Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-28T00:50:32.839Z Has data issue: false hasContentIssue false

Metaphase arrest in newly matured or microtubule-depleted mouse eggs after calcium stimulation

Published online by Cambridge University Press:  26 September 2008

Ruth M. Moses*
Affiliation:
Department of Zoology, University of Toronto, Toronto, Canada
Yoshio Masui
Affiliation:
Department of Zoology, University of Toronto, Toronto, Canada
*
Dr Ruth Moses, Department of Zoology, University of Toronto, 25, Harbord Street, Toronto, Ontario, Canada M5S 1A1. Telephone: (416) 978-3493. Fax: (416)978-8532.

Summary

In mouse eggs arrested at meiotic metaphase II, the increase in intracellular calcium that results from fertilisation induces nuclear formation in both newly ovulated and older eggs. In contrast, the calcium increase that results from exposure to the calcium ionophore A23187 induces nuclear formation in older, but not young, newly ovulated eggs. When treated with the microtubule inhibitor colcemid, and fertilised, young eggs remained at metaphase, but many older eggs formed nuclei, although older eggs treated with colcemid and A23187 remained at metaphase. However, young A23187-treated eggs, young colcemid-treated fertilised eggs, and older colcemid- and A23187-treated eggs, formed nuclei when treated, in addition, with the protein synthesis inhibitor cycloheximide, or the protein kinase inhibitor 6-dimethylaminopurine (6-DMAP). The possibility is discussed that metaphase in newly matured eggs and microtubule-depleted eggs may be maintained by similar mechanisms involving short-lived phosphorylated proteins.

