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Calcium-dependent development of secondary cytostatic factor (2°CSF) from Xenopus laevis oocytes and zygotes

Published online by Cambridge University Press:  26 September 2008

Jianshe Zhang  and
Yoshio Masui
Jianshe Zhang*
Affiliation:
Department of Zoology, University of Toronto, Toronto, Canada
Yoshio Masui
Affiliation:
Department of Zoology, University of Toronto, Toronto, Canada
*
J. Zhang, Department of Zoology, University of Toronto, Toronto, CanadaM5S 1A1. Telephone: 416-978-3493. Fax: 416-978-8532.
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Summary

Fresh cytosols extracted from unfertilised eggs of Xenopus laevis contain a cytostatic factor (CSF) which arrests the cell cycle at metaphase when microinjected into cleaving blastomeres. This CSF is sensitive to Ca2+ and is designated primary CSF (1°CSF). During storage of Ca2+-containing cytosols at 2°C, a stable CSF activity appears which is designated secondary CSF (2°CSF). In the present study, we report that 2°CSF activity can be induced in cytosols extracted from stage VI oocytes, unfertilised eggs, electrically activated eggs or blastulae, in the presence of Ca2+. Both the intensity and the rate of 2°CSF development are dependent on the concentration of Ca2+ ions added to the cytosol. At Ca2+ concentrations of 5–10 mM, 2°CSF activity reaches a maximum in about 7 days. Secondary CSF is relatively resistant to heat but loses all activity after 5 min at 70°C. When stored at −80°C, 2°CSF activity remains detectable for about 6 weeks. Cytological observations show that blastomeres arrested by microinjection of 2°CSF developed in cytosols of unfertilised eggs, activated eggs or blastulae contain metaphase chromosomes embedded in a bipolar spindle that has no asters developed at its poles. In contrast, blastomeres arrested by 2°CSF in cytosols of stage VI oocytes contain condensed chromosomes but no spindle is formed. The mechanisms of the development of 2°CSF in Ca2+-containing cytosols and its mode of action are discussed.

Keywords

Cell cycleCSFMeiosisXenopus
Type
Article
Information
Zygote , Volume 4 , Issue 1 , February 1996 , pp. 11 - 19
Copyright
Copyright © Cambridge University Press 1996

