaries of individual cows after in vitro fertilization. Japan. J. Anim. Reprod. 1990, 36, 110–113.

    Article  Google Scholar 

  • Greve T, Loskutoff NM, Buckrell BC, Christian CR, Leibo SP, Betteridge KJ Morphology and freezing tolerance of in vitro derived bovine embryos after culture in vivo or in vitro. 5eme colloque Franco-Tchecoslovaque sur la reproduction des animaux domistiques. Jouy-en-Josas, France. 1992, 36.

    Google Scholar 

  • Greve T, Avery B, Callesen H Viability of in-vivo and in-vitro produced bovine embryos. Reprod. Dorn. Anim. 1993, 28, 164–169.

    Article  Google Scholar 

  • Hamilton WJ, Laing JA Development of the egg of the cow up to the stage of blastocyst formation. J. Anat. 1946, 80, 194–204.

    PubMed  PubMed Central  Google Scholar 

  • Harvey MB, Kaye PL Insulin stimulates protein synthesis in compacted mouse embryos. Endocrinology 1988, 722, 1182–1184.

    Article  Google Scholar 

  • Harvey MB, Kaye PL Insulin increases the cell number of the inner cell mass and stimulates morphological development of mouse blastocysts in vitro. Development 1990, 110, 963–967.

    CAS  PubMed  Google Scholar 

  • Harvey MB, Kaye PL Mouse blastocysts respond metabolically to short-term stimulation by insulin and IGF-I through the insulin receptor. Mol. Reprod. Dev. 1991, 29, 253–258.

    Article  CAS  PubMed  Google Scholar 

  • Heyman Y, Menezo Y, Chesne P, Camous S, Garnier V In vitro cleavage of bovine and ovine early embryos: improved development using co-culture with trophoblastic vesicles. Theriogenology 1987, 27, 59–68.

    Article  Google Scholar 

  • Heyner S, Rao LV, Jarett L, Smith RM Preimplantation mouse embryos internalize maternal insulin via receptor-mediated endocytosis. Pattern of uptake and functional correlations. Dev. Biol. 1989, 134, 48–58.

    Article  CAS  PubMed  Google Scholar 

  • Hyafil F, Morello D, Babinet C, Jacob F A cell surface glycoprotein involved in embryonal carcinoma cells and cleavage stage embryos. Cell 1980, 27, 927–934.

    Article  Google Scholar 

  • Hyttel P, Greve T, Callesen H Ultrastructure of in vivo fertilization in superovulated cattle. J. Reprod. Fert. 1988, 82, 1–13.

    Article  CAS  Google Scholar 

  • Iwasaki S, Yoshiba N, Ushijima H, Watanabe S, Nakahara T Morphology and proportion of inner cell mass of bovine blastocysts fertilized in-vitro and in-vivo. J. Reprod. Fert. 1990, 90, 279–284.

    Article  CAS  Google Scholar 

  • Jiang HS, Wang WL, Lu KH, Gordon I Effects of PMSG, insulin, osmolarity and oestrous cow serum on development of IVF early bovine embryos cultured on granulosa cell monolayers. Theriogenology 1990, 33, 258.

    Article  Google Scholar 

  • Jiang HS, Wang WL, Lu KH, Gordon I, Polge C Examination of cell numbers of blastocysts derived from IVM, IVF and I VC of bovine follicular oocytes. Theriogenology 1992, 37, 229.

    Article  Google Scholar 

  • Kajihara Y, Kometani N, Kobayashi S, Shitanaka Y, Koshiba Y, Hishiyama K, Shiraiwa K, Goto K Pregnancy rates and births after coculture of cumulus cells with bovine embryos derived from in vitro fertilization of in vitro matured follicular oocytes. Theriogenology 1990, 33, 264.

    Article  Google Scholar 

  • Kajihara Y, Kometani N, Kobayashi S, Shitanaka Y, Goto K Pregnancy by bovine blastocysts developed in coculture with cumulus/uterine endometrial cells after in vitro fertilization. Japan. J. Anim. Reprod. 1991, 37, 177–184.

    Article  Google Scholar 

  • Kane MT Control of growth in preimplantation embryos. Ir. J. Med. Sci. 1990, 160, 17–22.

    Article  Google Scholar 

  • Kane MT, Carney EW, Ellington JE The role of nutrients, peptide growth factors and co-culture cells in the development of preimplantation embryos in vitro. Theriogenology 1992, 38, 297–313.

    Article  CAS  PubMed  Google Scholar 

  • Keefer CL Development of in vitro produced bovine embryos cultured individually in a simple medium: effects of EGF and TGFßl. Theriogenology 1992, 37, 236 (Abs).

    Article  Google Scholar 

  • King WA, Niar A, Chartrian I, Betteridge KJ, Guay P Nucleolus organizer regions and nucleoli in preattachment bovine embryos. J. Reprod. Fert. 1988, 82, 87–92.

