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First meiosis of early dictyate nuclei from primordial oocytes in mature and activated mouse oocytes

Published online by Cambridge University Press:  26 September 2008

Renata Czolowska  and
Andrzej K. Tarkowski
Renata Czolowska*
Affiliation:
Department of Embryology, Institute of Zoology, University of Warsaw, Poland.
Andrzej K. Tarkowski
Affiliation:
Department of Embryology, Institute of Zoology, University of Warsaw, Poland.
*
R. Czolowska, Department of Embryology, Institute of Zoology, University of Warsaw, Krakowskie Przedmiescie 26/28, 00-927 Warsaw 64, Poland. Telephone: +48 2 6200381, ext 536. Fax: + 48 22 268624.
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Summary

Nuclei of diplotene (dictyate) primordial oocytes (PO) were transferred to metaphase II oocytes and to activated mouse oocytes using cell fusion techniques. In a metaphase II oocyte, the PO nucleus condenses within 2–3 h to bivalents which become arranged on the first meiotic spindle. After oocyte activation, homologous chromosomes segregate between the oocyte and the first polar body, and a diploid pronucleus-like nucleus reforms from the one set of dyads. This nucleus condenses in the first embryonic mitosis into 40 ‘somatic’ chromosomes which coexist in the common metaphase plate with 20 somatic chromosomes originating from the female pronucleus. Shortening of the time between fusion and activation to about 1 h prevents bivalent differentiation. The PO nucleus condenses only partially and reforms, after oocyte activation, a pronucleus-like nucleus. This nucleus gives rise at the first embryonic mitosis to 20 bivalents which coexist with 20 somatic chromosomes originating from the female pronucleus. A PO nucleus introduced into an activated egg completes the first cell cycle as an intact interphase nucleus. It never condenses in the first embryonic mitosis into bivalents, and undergoes only initial condensation (preceding bivalent differentiation). These results indicate that: (1) condensation into bivalents, meiotic spindle formation and first meiotic division can be greatly accelerated by the introduction of an early diplotene (dictyate) oocyte nucleus into a metaphase II oocyte, and (2) depending on whether the diplotene nucleus enters the first embryonic (mitotic) cell cycle after just initiating or after completing the first meiosis, it gives rise at the first cleavage division to meiotic (bivalents) or ‘somatic’ chromosomes respectively.

Keywords

FusionMouseOocyte activationPremature meiosis IPrimordial oocytes
Type
Article
Information
Zygote , Volume 4 , Issue 1 , February 1996 , pp. 73 - 80
Copyright
Copyright © Cambridge University Press 1996

