Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-28T18:03:21.004Z Has data issue: false hasContentIssue false
  • English
  • Français

Procaine-induced maturation of Xenopus oocytes is mediated by a transient activation of M-Phase promoting factor

Published online by Cambridge University Press:  26 September 2008

Stéphane Flament ,
Jean-François Bodart ,
Edith Browaeys ,
Marc Bertout ,
Arlette Rousseau ,
Julian Gannon  and
Jean-Pierre Vilain
Stéphane Flament*
Affiliation:
Centre de Biologie Cellulaire, Université de Lille 1, Villeneuve d'Ascq, France.
Jean-François Bodart
Affiliation:
Centre de Biologie Cellulaire, Université de Lille 1, Villeneuve d'Ascq, France.
Edith Browaeys
Affiliation:
Centre de Biologie Cellulaire, Université de Lille 1, Villeneuve d'Ascq, France.
Marc Bertout
Affiliation:
Centre de Biologie Cellulaire, Université de Lille 1, Villeneuve d'Ascq, France.
Arlette Rousseau
Affiliation:
Centre de Biologie Cellulaire, Université de Lille 1, Villeneuve d'Ascq, France.
Julian Gannon
Affiliation:
Imperial Cancer Research Fund Clare Hall Laboratories, South Mimms, Hertfordshire, UK.
Jean-Pierre Vilain
Affiliation:
Centre de Biologie Cellulaire, Université de Lille 1, Villeneuve d'Ascq, France.
*
Stéphane Flament, Centre de Biologie Cellulaire, Unité de Dynamique des cellules embryonnaires et cancéreuses, Laboratoire de Biologie du Développement, EA DRED 1033, Université de Lille 1, SN3, F-59655 Villeneuve d'Ascq cedex, France. Telephone: +33 20-43-68-67. Fax: +33 20-43-40-38. e-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

We have recently shown that the incubation of Xenopus laevis oocytes in procaine-containing solutions induced germinal vesicle breakdown without white spot formation and, in some cases, with the appearance of spindle and chromosomes in the cytoplasm. The present study was performed to determine whether M-phase promoting factor was involved in this unusual maturation. Procaine failed to induce maturation in the presence of 6-dimethylamino purine or roscovitine, which are both known to inhibit p34cdc2kinase. Histone H1 kinase activity was detected in procaine-treated oocytes but it was always lower than in progesterone-treated controls. A shift in p34cdc2 was observed in oocytes that had been exposed to procaine for 16h, but it was not detected in those exposed for 24h. Finally, cytoplasm transfer experiments demonstrated that the maturation promoting activity that occurred in oocytes incubated in procaine for 16h could induce maturation of recipient stage VI oocytes. This transferable activity was weaker than that from progesterone-treated controls since only 30% of the recipients underwent germinal vesicle breakdown and only a few spindles were observed, which were not always correctly located. Taken together these results demonstrate that M-phase promoting factor is involved in the procaine maturing effect despite some differences compared with progesterone-treated oocytes which might explain the particular type of maturation induced by this substance. The discovery of the mechanisms by which procaine is able to activate M-phase promoting factor might now help in the understanding of some steps in progesterone-induced maturation that have still to be elucidated.

Keywords

Intracellular pHMaturationMPFProcaineXenopus oocyte
Type
Article
Information
Zygote , Volume 5 , Issue 1 , February 1997 , pp. 11 - 19
Copyright
Copyright © Cambridge University Press 1997