    Article  CAS  Google Scholar 

  • Kopecny V, Flechon JE, Camous S, Fulka J, Jr Nucleogenesis and the onset of transcription in the eight-cell bovine embryo: Fine structural and autoradiographic study. Mol. Reprod. Dev. 1989, 7, 79–90.

    Article  Google Scholar 

  • Larson RC, Ignotz GG, Currie WB Transforming growth factor ß and basic fibroblast growth factor synergistically promote early bovine embryo development during the fourth cell cycle. Mol. Reprod. Dev. 1992, 33, 432–435.

    Article  CAS  PubMed  Google Scholar 

  • Leese HJ Metabolism of the preimplantation mammalian embryo. Oxford Rev. Reprod. Biol. 1991, 13, 35–72.

    CAS  Google Scholar 

  • Linares T, King WA Morphological study of the bovine blastocyst with phase contrast microscopy. Theriogenology 1980, 14, 123–133.

    Article  CAS  PubMed  Google Scholar 

  • Lonergan P, Fair T, Gordon I Effect of time of transfer to granulosa cell monolayer and cell stage at 48 hours post-insemination on bovine oocyte development following IVM/IVF/IVC. 8th Scientific Meeting of the European Embryo Transfer Association, Lyon ll-12th September, 1992, 136.

    Google Scholar 

  • Lu KH, Gordon I, Chen HB, Gallagher M, McGovern H Birth of twins after transfer of cattle embryos produced by in vitro techniques. Vet. Rec. 1988, 122, 539–540.

    Article  CAS  PubMed  Google Scholar 

  • Mannaerts BML Cytological parameters for rating bovine embryo quality. Cur. Top. Vet. Med. Anim. Sci. 1986, 34, 216–222.

    Google Scholar 

  • Mermillod P, Boccart C, Wils C, Massip A, Dessy F Effect of oviduct-conditioned medium and of cumulus cells on bovine embryo development in vitro. Theriogenology 1992, 37, 256.

    Article  Google Scholar 

  • Motlik J, Kubelka M Cell-cycle aspects of growth and maturation of mammalian oocytes. Mol. Reprod. Dev. 1990, 27, 366–375.

    Article  CAS  PubMed  Google Scholar 

  • Palma GA, Clement-Sengewald A, Berg U, Brem G Role of the embryo number in the development of in vitro produced bovine embryos. Theriogenology 1992, 37, 271.

    Article  Google Scholar 

  • Paria BC, Dey SK Preimplantation embryo development in vitro: Cooperative interactions among embryos and role of growth factors. Proc. Natl. Acad. Sci. USA 1990, 87, 4756–4760.

    Article  CAS  PubMed  Google Scholar 

  • Picard L, Greve T, King WA, Betteridge KJ, Holm-Jorgensen P Bisection of post-compaction bovine embryos: the difference in viability between the two monozygotic halves. Acta. Vet. Scand. 1986, 27, 33–48.

    CAS  PubMed  Google Scholar 

  • Plante L, King WA Effects of time to first cleavage on hatching rate of bovine embryos in vitro. Theriogenology 1992, 37, 274.

    Article  Google Scholar 

  • Pollard JW, Xu KP, Rorie R, King WA, Betteridge KJ Influence of various oviductal epithelial cell culture on the development of early cleavage bovine embryos in vitro. Theriogenology 1988, 31, 239.

    Article  Google Scholar 

  • Pool SH, Rorie RW, Pendlton RJ, Menino AR, Godke RA Culture of early stage bovine embryos inside day-13 and day-14 precultured trophoblastic vesicles. Anns. New York Acad. Sci. 1988, 541, 407–418.

    Article  CAS  Google Scholar 

  • Quinn R Hirayama T, Marrs RP Cooperative interaction among mouse zygotes cultured in protein- free medium: blastocyst development and hatching. Serono Symposium on Preimplantation Embryo Development 1991, Abstract Vol., 11–35, 68.

    Google Scholar 

  • Rappolee DA, Wang A, Mark D, Werb Z Novel method for studying mRNA phenotypes in single or small numbers of cells. J. Cell Biochem. 1989, 39, 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Rappolee DA, Sturm KS, Schultz GA, Pederson RA, Zerb Z The expression of growth factor ligands and receptors in preimplantation embryos. UCLA Symposia on Molecular and Cellular Biology, New Series 1990, 117, 11–25.

    CAS  Google Scholar 

  • Rieger D Relationships between energy metabolism and development of early mammalian embryos. Theriogenology 1992, 37, 75–93.

    Article  CAS  Google Scholar 

  • Rose TA, Bavister BD Effect of oocyte maturation medium on in vitro development of in vitro fertilized bovine embryos. Mol. Reprod. Dev. 1992, 31, 72–77.

