Characterization of embryos derived from calf oocytes: kinetics of cleavage, cell allocation to inner cell mass, and trophectoderm and lipid metabolism.
Majerus, V.; Lequarré, Anne-Sophie; Ferguson, E. M.et al.
2000 • In Molecular Reproduction and Development, 57 (4), p. 346-52
Animals; Blastomeres/metabolism/physiology; Cattle; Female; Kinetics; Oocytes/metabolism/physiology; Staining and Labeling; Triglycerides/metabolism
Abstract :
[en] Embryos derived from calf oocytes were compared with adult cow oocyte-derived embryos (1) by studying the kinetics of embryo development using time-lapse cinematography (2) by evaluating the ratio between inner cell mass (ICM) and trophectoderm (TE) cells in blastocysts (3) by measuring the triglyceride content of the blastocysts. The rate of calf oocyte-derived embryos reaching the blastocyst stage was reduced (26 vs. 46% for adult derived embryos). Calf oocyte-derived embryos preferably arrested their development before the 9-cell stage. Those that developed into blastocysts had cleaved earlier to reach the 2-cell or 3-cell stages than embryos that arrested before the 9-cell stage. The 9-cell stage tended to appear later in calf oocyte-derived embryo that reached the blastocyst stage than in adult-derived embryos. This difference became significant at the morula stage. Accordingly, the fourth cell cycle duration was longer for calf oocyte-derived embryos. Day 8 blastocysts from both sources had similar total cell numbers (calf: 89 +/- 20; cow: 100 +/- 30) and cell distribution between TE and ICM. The triglyceride content of day 7 blastocysts was similar for both sources (64 +/- 15 vs. 65 +/- 6 ng/embryo, respectively). In conclusion, calf oocyte-derived embryos are characterized by a higher rate of developmental arrest before the 9-cell stage and by a longer lag phase preceding the major onset of embryonic genome expression. These changes might be related to insufficient "capacitation" of the calf oocyte during follicular growth. Despite these differences, modifications in the quality of the resulting blastocysts were not detected.
Disciplines :
Biotechnology
Author, co-author :
Majerus, V.
Lequarré, Anne-Sophie ; Université de Liège - ULiège > Département de productions animales > Génomique animale
Ferguson, E. M.
Kaidi, S.
Massip, A.
Dessy, F.
Donnay, I.
Language :
English
Title :
Characterization of embryos derived from calf oocytes: kinetics of cleavage, cell allocation to inner cell mass, and trophectoderm and lipid metabolism.
Publication date :
2000
Journal title :
Molecular Reproduction and Development
ISSN :
1040-452X
eISSN :
1098-2795
Publisher :
John Wiley & Sons, Hoboken, United States - New York
Armstrong D.T., Holm P., Irvine B., Petersen B.A., Stubbings R.B., McLean D., Stevens G., Seamark R.F. (1992) Pregnancies and live birth from in vitro fertilisation of calf oocytes collected by laparoscopic follicular aspiration. Theriogenology 38:667-678.
Armstrong D.T., Irvine B., Earl C.R., McLean D., Stevens G., Seamark R.F. (1994) Gonadotropin stimulation regimens for follicular aspiration and in vitro embryo production from calves oocytes. Theriogenology 42:1227-1236.
Barnes F.L., Eyestone W.H. (1990) Early cleavage and maternal zygotic transition in bovine embryos. Theriogenology 33:141-152.
Brogliatti G.M., Furnus C.C., De Matos D.G., Martinez A.G. (1999) In vitro fertilisation program in prepuberal brangus calves and later embryo collection. Theriogenology 51:313.
Dagnelie P. (1986) Les methodes de l'inference statistique., Gembloux Agronomics Press, editor. Theorie et methodes statistiques. Gembloux, Belgium; 213-240.
Damiani P., Fissore R.A., Cibelli J.B., Long C.R., Balise J.J., Robl J.M., Duby R.T. (1996) Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes. Mol Reprod Dev 45:521-534.
Earl C., Fry R.C., Maclellan L.J., Kelly J., Armstrong D.T. (1998) In vitro fertilisation and development potential of prepubertal calf oocytes., Lauria A, Gandolfi F, Enne G, Gianaroli L, editors. Serono Symposia, Gametes: Development and Function. Rome; 115-137.
Erickson B.H. (1966) Development and senescence of the postnatal bovine ovary. J Anim Sci 25:800-805.
Fair T., Hyttel P., Greve T. (1995) Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev 42:437-442.
Ferguson E., Leese H. (1999) Triglyceride content of bovine oocytes and early embryos. J Reprod Fertil 116:373-378.
Flynn T.J., Hillman N. (1978) Lipid synthesis from [U-14C]-glucose in preimplantation mouse embryos in culture. Biol Reprod 19:922-926.
Fry R.C., Simpson T.L., Squires T.J. (1998) Ultrasonically guided transvaginal oocyte recovery from calves treated with or without GnRH. Theriogenology 49:1077-1082.
Gandolfi F., Milanesi E., Pocar P., Luciano A.M., Brevini T.A.L., Acocella F., Lauria A., Armstrong D.T. (1998) Comparative analysis of calf and cow oocytes during in vitro maturation. Mol Reprod Dev 49:168-175.
Grisart B., Massip A., Dessy F. (1994) Cinematographic analysis of bovine embryo development in serum-free oviduct-conditioned medium. J Reprod Fertil 101:257-264.
Hardy K., Handyside A., Winston R. (1989) The human blastocyst: Cell number, death and allocation during late preimplantation development in vitro. Development 107:597-604.
Holm P., Booth P., Vajta G., Callesen H. (1997) A protein-free SOF system supplemented with amino acids, sodium citrate and myoinositol. Proceedings of the 13th Association Europeenne de Transfert Embryonnaire, Lyon 158.
Holm P., Shukri N.N., Vajta G., Booth P., Bendixen C., Callesen H. (1998) Developmental kinetics of the first cell cycles of bovine in vitro produced embryos in relation to their in vitro viability and sex. Theriogenology 50:1285-1299.
Hyttel P., Fair T., Callesen H., Greve T. (1997) Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47:23-32.
Iwasaki S., Yoshiba N., Ushijima H., Watanabe S., Nakahara T. (1990) Morphology and proportion of inner cell mass of bovine blastocysts fertilized in vitro and in vivo. J Reprod Fertil 90:279-284.
Kaidi S., Donnay I., Van Langendonckt A., Dessy F., Massip A. (1998) Comparison of two-coculture systems to assess the survival of in vitro produced bovine blastocysts after vitrification. Anim Reprod Sci 52:39-50.
Khatir H., Lonergan P., Carolan C., Mermillod P. (1996) Prepubertal bovine oocyte: A negative model for studying oocyte developmental competence. Mol Reprod Dev 45:2131-2319.
Khatir H., Lonergan P., Touze J.L., Mermillod P. (1998) The characterization of bovine embryos obtained from prepubertal calf oocytes and their viability after non surgical embryo transfer. Theriogenology 50:1201-1210.
Levesque J.T., Sirard M.A. (1994) Proteins in oocytes from calves and adult cows before maturation: Relationships with their developmental capacity. Reprod Nutr Dev 34:133-139.
Lohuis M.M. (1995) Potential benefits of bovine embryo-manipulation technologies to genetic improvement programs. Theriogenology 43:51-60.
Majerus V., De Roover R., Etienne D., Kaidi S., Massip A., Dessy F., Donnay I. (1999) Embryo production by ovum pick up in unstimulated calves before and after puberty. Theriogenology 52:1169-1179.
Melvin E.J., Lindsey B.R., Quintal-Franco J., Zanella E., Fike K.E., Van Tassel C.P., Kinder J.E. (1999) Circulating concentrations of estradiol, luteinizing hormone, and follicle-stimulating hormone during waves of avarian follicular development in prepubertal cattle. Biol Reprod 60:405-412.
Nagashima H., Kashiwasaki N., Ashman R.J., Grupen C.G., Seamark R.F., Nottle M.B. (1994) Removal of cytoplasmic lipid enhances the tolerance of porcine embryos to chilling. Biol Reprod 51:618-622.
Nicolson G., Yanagimachi R., Yanagimachi H. (1975) Ultrastructural localization of lectin-binding sites on the zona pellucida and plasma-membranes of mammalian eggs. J Cell Biol 66:263-274.
Otoi T., Yamamoto K., Koyama N., Tachikawa S., Suzuki T. (1997) Bovine oocyte diameter in relation to developmental competence. Theriogenology 48:769-774.
Papaioannou V., Ebert K. (1988) The preimplantation pig embryo: Cell number and allocation to trophectoderm and inner cell mass of the blastocyst in vivo and in vitro. Development 102:793-803.
Plante L., King W.A. (1992) Effect of time to first cleavage on hatching rate of bovine embryo in vitro. Theriogenology 37:274.
Pollard J.W., Leibo S.P. (1993) Comparative cryobiology of in vitro and in vivo derived bovine embryos. Theriogenology 39:287.
Presicce G.A., Jiang S., Simkin M., Zhang L., Looney C.R., Godke R.A., Yang X. (1997) Age and hormonal dependence of acquisition of oocyte competence for embryogenesis in prepubertal calves. Biol Reprod 56:386-392.
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 with that of cows. J Reprod Fertil 103:115-120.
Sata R., Tsijii H., Abe H., Yamashita S., Hoshi H. (1999) Fatty acid composition of bovine embryos cultured in serum-free and serum-containing medium during early embryonic development. J Reprod Dev 45:97-103.
Steeves T.E., Gardner D.K. (1999) Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from prepubertal and adult cows. Mol Reprod Dev 54:92-101.
Steeves T.E., Gardner D.K., Zuelke K.A., Squires T.S., Fry R.C. (1999) In vitro development and nutrient uptake by embryos derived from oocytes of pre-pubertal and adult cows. Mol Reprod Dev 54:49-56.
Stojkovic M., Buttner M., Zakhartchenko V., Brem G., Wolf E. (1998) A reliable procedure for differential staining of in vitro produced bovine blastocysts: Comparison of tissue culture medium 199 and Menezo's 2 medium. Anim Reprod Sci 50:1-9.
Telford N., Watson A., Schultz G. (1990) Transition from maternal to embryonic control in early mammalian development: A comparison of several species. Mol Reprod Dev 26:90-100.
Tervit H., McMillan W., McGowan L., Smith J., Hall D., Donnison M. (1997) Effect of juvenile calf age on follicular dynamics and in vitro embryo production. Theriogenology 47:300.
Van Langendonckt A., Donnay I., Schuurbiers N., Auquier P., Carolan C., Massip A., Dessy F. (1997) Effects of supplementation with fetal calf serum on development of bovine embryos in synthetic oviduct fluid medium. J Reprod Fertil 109:87-93.
Van Soom A., De Kruif A. (1992) A comparative study of in vivo and in vitro derived bovine embryos. Proceedings of the 12th International Congress of Animal Reproduction, The Hague 3:1363-1365.
Van Soom A., Boerjan M., Ysebaert M.-T., De Kruif A. (1996) Cell allocation to the inner cell mass and the trophectoderm in bovine embryos cultured in two different media. Mol Reprod Dev 45:171-182.
Van Soom A., Ysebaert M.-T., De Kruif A. (1997) Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol Reprod Dev 47:47-56.