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

Atherton-Fessler, S., Liu, F., Gabrieffi, B., Lee, M.S., Peng, C-Y. Piwnica-Worms, H. (1994). Cell cycle regulation of the p34cdc2 inhibitory kinases. Mol. Biol. Cell. 5, 989–1001.Google Scholar
Azzi, L., Meijer, L., ostvold, A.C., Lew, J. & Wang, J.H. 1994. Purification of a 15-kDa cdk4- and cdk5-binding protein. J. Biol. Chem. 269 13279–88.CrossRefGoogle ScholarPubMed
Dumont, L.W. 1972. Oogenesis in Xenopus laevis (Daudin).I. Stages of oocyte development in laboratory maintained animals. J. Morphol. 136, 153–80.Google Scholar
Flament, S., Browaeys, E., Rodeau, J.L., Bertout, M. & Vilain, J.P. 1996. Xenopus oocyte maturation: cytoplasm alkalization is involved in germinal vesicle migration. Int J Dev Riol. 40, 471–6.Google ScholarPubMed
Gerhart, J., Wu, M. & Kirschner, M. 1984. Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs. J. Cell Riol. 98, 1247–55.CrossRefGoogle ScholarPubMed
Goodger, N., Gannon, J., Hunt, T. & Morgan, P.R. 1996. On the abundance and localisation of p34cdc2 in the cells of normal, hyperplasic and malignant human lymphoid and epithelial tissues. J. Pathol. 178, 422–8.Google Scholar
Hausen, P. & Riebesell, M. 1991. The Early Development of Xenopus laevis: An Atlas of Histology. Berlin: Springer- Verlag.Google Scholar
Houle, J.G. & Wasserman, W.J. 1983. Intracellular pH plays a role in regulating protein synthesis in Xenopus oocytes. Dev. Biol. 97, 302–12.CrossRefGoogle Scholar
Huchon, D., Rime, H., Jessus, C. & Ozon, R. 1993. Control of metaphase I formation in Xenopus oocyte: effects of an indestructible cydliri B and of protein synthesis. Riol. Cell 77, 133–41.Google ScholarPubMed
Jessus, C., Rime, H., Haccard, O., VanLint, J., Goris, J., Merlevede, W. & Ozon, R. 1991.Tyrosine phosphorylation of p34cdc2 and p42 during meiotic maturation of xenopus oocyte: antagonistic action of okadaic acid and 6- DMAP. Development 111, 813–20.CrossRefGoogle ScholarPubMed
King, R.W., Jackson, P.K. & Kirschner, M.W. 1994. Mitosis in transition. Cell 79, 563–71.CrossRefGoogle ScholarPubMed
Kishimoto, T. 1994. Cell reproduction: induction of Mphase events by cyclin-dependent cdc2 kinase. Int. J. Dev. Blot. 38, 185–91.Google Scholar
Lee, S.C. & Steinhardt, R.A. 1981. pH changes associated with meiotic maturation in oocytes of Xenopus laevis. Dev. Biol. 85, 358–69.CrossRefGoogle ScholarPubMed
Masui, Y. 1992. Towards understanding the control of the division cycle in animal cells. Biochem. Cell Biot. 70, 920–45.Google Scholar
Meijer, L. & Pondaven, P. 1988. Cyclic activation of histone H1 kinase during sea urchin mitotic divisions. Exp. Cell Res. 174, 116–29.Google Scholar
Néant, I. & Guerrier, P. 1988. Meiotic reinitiation in the mollusc Patella vulgata: regulation of MPF, CSF and chromosome condensation activity by intracellular pH, protein synthesis and phosphorylation. Development 102, 505–16.CrossRefGoogle Scholar
Nebreda, A.R. & Hunt, T. 1993. The c-mos proto-oncogene protein kinase turns on and maintains the activity of MAP kinase, but not MPF, in cell-free extracts of Xenopus oocytes and eggs. EMBO J. 12, 1979–86.CrossRefGoogle Scholar
Reynhout, J.K., Smith, L.D. 1974. Studies on the appearance and nature of a maturation-inducing factor in the cytoplasm of amphibian oocytes exposed to progesterone. Den. Biol. 38, 394–400.Google Scholar
Rezai, K., Kulisz, A. & Wasserman, W.J. 1994. Protooncogene product, c-mos kinase, is involved in upregulating Na+/H+ antiporter in Xenopus oocytes Am. J. Physiol. 267, C1717–22.Google Scholar
Rime, H., Neant, I., Guerrier, P. & Ozon, R. 1989. 6-Dimethylamiriopurine (6-DMAP), a reversible inhibitor of the transition to metaphase during the first meiotic cell division of the mouse oocyte. Den. Riot. 13, 169–79.Google Scholar
Sagata, N. 1996. Meiotic metaphase arrest in animal oocytes: its mechanisms and biological significance. Trends Cell Biol. 6, 22–8.Google Scholar
Solomon, M.J. 1993. Activation of the various cyclin/cdc2 protein kinases. Curr. Opin. Cell Biol. 5, 180–6.CrossRefGoogle ScholarPubMed
Stith, B.J. & Mailer, J.L. 1984. The effect of insulin on intracellular pH and ribosomal protein S6 phosphorylation in oocytes of Xenopus laevis. Dev. Biol. 102, 79–89.Google Scholar
Vesely, J., Havlicek, L., Strand, M., Blow, J.J., Donella-Deana, A., Pinna, L., Letham, D.S., Kato, J.Y., Detivaud, L., Leclerc, S. & Meijer, L. 1994. Inhibition of cyclin-dependent kinases by purine analogues. Eur. J. Biochem. 224, 771–86.Google Scholar