Type
Article
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Cho, W.K., Stern, S. & Biggers, J.D. (1974). Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J. Exp. Zool. 187, 383–6.CrossRefGoogle ScholarPubMed
Cuthbertson, K.S.R. & Cobbold, P.H. (1985). Phorbol ester and sperm activate mouse oocytes by inducing sustained oscillations in cell Ca2+. Nature. 316, 541–2.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
Felix, M.-A., Labbe, J.-C., Doree, M., Hunt, T. & Karsenti, E.. (1990). Triggring of cyclin degradation in interphase extracts of amphibian eggs by cdc2 kinase. Nature. 346, 379–82.CrossRefGoogle ScholarPubMed
Fraser, L.R. (1979). Rate of fertilization in vitro and subsequent nuclear development as a function of postovulatory age of the mouse egg. J. Reprod. Fert. 55, 153–60.CrossRefGoogle ScholarPubMed
Gabrielli, B.G., Roy, L.M. & Maller, J.L. (1993). Requirement for Cdk2 in cytostatic factor-mediated metaphase II arrest. Science. 259, 1766–9.CrossRefGoogle ScholarPubMed
Glotzer, M., Murray, A.. & Kirschner, M.W. (1991). Cyclin is degraded by ubiquitin pathway. Nature. 349, 132–8.CrossRefGoogle ScholarPubMed
Haccard, O., Saracevic, B., Lewellyn, A., Hartley, R., Roy, L., Izumi, T., Erikson, E. & Maller, J.L. (1993). Induction of metaphase arrest in cleaving Xenopus embryos by MAP kinase. Science. 262, 1262–5.CrossRefGoogle ScholarPubMed
Hartwell, L.H. & Weinert, T.A. (1989). Checkpoints: controls that ensure the order of cell cycle events. Science. 246, 629–34.CrossRefGoogle ScholarPubMed
Hoyt, M.A., Totis, L. & Roberts, T. (1991). S. Cerevisiae genes required for cell cycle arrest in response to loss of microtuble function. Cell. 66, 507–17.CrossRefGoogle Scholar
Kaufman, M.H. (1983). Early Mammalian Development: Parthenogenetic Studies. Cambridge: Cambridge University Press.Google Scholar
Kline, D. & Kline, J.T. (1992). Repetitive calcium transients and the role of calcium exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149, 80–9.CrossRefGoogle ScholarPubMed
Kubiak, J.Z. (1989). Mouse oocytes gradually develop the capacity for activation during the metaphase II arrest. Dev. Biol. 136, 537–45.CrossRefGoogle ScholarPubMed
Kubiak, J.Z., Weber, M., Geraud, G. & Maro, B.. (1992). Cell cycle modification during the transitions between meiotic M-phases in mouse oocytes. J. Cell Sci. 102, 457–67.CrossRefGoogle ScholarPubMed
Kubiak, J.Z., Weber, M., de Pennart, H., Winston, N.J. & Maro, B.. (1993). The metaphase II arrest in mouse oocytes is controlled through microtubule-dependent destruction of cyclin B in the presence of CSF. EMBO J. 12, 3773–8.CrossRefGoogle ScholarPubMed
Li, R. & Murray, A.W. (1991). Feedback control of mitosis in budding yeast. Cell. 66, 519–31.CrossRefGoogle ScholarPubMed
Lohka, M.J., Hayes, M.K. & Maller, J.L. (1988). Purification of maturation-promoting factor, an intracellular regulator of early mitotic events. Proc. Natl. Acad. Sci. USA. 85, 3009–13.CrossRefGoogle ScholarPubMed
Luca, F.C., Shibuya, E.K., Dohrmann, C.E. & Ruderman, J.V. (1991). Both cyclin A60 and B97 are stable and arrest cells in M-phase, but only cyclin B97 turns on cyclin destruction. EMBO J. 10, 4311–20.CrossRefGoogle Scholar
Maro, B., Johnson, M.H., Webb, M. & Flach, G. (1986). Mechanism of polar body formation in the mouse oocyte: an interaction between the chromosomes, the cytoskeleton and the plasma membrane. J. Embryol. Exp. Morphol. 92, 1132.Google ScholarPubMed
Masui, Y.. & Markert, C.L. (1971). Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 117, 129–46.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
Moses, R.M. & Masui, Y. (1992). Enhancement of nuclear formation in metaphase II mouse oocytes: synergistic action of calcium ionophore/protein synthesi inhibition. ARTA. 3, 205–12.Google Scholar
Moses, R.M. & Masui, Y. (1993). Enhancement of nuclear formation in metaphase II mouse oocytes by the synergistic action of the calcium ionophore and protein syn inhibition. In Preimplantation Embryo Development, ed. B. Bavister, p. 321. New York: Springer-Verlag.Google Scholar
Moses, R.M. & Masui, Y. (1994 a). Enhancement of mouse egg activation by the kinase inhibitor, 6-dimethylaminopurine (6-DMAP). J. Exp. Zool. 270. 211–18.CrossRefGoogle ScholarPubMed
Moses, R.M. & Masui, Y. (1994 b). Requirements for microtubule polymerization and a calcium surge for the metaphase-to-interphase transition in mature mouse oocytes. In The Cell Cycle: Regulators, Targets, and Clinical Applications, ed. Hu, V.W., pp. 237–43. New York: Plenum Press.CrossRefGoogle Scholar
Moses, R.M. & Masui, Y. (1994 c). A rapid method for whole mount preparations of mammalian oocytes and early embryos. Biotechnic Histochem. 69, 148–51.CrossRefGoogle ScholarPubMed
Moses, R.M., Kline, D. & Masui, Y. (1995). Maintenance of metaphase in colcemid-treated mouse eggs by distinct calcium-and 6-dimethylaminopurine(6-DMAP)-sensitive mechanisms. Dev. Biol. (in press).CrossRefGoogle Scholar
Newport, J.W.. & Kirschner, M.W. (1984). Regulation of the cell cycle during early Xenopus development. Cell. 37, 731–42.CrossRefGoogle ScholarPubMed
Rime, H., Neant, I., Guerrier, P. & Ozon, R. (1989). 6-Dimethylaminopurine (6-DAMP), a reversible inhibitor of the transition to metaphase during the first meiotic cell division of the mouse oocyte. Dev. Biol. 133, 169–79.CrossRefGoogle Scholar
Roberts, C.G.. & O'Neil, C. (1988). A simplified method for fixation of human and mouse preimplantation embryos which facilitates G-banding and karyotypic analysis. Hum. Reprod. 3, 990–2.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
Schatten, G., Simmerly, C. & Schatten, H. (1985). Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc. Natl. Acad. Sci. USA. 82, 4152–6.CrossRefGoogle ScholarPubMed
Schatten, H., Simmerly, C., Maul, G. & Schatten, G. (1989). Microtubule assembly is required for the formation of the pronuclei, nuclear lamin acquisition, and DNA synthesis during mouse, but not sea urchin, fertilization. Gamete Res. 23, 309–22.CrossRefGoogle Scholar
Steinhardt, R.A., Epel, D., Carroll, E.J. Jr. & Yanagimachi, R.. (1974). Is calcium ionophore a universal activator for unfertilised eggs? Nature. 252, 41–3.CrossRefGoogle ScholarPubMed
Szollosi, M.S., Debey, P., Szollosi, D., Rime, A.. & Vautier, D.. (1991). Chromatin behavior under influence of puromycin and 6-DMAP at different stages of mouse oocyte maturation. Chromosoma. 100, 339–54.CrossRefGoogle ScholarPubMed
Szollosi, M.S., Kubiak, J.Z., Debey, P., dePennart, H., Szollosi, D.. & Maro, B.. (1993). Inhibition of protein Kinases by 6-dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J. Cell Sci. 104, 861–72.CrossRefGoogle ScholarPubMed
Tarkowski, A.K.. (1966). An air-drying method of chromosome preparations from mouse eggs. Cytogenetics. 5, 394400.CrossRefGoogle Scholar
Tarkowski, A.K.. (1971). Development of single blastomeres. In Methods in Mammalian Embryology, ed. Daniel, J.C., pp 172–85. San Francisco: Freeman.Google Scholar
Vincent, C., Cheek, T.R.. & Johnson, M.H.. (1992). Cell cycle progression of parthenogentically activated mouse oocytes to interphase is dependent on the level of internal calcium. J. Cell Sci. 130, 389–96.CrossRefGoogle Scholar
Vitullo, A.D.. & Ozil, J.P.. (1992). Repetitive calcium stimuli drive meiotic resumption and pronuclear development during mouse oocyte activation. Dev.Biol. 151, 128–36.CrossRefGoogle ScholarPubMed