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:

Site of the previous meiotic division defines cleavage orientation in the mouse embryo

An Erratum to this article was published on 01 November 2002

Abstract

The conservation of early cleavage patterns in organisms as diverse as echinoderms and mammals suggests that even in highly regulative embryos such as the mouse, division patterns might be important for development1,2,3,4. Indeed, the first cleavage divides the fertilized mouse egg into two cells: one cell that contributes predominantly to the embryonic part of the blastocyst, and one that contributes to the abembryonic part5,6. Here we show, by removing, transplanting or duplicating the animal or vegetal poles of the mouse egg, that a spatial cue at the animal pole orients the plane of this initial division. Embryos with duplicated animal, but not vegetal, poles show abnormalities in chromosome segregation that compromise their development. Our results show that localized factors in the mammalian egg orient the spindle and so define the initial cleavage plane. In increased dosage, however, these factors are detrimental to the correct execution of division.

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 animal pole defines the first cleavage plane of the zygote.
Figure 2: Embryos with two animal poles, but not two vegetal poles, cleave with respect to the position of either or both poles.
Figure 3: Chromatin bridging appears in AA embryos irrespective of the position of the ectopic A pole.
Figure 4: Associations between the zygotic spindle and the second meiotic mid-body.

Similar content being viewed by others

References

  1. Gulyas, B. J. J. Exp. Zool. 193, 235–248 (1975).

    Article  CAS  PubMed  Google Scholar 

  2. Graham, C. F & Deussen, Z. A. J. Embryol. Exp. Morphol. 48, 53–72 (1978).

    CAS  PubMed  Google Scholar 

  3. Ciemerych, M. A., Mesnard, D. & Zernicka-Goetz, M. Development 127, 3467–3474 (2000).

    CAS  PubMed  Google Scholar 

  4. Zernicka-Goetz, M. Development 129, 815–829 (2002).

    CAS  PubMed  Google Scholar 

  5. Piotrowska, K. & Zernicka-Goetz, M. Nature 409, 517–521 (2001).

    Article  CAS  PubMed  Google Scholar 

  6. Piotrowska, K., Wianny, F., Pedersen, R. A. & Zernicka-Goetz, M. Development 128, 3739–3748 (2001).

    CAS  PubMed  Google Scholar 

  7. Weber, R. J., Pedersen, R. A., Wianny, F., Evans, M. J. & Zernicka-Goetz, M. Development 126, 5591–5598 (1999).

    CAS  PubMed  Google Scholar 

  8. Zernicka-Goetz, M. et. al. Development 124, 1133–1137 (1997).

    CAS  PubMed  Google Scholar 

  9. Antczak, M. & Van Blerkom, J. Mol. Hum. Repr. 12, 1067–1086 (1997).

    Article  Google Scholar 

  10. Plusa, B., Piotrowska, K. & Zernicka-Goetz, M. Genesis 32,193–198 (2002).

    Article  PubMed  Google Scholar 

  11. Davies, T. J. & Gardner, R. L. Hum. Reprod. 17, 2368–2379 (2002).

    Article  CAS  PubMed  Google Scholar 

  12. Bloom, K. Curr. Biol. 11, R326–R329 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Hyman, A. A. J. Cell Biol. 3, 1185–1193 (1989).

    Article  Google Scholar 

  14. Skop, A. R. & White, J. G. Curr. Biol. 8, 1110–1106 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Busson, S., Dujardin, D., Moreau, A., Dompierre, J. & De Mey, J. R. Curr. Biol. 8, 541–544 (1998).

    Article  CAS  PubMed  Google Scholar 

  16. Dujardin, D. L. & Vallee, R. B. Curr. Opin. Cell Biol. 14, 44–49 (2002).

    Article  CAS  Google Scholar 

  17. Zernicka-Goetz, M. Development 125, 4803–4808 (1998).

    CAS  PubMed  Google Scholar 

  18. McGrath, J. & Solter, D. Science 220, 1300–1302 (1983).

    Article  CAS  PubMed  Google Scholar 

  19. Brunet, S., Polanski, Z., Verlhac, M.-H., Kubiak, J. Z. & Maro, B. Curr. Biol. 8, 1231–1234 (1998).

    Article  CAS  PubMed  Google Scholar 

  20. Wianny, F., Tavares, A., Evans, M. J., Glover, D. M. & Zernicka-Goetz, M. Chromosoma 107, 430–439 (1998).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank L. Clayton for some of the earlier immunostaining of mouse embryos, and S. Frankenberg, M. Savoian, J. Pines, A. Brand and J. Ahringer for discussions. This work was supported by the Wellcome Trust (M.Z.-G.), Cancer Research UK (D.M.G.) and the Biotechnology and Biological Science Research Council (M.Z.-G. and D.M.G.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Magdalena Zernicka-Goetz.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary tables

Table 1. Position of the external marker with respect to the first cleavage plane following removal of the animal or vegetal poles. (PDF 22 kb)

Table 2. Association of cleavage plane with ectopic polar body transplanted at either G2 or M phase.

Table 3. Development of embryos with two animal or two vegetal poles

Rights and permissions

Reprints and permissions

About this article

Cite this article

Plusa, B., Grabarek, J., Piotrowska, K. et al. Site of the previous meiotic division defines cleavage orientation in the mouse embryo. Nat Cell Biol 4, 811–815 (2002). https://doi.org/10.1038/ncb860

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ncb860

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