Abstract
Author SummaryThe early embryonic cell cycles, which initiate cell division, mark the beginning of the life of an organism. Across different phyla, these cycles have a characteristic temporal pattern, with the first cycle being long and the subsequent cycles shorter, leading to rapid increase in cell numbers. Here we have made use of the Xenopus laevis embryos to study the mechanism and significance of this temporal transition. In X. laevis embryos, the cell cycles are driven by oscillations in the activity of the cyclin B–Cdk1 complex, which regulates cell cycle progression by protein phosphorylation. We quantified the oscillatory dynamics of key regulators in the first few embryonic cell cycles, and developed an experimentally parameterized mathematical model of the oscillations. We found that a change in the balance between the Cdk1-activating phosphatase Cdc25 and the Cdk1-inhibiting kinases Wee1 and Myt1 is critical for this transition. Tuning this balance converts the cyclin B–Cdk1 oscillator from generating spiky oscillations with delayed activation, to smooth-varying oscillations with a shorter period. Moreover, we found that it is crucial for the first embryonic cell cycle to be sufficiently long, as shortening it with drugs dramatically decreases embryo viability. Our work shows how X. laevis embryos modulate their cell cycle oscillator dynamics to meet two developmental requirements: a sufficiently long first cell cycle and rapid progression of the subsequent cycles.
Highlights
The early embryonic cell cycles mark the beginning of the life of an organism
In X. laevis embryos, the cell cycles are driven by oscillations in the activity of the cyclin B–cyclin–dependent kinase 1 (Cdk1) complex, which regulates cell cycle progression by protein phosphorylation
We quantified the oscillatory dynamics of key regulators in the first few embryonic cell cycles, and developed an experimentally parameterized mathematical model of the oscillations
Summary
The early embryonic cell cycles mark the beginning of the life of an organism. Across different phyla, including worms [1], flies [2], sea urchins [3], zebrafish [4], and frogs [5], these cycles have a characteristic temporal pattern, with the first cycle being longer and the subsequent cycles shorter. The Xenopus laevis embryo has been a fruitful model system for studies of the regulation of these early embryonic cell cycles. The Xenopus egg completes meiosis and carries out a special first mitotic cell cycle. During this cycle the male pronucleus migrates inward from the sperm entry point, the female pronucleus migrates downward from the animal pole, and the two pronuclei congress and proceed through mitosis together. Subsequent divisions occur every ,30 min in a remarkably precise fashion, with the individual cells within an embryo staying nearly synchronized and the variability in period from embryo to embryo being ,5% (Table S1). After the 12th division, the embryo proceeds through the midblastula transition, and the rapid embryonic cell cycle is converted into a slower, somatic cell cycle
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