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Protein synthesis is not required for male pronuclear formation in bovine zygotes

Published online by Cambridge University Press:  26 September 2008

R.C. Chian
Affiliation:
Centre de Recherche en Biologie de la Reproduction, Département des sciences animales, Université Laval, Québec, Canada.
M.A. Sirard*
Affiliation:
Centre de Recherche en Biologie de la Reproduction, Département des sciences animales, Université Laval, Québec, Canada.
*
Dr M.A. Sirard, Département des sciences animales, Université Laval, Québec, PQ, Canada GIK 7P4. Fax: +1(418)-656-3766.

Summary

Following fertilisation, the sperm triggers a series of intracellular changes which initiate oocyte activation and pronuclear formation. Oocyte activation can also be induced artificially by several chemicals, such as the calcium ionophore A23187. The sperm nucleus is transformed into the male pronucleus through the interaction of oocyte cytoplasmic factors. The profile of protein synthesis is different in bovine oocytes following fertilisation and parthenogenetic activation. The formation of male and female pronuclei was not blocked by the presence of the protein synthesis inhibitor cycloheximide. These results suggest that bovine oocyte activation by sperm and parthenogenetic activation induce different cytoplasmic responses for protein synthesis and that new protein synthesis is not required for male pronuclear formation in bovine zygotes.

