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

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.

Ran modulates spindle assembly by regulating a subset of TPX2 and Kid activities including Aurora A activation

“…By regulating chromosome attachment to microtubules through the modulation of Kid activity, the RanGTP gradient surrounding the chromosomes would ensure the correct alignment of chromosomes upon the spindle, especially in meiotic systems, thereby ensuring the equal segregation of the genetic material into the two newly formed daughter cells. However, it is possible that Ran may regulate an uncharacterized function of Kid in the activation of MPF after germinal vesicle break down during Xenopus oocyte maturation (Perez et al, 2002). If Kid expression was inhibited during oocyte maturation, oocytes would enter an interphase like state after meiosis I, whereas, if a mutant of Kid lacking the DNA binding domain was ectopically expressed in these Kid-depleted oocytes, the oocyte could progress to meiosis II.…”

Progression through Meiosis I and Meiosis II in Arabidopsis Anthers Is Regulated by an A-Type Cyclin Predominately Expressed in Prophase I

“…This phenomenon suggests that the meiosis I-meiosis II transition does not likely involve an exit from an earlier M-phase and reentry into a subsequent M-phase, because degradation of mitotic cyclins is required for exit from M-phase in mitosis (Nurse, 2002). In fact, incomplete degradation of cyclin B at the end of meiosis I is essential for preventing the entry into S-phase in meiosis II in animals (Picard et al, 1996;Sakamoto et al, 1998;Iwabuchi et al, 2000;Taieb et al, 2001;Perez et al, 2002). In female meiosis of some animal species that normally undergo an arrest in metaphase II, depletion of cyclin B leads to the absence of the meiosis II spindle, underscoring the importance of new cyclin B synthesis for stabilizing the metaphase II spindle in these species (Hunt et al, 1992;Hochegger et al, 2001;Perez et al, 2002).…”

The anaphase-promoting complex: a key factor in the regulation of cell cycle

“…Xkid plays an important role in both meiotic and mitotic cell cycles. At meiosis, this chromokinesin is required to reactivate cyclin B/cdk1 complex after meiosis I and to inhibit DNA replication between meiosis I and meiosis II (Perez et al, 2002). At mitosis, Xkid is required during prometaphase to maintain the polar ejection force, a force that pushes chromosomes away from the pole and that mediates chromosome congression (Antonio et al, 2000;Funabiki and Murray, 2000).…”