Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Brief Communication
  • Published:

The APC is dispensable for first meiotic anaphase in Xenopus oocytes

Abstract

Here we show that segregation of homologous chromosomes and that of sister chromatids are differentially regulated in Xenopus and possibly in other higher eukaryotes. Upon hormonal stimulation, Xenopus oocytes microinjected with antibodies against the anaphase-promoting complex (APC) activator Fizzy or the APC core subunit Cdc27, or with the checkpoint protein Mad2, a destruction-box peptide or methylated ubiquitin, readily progress through the first meiotic cell cycle and arrest at second meiotic metaphase. However, they fail to segregate sister chromatids and remain arrested at second meiotic metaphase when electrically stimulated or when treated with ionophore A34187, two treatments that mimic fertilization and readily induce chromatid segregation in control oocytes. Thus, APC is required for second meiotic anaphase but not for first meiotic anaphase.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Xenopus oocytes microinjected with anti-FZY antibodies, the recombinant Mad2 protein or a combination of both undergo meiotic maturation and arrest at second meiotic metaphase following progesterone stimulation.
Figure 2: Oocytes microinjected with anti-FZY antibodies, recombinant Mad2, or a combination of both, fail to degrade mitotic cyclins in the first meiotic cell cycle.
Figure 3: Oocytes microinjected with anti-Cdc27 antibodies, destruction-box (D-box) peptide, methylated ubiquitin or xSecurindm mRNA undergo meiotic maturation and arrest at second meiotic metaphase following progesterone stimulation.
Figure 4: Hormone-stimulated oocytes microinjected with anti-FZY antibodies and the Mad2 checkpoint protein fail to degrade mitotic cyclins and to undergo the metaphase II to anaphase II transition upon activation.

Similar content being viewed by others

References

  1. Zachariae, W. & Nasmyth, K. Genes Dev. 13, 2039–2058 (1999).

    Article  CAS  PubMed  Google Scholar 

  2. Simchen, G. Genetics 76, 745–753 ( 1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Salah, S.M. & Nasmyth, K. Chromosoma 109, 27–34 (2000).

    Article  CAS  PubMed  Google Scholar 

  4. Lorca, T. et al. J.C. EMBO J. 17, 3565– 3575 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Fang, G., Yu, H. & Kirschner, M.W. Genes Dev. 12, 1871– 1883 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ohsumi, K., Sawada, W. & Kishimoto, T. J. Cell Sci. 107, 3305– 3013 (1994).

    Google Scholar 

  7. Huang, J. & Raff, J.W. EMBO J. 18, 2184–2195 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Clute, P. & Pines, J. Nature Cell Biol. 1, 82–87 (1999).

    Article  CAS  PubMed  Google Scholar 

  9. Furuno, H. et al. EMBO J. 13, 2399–2410 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Galas, S., Barakat, H., Doree, M. & Picard, A. Mol. Biol. Cell 4, 1295–1306 ( 1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kotani, S., Tanaka, H., Yasuda, H. & Todokoro, K. J. Cell Biol. 146, 791–800 ( 1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Fisher, D., Coux, O., Bompard-Maréchal, G. & Dorée, M. Biol. Cell 90, 497–508 ( 1998).

    Article  CAS  PubMed  Google Scholar 

  13. Schwab, M., Lutum, A.S. & Seufert, W. Cell 90, 683– 693 (1997).

    Article  CAS  PubMed  Google Scholar 

  14. Visintin, R., Prinz, S. & Amon, A. Science 278, 460– 463 (1997).

    Article  CAS  PubMed  Google Scholar 

  15. Chu, S. et al. Science 282, 699–705 (1998).

    Article  CAS  PubMed  Google Scholar 

  16. Tugendreich, S., Tomkiel, J., Earnshaw, W. & Hieter, P. Cell 81, 261–268 ( 1995).

    Article  CAS  PubMed  Google Scholar 

  17. Zou, H., McGarry, T.J., Bernal, T. & Kirschner, M.W. Science 285, 418–422 ( 1999).

    Article  CAS  PubMed  Google Scholar 

  18. Holloway, S.L., Glotzer, M., King, R.W. & Murray, A.W. Cell 73, 1393–1402 ( 1993).

    Article  CAS  PubMed  Google Scholar 

  19. Lorca, T. et al. Nature 366, 270–273 (1993).

    Article  CAS  PubMed  Google Scholar 

  20. Ciosk, R. et al. Cell 93, 1067–1076 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. Shonn, M.A., McCarroll, R. & Murray, A.W. Science 289, 300– 303 (2000).

    Article  CAS  PubMed  Google Scholar 

  22. Roeder, G.S. Genes Dev. 11, 2600–2621 (1997).

    Article  CAS  PubMed  Google Scholar 

  23. Furuta, T. et al. Mol. Biol. Cell 11 1401– 1419 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gerhart, J., Wu, M. & Kirschner, M. J. Cell Biol. 98, 1247– 1255 (1984).

    Article  CAS  PubMed  Google Scholar 

  25. Kobayashi, H. et al. J. Cell Biol. 114, 755– 765 (1991).

    Article  CAS  PubMed  Google Scholar 

  26. Rieder, C.L. & Cole, R. J. Cell Sci. 112, 2607–2613 (1999).

    CAS  PubMed  Google Scholar 

  27. Sumner, A.T. Chromosoma 100, 410–418 (1991).

    Article  CAS  PubMed  Google Scholar 

  28. Minshull, J., Sun, H., Tonks, N.K. & Murray, A.W. Cell 79, 475–486 (1994).

    Article  CAS  PubMed  Google Scholar 

  29. Nicklas, R.B. Phil. Trans. R. Soc. Lond. B 277, 267– 276 (1977).

    Article  CAS  Google Scholar 

  30. Labbe, J.C., Picard, A., Karsenti, E. & Doree, M. Dev Biol. 127, 157–169 ( 1988).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to H. Zou and M. Kirschner for providing the Securin constructs. We thank Pierre Travo, head of the IFR 24 Integrated Imaging Facility for his constant interest and support. This work was supported by grants from the Association pour la Recherche sur le Cancer and the Ligue Nationale contre le Cancer. We apologise to our collegues whose work has not been cited as a result of referencing constraints.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jean-Claude Labbé.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peter, M., Castro, A., Lorca, T. et al. The APC is dispensable for first meiotic anaphase in Xenopus oocytes . Nat Cell Biol 3, 83–87 (2001). https://doi.org/10.1038/35050607

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35050607

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing