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Xkid chromokinesin is required for the meiosis I to meiosis II transition in Xenopus laevis oocytes

Nature Cell Biology volume 4, pages 737–742 (2002)Cite this article

Abstract

Xkid chromokinesin is required for chromosome alignment on the metaphase plate of spindles formed in Xenopus laevis egg extracts. We have investigated the role of Xkid in Xenopus oocyte meiotic maturation, a progesterone-triggered process that reinitiates the meiotic cell cycle in oocytes arrested at the G2/M border of meiosis I. Here we show that Xkid starts to accumulate at the time of germinal vesicle breakdown and reaches its largest quantities at metaphase II in oocytes treated with progesterone. Both germinal vesicle breakdown and spindle assembly at meiosis I can occur normally in the absence of Xkid. But Xkid-depleted oocytes cannot reactivate Cdc2/cyclin B after meiosis I and, instead of proceeding to meiosis II, they enter an interphase-like state and undergo DNA replication. Expression of a Xkid mutant that lacks the DNA-binding domain allows Xkid-depleted oocytes to complete meiotic maturation. Our results show that Xkid has a role in the meiotic cell cycle that is independent from its role in metaphase chromosome alignment.

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Figure 1: Synthesis of Xkid is not required for entry into meiosis I in Xenopus oocytes.
Figure 2: Biochemical analysis of Xkid-depleted oocytes.
Figure 3: Xkid-depleted oocytes do not reactivate Cdc2/cyclin B after meiosis I and undergo DNA replication.
Figure 4: Absence of the meiotic spindle in Xkid-depleted oocytes.
Figure 5: Xkid is required for spindle formation in meiosis II but not meiosis I.
Figure 6: Expression of a Xkid mutant lacking the DNA-binding domain allows Xkid-depleted oocytes to enter into meiosis II.

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Acknowledgements

We thank M. Wiersma for the synthesis and purification of 3′-propanediol oligonucleotides; I. Ferby for help with preliminary Xkid antisense experiments; H. Hochegger for his protocol for visualizing the spindle in Xenopus oocytes; and S. Brunet, J. Ellenberg, G. Gutierrez and E. Karsenti for comments on the manuscript. S.F. acknowledges the use of J.-L. Merlin's microscope to get digital images of oocyte sections.

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  1. Laurent H. Perez and Celia Antonio: These authors contributed equally to this work

Authors and Affiliations

  1. European Molecular Biology Laboratory, Meyerhofstrasse 1, Heidelberg, 69117, Germany

    Laurent H. Perez, Celia Antonio, Isabelle Vernos & Angel R. Nebreda

  2. Université de Nancy 1, Génétique, Signalisation, Différenciation, BP239, Vandoeuvre les Nancy cedex, 54506, France

    Stéphane Flament

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Correspondence to Angel R. Nebreda.

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Supplementary information

Supplementary Figures and table

Fig S1a, Oocytes were injected with mRNAs encoding full-length Xkid (myc-Xkid) or a truncated Xkid mutant that lacks the C-terminal DNA binding domain (myc- XkidΔDNA-BD) and then incubated overnight in the absence (G2) or presence (MII) of progesterone. (PDF 105 kb)

Figure S2 Quantification of the meiosis II phenotypes observed by confocal microscopy in control and Xkid-depleted oocytes, as well as in Xkid-depleted oocytes that were rescued with either full-length myc-Xkid or truncated myc- XkidDNA-BD.

Table Cytological analysis of oocytes.

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Perez, L., Antonio, C., Flament, S. et al. Xkid chromokinesin is required for the meiosis I to meiosis II transition in Xenopus laevis oocytes. Nat Cell Biol 4, 737–742 (2002). https://doi.org/10.1038/ncb850

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