Type
Article
Copyright
Copyright © Cambridge University Press 1996

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References

Balakier, H., & Tarkowski, A. (1980). The role of the germinal vesicle karyoplasm in the development of the male pronucleus in the mouse. Exp. Cell Res. 128, 7985.CrossRefGoogle ScholarPubMed
Bavister, B.D., Leibfried, L.M., & Leiberman, G. (1983), Development of preimplantation embryos of the golden hamster in a defined culture medium. Biol Reprod. 28, 235–47.CrossRefGoogle Scholar
Blow, J.J. & Laskey, R.A. (1986), Initiation of DNA replication in nuclei and purified DNA by a cell-free extract of Xenopus eggs. Cell 47, 577–87.CrossRefGoogle ScholarPubMed
Borsuk, E., & Tarkowski, A.K. (1989), Transformation of sperm nuclei into male pronuclei in nucleate and anucleate fragments of parthenogenetic mouse eggs. Gamete Res. 24, 471–81.CrossRefGoogle ScholarPubMed
Chian, R.C. & Niwa, K. (1994).Effect of cumulus cells present during different periods of culture on maturation in vitro of bovine oocytes. Theriogenology 41, 176.CrossRefGoogle Scholar
Chian, R.C., Niwa, K., & Sirard, M.A. (1994).Effects of cumulus cells on male pronuclear formation and subsequent early development of bovine oocytes in vitro. Theriogenology 41, 1499–508.CrossRefGoogle ScholarPubMed
Clarke, H. & Masui, Y. (1987).The induction of reversible and irreversible chromosome decondensation by protein synthesis inhibition during meiotic maturation of mouse oocytes. Dev. Biol. 97, 291301.CrossRefGoogle Scholar
Clarke, H. & Masui, Y. (1987).Dose-dependent relationship between oocyte cytoplasmic volume and transformation of sperm nuclei to metaphase chromosomes. J. Cell Biol. 104, 831–40.CrossRefGoogle ScholarPubMed
Ding, J., Clarke, N., Nagai, T., & Moor, R.M. (1992)a.Protein and nuclear changes in pig eggs at fertilization. Mol. Reprod. Dev. 31, 287–96.CrossRefGoogle ScholarPubMed
Ding, J., Moor, R.M., & Foxcroft, G.R. (1992)b.Effects of protein synthesis on maturation, sperm penetration, and pronuclear development in porcine oocytes. Mol. Reprod. Dev. 33, 5966.CrossRefGoogle ScholarPubMed
Eid, L.N., Lorton, S.P., & Parrish, J.J. (1994).Paternal influence on S-phase in the first cell cycle of the bovine embryo. Biol. Reprod. 51, 1232–7.CrossRefGoogle ScholarPubMed
Ekholm, C., & Magnusson, C. (1979), Rat oocyte maturation:effects of protein synthesis inhibitors. Biol. Reprod. 21, 1287–93.CrossRefGoogle ScholarPubMed
Endo, Y., Kopf, G.S., & Schultz, R.M. (1986).Stage-specific changes in protein phosphorylation accompanying meiotic maturation of mouse oocytes and fertilization of mouse eggs. J. Exp. Zool. 239, 401–9.CrossRefGoogle ScholarPubMed
Fulka, J. Jr, Motlik, J., Fulka, J., & Jilet, F. (1986).Effect of cycloheximide on nuclear maturation of pig and mouse oocytes. J. Reprod. Fertil. 77, 281–5.CrossRefGoogle ScholarPubMed
Gagne, M., Pothier, F., & Sirard, M.A. (1995). Effect of microinjection time during postfertilization S-phase on bovine embryonic development. Mol. Reprod. Dev. 41, 184–94.CrossRefGoogle ScholarPubMed
Golbus, M.S., & Stein, M.P. (1976).Qualitative patterns of protein synthesis in the mouse oocyte. J. Exp. Zool. 198, 337–42.CrossRefGoogle ScholarPubMed
Hagemann, L.J., Hillery-Weinhold, F.L., Leibfried-Rutledge, M.L., & First, N.L. (1995).Activation of murine oocytes with Ca2+ ionophore cycloheximide. J. Exp. Zool. 271, 5761.CrossRefGoogle ScholarPubMed
Hirao, Y., & Yanagimachi, R. (1979).Development of pronuclei in polyspermic eggs of the golden hamster: is there any limit to the number of sperm heads that are capable of developing into pronuclei?. Zoo Mag. 88, 2433.Google Scholar
Howlett, S.K. (1986).A set of proteins showing cell cycle-dependent modification in the early mouse embryo. Cell 45, 387–96.CrossRefGoogle ScholarPubMed
Howlett, S., Bolton, V.N. (1985).Sequence and regulation of morphological and molecular events during the first cell cycle of mouse embryogenesis. J. Embryol. Exp. Morphol. 87, 175206.Google ScholarPubMed
Hunter, A.G., & Moor, R.M. (1987).Stage dependent effects of inhibiting RNA and protein synthesis on meiotic maturation of bovine embryos in vitro. J. Dairy Sci. 70, 1646–51.CrossRefGoogle Scholar
Komar, A. (1982).Fertilization of parthenogenetically activated mouse eggs. I. Behaviour of sperm nuclei in the cytoplasm of parthenogenetically activated eggs. Exp. Cell Res. 139, 361–7.Google ScholarPubMed
Laemmli, U.K. (1970).Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277, 680–5.CrossRefGoogle Scholar
Laurincik, J., Kopecny, V., & Hyttel, P. (1994).Pronucleus development and DNA synthesis in bovine zygotes in vitro. Theriogenology 42, 1285–93.CrossRefGoogle Scholar
Leibfried, M.L., & Bavister, E.D. (1982).Effects of epinephrine and hypotaurine in in vitro fertilization in the golden hamster. J. Reprod. Fertil. 66, 8793.CrossRefGoogle ScholarPubMed
Lohka, M.J., & Maller, J.L. (1987).Regulation of nuclear formation and breakdown in cell-free extracts of amphibian eggs. In Molecular Regulation of Nuclear Events in Mitosis and Meiosis, ed. Schlegel, R.A., Halleck, M.S. & Rao, P.N., pp. 67109. New York: Academic Press.CrossRefGoogle Scholar
Longo, F.J., & Kunkle, M. (1978).Transformation of sperm nuclei upon insemination. Curr. Top. Dev. Biol. 12, 149–84.CrossRefGoogle ScholarPubMed
Moor, R.M., & Gandolfi, F. (1987).Molecular and cellular changes associated with maturation and early development of sheep eggs. J. Reprod. Fertil. Suppl. 34, 5569.Google ScholarPubMed
Moses, R.M., & Kline, D. (1995).Release of mouse eggs from metaphase arrested by protein synthesis inhibition in the absence of a calcium signal or microtubule assembly. Mol. Reprod. Dev. 41, 264–73.CrossRefGoogle ScholarPubMed
Moses, R.M., & Masui, Y. (1994). Enhancement of mouse egg activation by the kinase inhibitor, 6-dimethylaminopurine (6-DMAP). J. Exp. Zool. 270, 211–18.CrossRefGoogle ScholarPubMed
Osborn, J.C., & Moor, R.M. (1983). Time-dependent effects of α-amanitin on nuclear maturation and protein synthesis in mammalian oocytes. J. Embryol.Exp. Morphol. 73, 317–38.Google ScholarPubMed
Park, C.K., Ohgoda, O., & Niwa, K. (1989). Penetration of bovine follicular oocytes by frozen-thawed spermatozoa in the presence of caffeine and heparin. J. Reprod. Fertil. 86, 577–82.CrossRefGoogle ScholarPubMed
Parrish, J.J., Susko-Parrish, J.L., Leibfried-Rutledge, M.L., Critser, E.S., Eyestone, W.H. & First, N.L. (1986). Bovine in vitro fertilization with frozen-thawed semen. Theriogenology 25, 591600.CrossRefGoogle ScholarPubMed
Parrish, J.J., Susko-Parrish, J.L., Weiner, M.A., & First, N.I. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–80.CrossRefGoogle ScholarPubMed
Saeki, K., Kato, H., Hosoi, Y., Miyake, M., Utsumi, K., & Iritani, A. (1991).Early morphological events of in vitro fertilized bovine oocytes with frozen-thawed spermatozoa. Theriogenology 35, 1051–8.CrossRefGoogle ScholarPubMed
Schultz, R.M., & Wassarman, P.M. (1977).Specific changes in the pattern of protein synthesis during meiotic maturation of mammalian oocytes in vitro. Proc. Natl. Acad. Sci. USA. 74, 538–41.CrossRefGoogle ScholarPubMed
Siracusa, G., Whithingham, D.G., Molinaro, M., & Vivarelli, E. (1978). Parthenogenetic activation of mouse oocytes induced by inhibitors of protein synthesis. J. Embryol. Exp. Morphol. 32, 157–66.Google Scholar
Sirard, M.A., Leibfried-Rutledge, M.L., Pamsh, J.J., Ware, C., & First, N.L. (1988).The culture of bovine oocytes to obtain developmentally competent embryos. Biol. Reprod. 39, 546–52.CrossRefGoogle ScholarPubMed
Steel, R.G.D., & Torrie, J.H. (1980). Principles and Procedures of Statistics: A Biometrical Approach, pp. New York: 172–94.McGraw-Hill.Google Scholar
Sun, F.Z., Hoyland, J., Huang, X., Mason, W., & Moor, R.M. (1992). A comparison of intracellular changes in porcine eggs after fertilization and electroactivation. Development 115, 947–56.CrossRefGoogle ScholarPubMed
Tarkowski, A. (1980). Fertilization of nucleate and anucleate egg fragments in the mouse. Exp. Cell Res. 128, 73–7.CrossRefGoogle ScholarPubMed
Thibault, C. (1977). Are follicular maturation and oocyte maturation independent processes? J. Reprod. Fertil. 51. 115.CrossRefGoogle ScholarPubMed
Van Blerkom, J. (1979). Molecular differential of the rabbit ovum. III. Fertilization-autonomous polypeptide synthesis. Dev. Biol. 72, 8894.Google ScholarPubMed
Xu, K.P., & Greve, T. (1988). A detail analysis of early events during in-vitro fertilization of bovine follicular oocytes. J. Reprod. Fertil. 82, 127–34.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1978).Sperm-egg association in mammals. Curr. Top. Dev. Biol. 12, 83105.CrossRefGoogle Scholar
Yanagimachi, R. (1981). Mechanisms of fertilization in mammals. In Fertilization and Embryonic Development In Vitro, Mastroianni, L. Jr & J.D., Biggers, pp. 81182. New York: Plenum Press.CrossRefGoogle Scholar
Zemicka-Goetz, M., Ciemerych, M.A., Kubiak, J.Z., Tarkowski, A.K., & Maro, B. (1995). Cytostatic factor inactivation is induced by a calcium-dependent mechanism present until the second cell cycle in fertilized but not in parthenogenetically activated mouse eggs. J. Cell Sci. 108, 469–74.CrossRefGoogle Scholar
Zhang, S.C., Masui, Y. (1992). Activation of Xenopus laevis eggs in the absence of intracellular Ca activity by the protein phosphorylation inhibitor, 6-dimethylaminopurine (6-DMAP). J. Exp. Zool. 262, 317–29.CrossRefGoogle ScholarPubMed
Zirkin, B.R., Perreault, S.D., & Naish, S.J. (1989). Formation and function of the male pronucleus during mammalian fertilization. In The Nuclear Biology of Fertilization. Schatten, H. & Schatten, G., pp91114. New York: Academic Press.CrossRefGoogle Scholar