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:

Rough Deal and Zw10 are required for the metaphase checkpoint in Drosophila

Abstract

The metaphase–anaphase transition during mitosis is carefully regulated in order to assure high-fidelity transmission of genetic information to the daughter cells. A surveillance mechanism known as the metaphase checkpoint (or spindle-assembly checkpoint) monitors the attachment of kinetochores to the spindle microtubules, and inhibits anaphase onset until all chromosomes have achieved a proper bipolar orientation on the spindle. Defects in this checkpoint lead to premature anaphase onset, and consequently to greatly increased rates of aneuploidy. Here we show that the Drosophila kinetochore components Rough deal (Rod) and Zeste-White 10 (Zw10) are required for the proper functioning of the metaphase checkpoint in flies. Drosophila cells lacking either ROD or Zw10 exhibit a phenotype that is similar to that of bub1 mutants — they do not arrest in metaphase in response to spindle damage, but instead separate sister chromatids, degrade cyclin B and exit mitosis. These are the first checkpoint components to be identified that do not have obvious homologues in budding yeast.

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: The metaphase-arrest phenotype of asp is suppressed by rod .
Figure 2: Premature cyclin B degradation in colchicine-treated and untreated rod and zw10 mutant neuroblasts.

Similar content being viewed by others

References

  1. Rieder, C. L., Schultz, A., Cole, R. & Sluder, G. J. Cell Biol. 127, 1301–1310 ( 1994).

    Article  CAS  Google Scholar 

  2. Amon, A. Curr. Opin. Genet. Dev. 9, 69–75 (1999).

    Article  CAS  Google Scholar 

  3. Gorbsky, G. J., Kallio, M., Daum, J. R. & Topper, L. M. Faseb J. 13, S231–S234 ( 1999).

    Article  CAS  Google Scholar 

  4. Cohen-Fix, O., Peters, J. M., Kirschner, M. W. & Koshland, D. Genes Dev. 10, 3081–3093 (1996).

    Article  CAS  Google Scholar 

  5. Funabiki, H. et al. Nature 381, 438–441 (1996).

    Article  CAS  Google Scholar 

  6. Sudakin, V. et al. Mol. Biol. Cell 6, 185– 197 (1995).

    Article  CAS  Google Scholar 

  7. King, R. W. et al. Cell 81, 279–288 (1995).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Taylor, S. S. & McKeon, F. Cell 89, 727–735 (1997).

    Article  CAS  Google Scholar 

  11. Taylor, S. S., Ha, E. & McKeon, F. J. Cell Biol. 142, 1– 11 (1998).

    Article  CAS  Google Scholar 

  12. Li, Y., Gorbea, C., Mahaffey, D., Rechsteiner, M. & Benezra, R. Proc. Natl Acad. Sci. USA 94, 12431–12436 ( 1997).

    Article  CAS  Google Scholar 

  13. Basu, J. et al. Chromosoma 107, 376–385 (1998).

    Article  CAS  Google Scholar 

  14. Basu, J. et al. J. Cell Biol. 146, 13– 28 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Cahill, D. P. et al. Nature 392, 300–303 (1998).

    Article  CAS  Google Scholar 

  16. Karess, R. E. & Glover, D. M. J. Cell Biol. 109, 2951–2961 (1989).

    Article  CAS  Google Scholar 

  17. Williams, B. C., Karr, T. L., Montgomery, J. M. & Goldberg, M. L. J. Cell Biol. 118, 759– 773 (1992).

    Article  CAS  Google Scholar 

  18. Starr, D. A. et al. J Cell Biol 138, 1289– 1301 (1997).

    Article  CAS  Google Scholar 

  19. Scaërou, F. et al. J. Cell Sci. 112, 3757– 3768 (1999).

    PubMed  Google Scholar 

  20. Williams, B. C., Gatti, M. & Goldberg, M. L. J Cell Biol 134, 1127–1140 (1996).

    Article  CAS  Google Scholar 

  21. Williams, B. C. & Goldberg, M. L. J. Cell Sci. 107, 785–798 ( 1994).

    CAS  PubMed  Google Scholar 

  22. Scaërou, F. et al. The Zw10 and rough deal gene products are in a large, evolutionarily conserved complex targeted to the leinetochore (submitted) .

  23. Starr, D. A., Williams, B. C., Hays, T. S. & Goldberg, M. L. J. Cell Biol. 142, 763–774 (1998).

    Article  CAS  Google Scholar 

  24. Saunders, R. D., Avides, M. C., Howard, T., Gonzalez, C. & Glover, D. M. J. Cell Biol. 137, 881–890 (1997).

    Article  CAS  Google Scholar 

  25. Gonzalez, C. et al. J. Cell Sci. 96, 605– 616 (1990).

    PubMed  Google Scholar 

  26. Gonzalez, C., Sunkel, C. E. & Glover, D. M. Chromosoma 107, 452– 460 (1998).

    Article  CAS  Google Scholar 

  27. do Carmo Avides, M. & Glover, D. M. Science 283, 1733–1735 (1999).

    Article  CAS  Google Scholar 

  28. Straight, A. F., Marshall, W. F., Sedat, J. W. & Murray, A. W. Science 277, 574– 578 (1997).

    Article  CAS  Google Scholar 

  29. Chan, G. K. T., Jablonski, S. A., Starr, D., Goldberg, M. L. & Yen, T. J. Nature Cell Biol. 2, 944–947 ( 2000).

    Article  CAS  Google Scholar 

  30. Echeverri, C. J., Paschal, B. M., Vaughan, K. T. & Vallee, R. B. J. Cell Biol. 132, 617– 633 (1996).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Lehner for anti-cyclin B antibody, C. Gonzalez for the asp mutant, and M.Goldberg and B. Williams for the bub1 mutant, as well as for their encouragement and advice. We also thank F. Scaerou for helpful discussions, suggestions and encouragement. This work was carried out at the UPR 2420 Centre de Génétique Moléculaire of the CNRS, associated with the Université Pierre et Marie Curie, and was supported in part by grants to R.K. from the CNRS and from the Association Pour la Recherche sur le Cancer (France). R.B. was supported by grants BD/11488/97 and P/BIA/111055/1998 from FCT, Portugal.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roger E. Karess.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Basto, R., Gomes, R. & Karess, R. Rough Deal and Zw10 are required for the metaphase checkpoint in Drosophila. Nat Cell Biol 2, 939–943 (2000). https://doi.org/10.1038/35046592

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35046592

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