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References

Bachvarova, R. (1985). Gene expression during oogenesis and oocyte development in mammals. In Developmental Biology, ed. Browder, L.W., vol. 1, pp. 453–524. New York: Plenum Press.Google Scholar
Balakier, H. (1978). Induction of maturation in small oocytes from sexually immature mice by fusion with meiotic or mitotic cells. Exp. Cell Res. 112, 137–41.CrossRefGoogle ScholarPubMed
Choi, T., Aoki, F., Mori, M., Yamashita, M., Nagahama, Y. & Kohmoto, K. (1991). Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113, 789–95.CrossRefGoogle ScholarPubMed
Cuthbertson, K.S.R. (1983). Parthenogenetic activation of mouse oocytes with ethanol and benzyl alcohol. J. Exp. Zool. 226, 311–14.CrossRefGoogle ScholarPubMed
Cuthbertson, K.S.R., Whittingham, D.G. & Cobbold, P.H. (1981). Free Ca2+ increases in exponential phases during mouse oocyte activation. Nature 294, 754–7.CrossRefGoogle ScholarPubMed
Czolowska, R., Modlinski, J.A. & Tarkowski, A.K. (1984). Behaviour of thymocyte nuclei in non-activated and activated mouse oocytes. J. Cell Sci. 69, 19–34.CrossRefGoogle ScholarPubMed
Czolowska, R., Szöllösi, D. & Szöllösi, M.S. (1992). Changes in embryonic 8-cell nuclei transferred by means of cell fusion to mouse eggs. Int. J. Dev. Biol. 36, 543–53.Google ScholarPubMed
Donahue, R.P. (1968). Maturation of the mouse oocyte in vitro. I. Sequence and timing of nuclear progression. J. Exp. Zool. 169, 237–50.CrossRefGoogle ScholarPubMed
Edwards, R.G. & Gates, A.H. (1959). Timing of the stages of the maturation divisions, ovulation, fertilization and the first cleavage of eggs of adult mice treated with gonadotrophins. J. Endocrinol. 18, 292–304.CrossRefGoogle ScholarPubMed
Eichenlaub-Ritter, U. & Boll, I. (1989). Nocodazole sensitivity, age-related aneuploidy, and alterations in the cell cycle during maturation of mouse oocytes. Cytogenet. Cell Genet. 52, 170–6.CrossRefGoogle ScholarPubMed
Fulton, B.P. & Whittingham, D.G. (1978). Activation of mammalian oocytes by intracellular injection of calcium. Nature 273, 149–51.CrossRefGoogle ScholarPubMed
Hampl, A. & Eppig, J.J. (1995). Translational regulation of the gradual increase in histone H1 kinase activity in maturing mouse oocytes. Mol. Reprod. Dev. 40, 9–15.CrossRefGoogle ScholarPubMed
Hashimoto, N. & Kishimoto, T. (1988). Regulation of meiotic metaphase by a cytoplasmic maturation-promoting factor during mouse oocyte maturation. Dev. Biol. 126, 242–52.CrossRefGoogle ScholarPubMed
Kaufman, M.H. (1983). Early Mammalian Development: Parthenogenetic Studies. Cambridge: Cambridge University Press.Google Scholar
Kaufman, M.H. & O'Neill, G.T. (1988). Aneuploidy induced by ethanol. In Aneuploidy, part B, Induction and Test Systems, pp. 95–122. New York: Alan R. Liss.Google Scholar
Kubiak, J.Z. & Tarkowski, A.K. (1985). Electrofusion of mouse blastomeres. Exp. Cell Res. 157, 561–6.CrossRefGoogle ScholarPubMed
Mangia, F. & Epstein, C.J. (1975). Biochemical studies of growing mouse oocytes: preparation of oocytes and analysis of glucose-6-phosphate dehydrogenase and lactate dehydrogenase activities. Dev. Biol. 45, 211–20.CrossRefGoogle ScholarPubMed
Masui, Y. & Markert, C.L. (1971). Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 177, 129–45.CrossRefGoogle ScholarPubMed
Meyerhof, P.G. & Masui, Y. (1977). Ca and Mg control of cytostatic factors from Rana pipiens oocytes which cause metaphase and cleavage arrest. Dev. Biol. 61, 214–29.CrossRefGoogle ScholarPubMed
Meyerhof, P.G. & Masui, Y. (1979 a). Chromosome condensation activity in Rana pipiens eggs matured in vivo and in blastomeres arrested by cytostatic factor (CSF). Exp. Cell Res. 123, 345–53.CrossRefGoogle ScholarPubMed
Meyerhof, P.G. & Masui, Y. (1979 b). Properties of a cytostatic factor from Xenopus laevis eggs. Dev. Biol. 72, 182–7.CrossRefGoogle ScholarPubMed
Murray, A.W., Solomon, M.J. & Kirschner, M.W. (1989). The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339, 280–6.CrossRefGoogle ScholarPubMed
Norbury, C. & Nurse, P. (1992). Animal cell cycles and their control. Annu. Rev. Biochem. 61, 441–70.CrossRefGoogle ScholarPubMed
O'Neill, G.T. & Kaufman, M.H. (1987). Ovulation and fertilization of primary and secondary oocytes in LT/Sv strain mice. Gamete Res. 18, 27–36.CrossRefGoogle ScholarPubMed
Peters, H. (1969). The development of the mouse ovary from birth to maturity. Ada Endocrinol. 62, 98–116.Google ScholarPubMed
Polanski, Z. (1986). In-vivo and in-vitro maturation rate of oocytes from two strains of mice. J. Reprod. Fertil. 78, 103–9.CrossRefGoogle ScholarPubMed
Szöllösi, D. (1993). Oocyte maturation. In Reproduction in Mammals and Man, ed. Thibault, C., Levasseur, M.C. & Hunter, R.H.F., pp. 307–25. Paris: Ellipses.Google Scholar
Szöllösi, D., Calarco, P. & Donahue, R.P. (1972). Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J. Cell Sci. 11, 521–41.CrossRefGoogle ScholarPubMed
Szöllösi, D., Czolowska, R., Szöllösi, M.S. & Tarkowski, A.K. (1986). Remodeling of thymocyte nuclei in activated mouse oocytes: an ultrastructural study. Eur. J. Cell Biol. 42, 140–51.Google ScholarPubMed
Szöllosi, D., Czolowska, R., Szöllösi, M.S. & Tarkowski, A.K. (1988). Remodeling of mouse thymocyte nuclei depends on the time of their transfer into activated, homologous oocytes. J. Cell Sci. 91, 603–13.CrossRefGoogle ScholarPubMed
Tarkowski, A.K. (1966). An air-drying method for chromosome preparations from mouse eggs. Cytogenetics 5, 394–400.CrossRefGoogle Scholar
Tarkowski, A.K. & Balakier, H. (1980). Nucleo-cytoplasmic interactions in cell hybrids between mouse oocytes, blastomeres and somatic cells. J. Embryol. Exp. Morphol. 55, 319–30.Google ScholarPubMed
Tarkowski, A.K. & Wroblewska, J. (1967). Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J. Embryol. Exp. Morphol. 18, 155–80.Google Scholar