    Article  CAS  PubMed  Google Scholar 

  • Shamsuddin M, Larsson B, Gustafsson H, Gustari S, Bartolome J, Rodriguez-Martinez H Comparative morphological evaluation of in vivo and in vitro produced bovine embryos. 12th International Congress on Animal Reproduction 1992, 3, 1333–1335.

    Google Scholar 

  • Shamsuddin M, Larsson B, Rodriguez-Martinez H Culture of bovine IVM/IVF embryos up to the blastocyst stage in defined medium using insulin, transferrin and selenium or growth factors. Reprod. Dom. Anim. 1993, 28, 209–210.

    Article  Google Scholar 

  • Sirard MA, Lambert RD In vitro fertilization of bovine follicular oocytes obtained by laparoscopy. Biology of Reproduction 1985, 33, 487–494.

    Article  CAS  PubMed  Google Scholar 

  • Smith RKW, Johnson MH Analysis of the third and fourth cell cycles of mouse early development. J. Reprod. Fert. 1986, 76, 393–399.

    Article  CAS  Google Scholar 

  • Tan SJ, Lu KH Effects of different oestrous cycle stages of ovaries and sizes of follicles on generation of IVF early embryos. Theriogenology 1990, 33, 335.

    Article  Google Scholar 

  • Thibodeaux JK, Del Vecchio RP, Hansel W Role of platlet-derived growth factor in development of in vitro matured and in vitro fertilized bovine embryos. J. Reprod. Fert. 1993, 98, 61–66.

    Article  CAS  Google Scholar 

  • Tsimoda Y, Todunaga T, Sugie T Altered sex ratio of live young after transfer of fast and slow-developing mouse embryos. Gamete Research 1985, 72, 301–304.

    Article  Google Scholar 

  • Van Soom A, Van Vlaenderen I, Mahmoudzadeh AR, Deluyker H, de Kruif A Compaction rate of in vitro fertilized bovine embryos related to the interval from insemination to first cleavage. Theriogenology 1992, 38, 905–919.

    Article  CAS  PubMed  Google Scholar 

  • Watson AJ, Hogan A, Hahnel A, Wiemer KE, Schultz GA Expression of growth factor ligand and receptor genes in the preimplantation bovine embryo. Mol. Reprod. Dev. 1992, 31, 87–95.

    Article  CAS  PubMed  Google Scholar 

  • Werb Z Expression of EGF and TGF-a genes in early mammalian development. Mol. Reprod. Dev. 1990, 27, 10–15.

    Article  CAS  PubMed  Google Scholar 

  • van der Westerlaken LAJ, de Wit AAC, van der Schans A, Eyestone WH, de Boer H Relationship between kinetics of polar body extrusion and developmental potential of bovine oocytes. 12th Int Congr. on Anim. Reprod., The Hague, The Netherlands 1992. Vol. 1, 384–386.

    Google Scholar 

  • Wiemer KE, Denniston RS, Amboroski GF, White KL, Godke RA A fetal bovine uterine fibroblast monolayer system for in vitro culture of bovine embryos. J. Anim. Sci. 1987, 65 (Suppl. 1), 53.

    Google Scholar 

  • Wiemer KE, Watson AJ, Polanski V, McKenna AI, Fick GH, Schultz GA Effects of maturation and co-culture treatments on the developmental capacity of early bovine embryos. Mol. Reprod. Dev. 1991, 30, 330–338.

    Article  CAS  PubMed  Google Scholar 

  • Wood SA, Kaye PL Effects of epidermal growth factor on preimplantation mouse embryos. J. Reprod. Fert. 1989, 85, 575–582.

    Article  CAS  Google Scholar 

  • Wurth YA, van der Zee-Kotting W, Kruip TAM, Dieleman SJ, Bevers MM Relation between macroscopic qualification of bovine embryos and number of blastomeres. Proc. 11th Int. Congr. Anim. Reprod. Al, Dublin, Ireland 1988, 3, 352.

    Google Scholar 

  • Xu KP, Yada BR, King WA, Betteridge KJ Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro. Mol. Reprod. Dev. 1992, 31, 249–252.

    Article  CAS  PubMed  Google Scholar 

  • Yang BK, Yang X, Foote RH Effect of growth factors on morula and blastocyst development of in vitro matured and in vitro fertilized bovine oocytes. Theriogenology 1993, 40, 521–530.

    Article  CAS  PubMed  Google Scholar 

  • Younis AI, Brackett BG In vitro development of bovine oocytes into morulae and blastocysts. Theriogenology 1990, 33, 362.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Reproduction and Forensic Medicine, Norwegian College of Veterinary Medicine, Oslo, Norway

    P. Lonergan

Authors
  1. P. Lonergan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Lonergan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lonergan, P. Growth of Preimplatation Bovine Embryos. Acta Vet Scand 35, 307–320 (1994). https://doi.org/10.1186/BF03548303

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1186/BF03548303

Keywords

Acta Veterinaria Scandinavica

ISSN: 1751-0147