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References

Brachet, J.F., Hanocq, F., & Van Gansen, P. (1970). A cytochemical and ultrastructural analysis of in vitro maturation in amphibian oocytes. Dev. Biol. 21, 157–95.CrossRefGoogle ScholarPubMed
Duesbery, N.S., & Masui, Y. (1993). Changes in protein association with intracellular membranes of Xenopus laevis oocytes during maturation and activation. Zygote 1, 129–41.CrossRefGoogle ScholarPubMed
Dumont, J.N., (1972). Oogenesis in Xenopus laevis (Daudin). I Stages of oocyte development in laboratory-maintained animals. J. Morphol. 139, 153.CrossRefGoogle Scholar
Gabrielli, B.G., Linda, M.R., & Maller, J.H. (1993). Requirements for cdk2 in cytostatic factor mediated metaphase II arrest. Science 259, 1766–9.CrossRefGoogle ScholarPubMed
Haccard, O., Sarcevic, B., Llewellyn, A., Hartley, R., Roy, T., Isumi, T., Erikson, E., & Maller, J.L. (1993). Induction of metaphase arrest in cleaving Xenopus embryos by MAP kinase. Science 262, 1262–5.CrossRefGoogle ScholarPubMed
Lorca, T., Gals, S., Fequet, D., Devault, A., Cavadov, J.C., & Doree, M. (1991). Degradation of the protooncogene product p39mos is not necessary for cyclin proteolysis and exit from mitotic metaphase: requirement for Ca2+-calmodulin dependent event. EMBO J. 10, 2087–93.CrossRefGoogle ScholarPubMed
Masui, Y. (1974). A cytostatic factor in amphibian oocytes: its extraction and partial characterization. J. Exp. Zool. 187, 141–7.CrossRefGoogle ScholarPubMed
Masui, Y. & Clark, H.J. (1979). Oocytes maturations. Int. Rev. Cytol. 57, 185–282.CrossRefGoogle Scholar
Masui, Y. & Markert, C.L. (1971). Cytoplasmic control of nuclear behaviour during meiotic maturation of frog oocyte. J. Exp. Zool. 177, 129–45.CrossRefGoogle Scholar
Masui, Y. & Shibuya, E.K. (1987). Development of cytoplasmic activities that control chromosome cycles during maturation of amphibian oocytes. In Molecular Regulation of Nuclear Events in Mitosis and Meiosis, pp. 1–41. New York: Academic Press.Google Scholar
Masui, Y., Meyerhof, P.G., Miller, M.A., & Wasserman, W.J. (1977). Roles of divalent cations in maturation and activation of vertebrates oocytes. Differentiation 9, 49–57.CrossRefGoogle ScholarPubMed
Masui, Y., Meyerhof, P.G. & Miller, M.A. (1980). Cytostatic factor and chromosome behaviour in early development. In The Cell Surface: Mediator of Developmental Processes, ed. Subtelney, S., Eighth Symposium of the Society for Developmental Biology, pp. 235–56. New York: Academic Press.CrossRefGoogle Scholar
Matten, W.T., & Vande Woude, G.F. (1994). Cell cycle control and early embryogenesis: Xenopus laevis maturation and early embryonic cell cycles. Semin. Dev. Biol. 5, 173–81.CrossRefGoogle Scholar
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. (1979a). Properties of a cytostatic factor from Xenopus laevis eggs. Dev. Biol. 72, 182–7.CrossRefGoogle ScholarPubMed
Meyerhof, P.G., & Masui, Y. (1979b). 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
Moses, M.R., & Masui, Y. (1989). Cystostatic factor (CSF) in the eggs of Xenopus laevis. Exp. Cell Res. 185, 271–6.CrossRefGoogle Scholar
Moses, M.R., & Masui, Y. (1990). Cystostatic factor (CSF) activity in cytosols extracted from Xenopus laevis eggs. Exp. Cell Res. 186, 66–73.CrossRefGoogle Scholar
Moore, B.C., & Ryan, W.R. (1940). Chromosomes of frog eggs and embryos stained by the Feulgen method to avoid excessive staining of yolk granules. Anat. Rec. 78, (Supp1), 122.Google Scholar
Posada, J., & Cooper, J.A. (1992). Requirements for phosphorylation of MAP kinase during meioses in Xenopus oocytes. Science 255, 212–15.CrossRefGoogle ScholarPubMed
Posada, J., Yew, N., Ahn, G., Vande Woude, G.F., & Cooper, J.A. (1993). Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase Kinase in vitro. Mol. Cell Biol., 13, 2546–53.Google ScholarPubMed
Sadakane, Y., & Iwao, Y. (1993). A factor that intercepts the cell cycle at G2 or prophase is present in full grown frog oocytes. Dev. Growth Differ. 35, 129–38.CrossRefGoogle ScholarPubMed
Sagata, N., Oskasson, M., Copeland, M.T., Brumbaugh, J.L., & Vande Woude, G.F.. (1988). Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature 335, 519–25.CrossRefGoogle ScholarPubMed
Sagata, N., Watanabe, N., Vande Woude, G.F., & Ikawa, Y. (1989). The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs. Nature 342, 512–18.CrossRefGoogle ScholarPubMed
Shibuya, E.K., & Masui, Y. (1988). Stabilization and enhancement of primary cytostatic factor (CSF) by ATP and NaF in amphibian egg cytosols. Dev. Biol. 129, 253–64.CrossRefGoogle ScholarPubMed
Shibuya, E.K., & Masui, Y. (1989a). Molecular characteristics of cytostatic factors in amphibian egg cytosols. Development 106, 799–808.CrossRefGoogle ScholarPubMed
Shibuya, E.K., & Masui, Y. (1989b). Fractionation of cytostatic factors from cytosols of amphibian eggs. Dev. Biol. 135, 212–19.CrossRefGoogle ScholarPubMed
Shibuya, E.K., & Ruderman, Y. (1993) Mos induces the in vitro activation of mitogen-activated protein kinases in lysates of frog oocytes and mammalian somatic cells. Mol. Biol. Cell 4, 781–90.CrossRefGoogle ScholarPubMed
Smith, B.G. (1912). The embryology of Crytobranchus allegeheniensis including comparisons with some other vertebrates. J. Morphol. 23, 61–153.CrossRefGoogle Scholar
Smith, L.D., & Ecker, R.E. (1971). The interaction of steroids with Rana pipiens oocytes in induction of maturation. Dev. Biol. 25, 233–47.CrossRefGoogle ScholarPubMed
Thomas, G. (1992). MAP kinase by any other name smells just as sweet. Cell 68, 3–6.CrossRefGoogle ScholarPubMed
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