How Does the Xenopus laevis Embryonic Cell Cycle Avoid Spatial Chaos?

Lendert Gelens,Kerwyn Casey Huang,James E Ferrell

doi:10.1016/j.celrep.2015.06.070

Lendert Gelens, Kerwyn Casey Huang + Show 1 more

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https://doi.org/10.1016/j.celrep.2015.06.070

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Journal: Cell Reports	Publication Date: Jul 23, 2015
Citations: 19	License type: cc-by

Affiliation: Vrije Universiteit Brussel, Stanford University

Abstract

Theoretical studies have shown that a deterministic biochemical oscillator can become chaotic when operating over a sufficiently large volume and have suggested that the Xenopus laevis cell cycle oscillator operates close to such a chaotic regime. To experimentally test this hypothesis, we decreased the speed of the post-fertilization calcium wave, which had been predicted to generate chaos. However, cell divisions were found to develop normally, and eggs developed into normal tadpoles. Motivated by these experiments, we carried out modeling studies to understand the prerequisites for the predicted spatial chaos. We showed that this type of spatial chaos requires oscillatory reaction dynamics with short pulse duration and postulated that the mitotic exit in Xenopus laevis is likely slow enough to avoid chaos. In systems with shorter pulses, chaos may be an important hazard, as in cardiac arrhythmias, or a useful feature, as in the pigmentation of certain mollusk shells.

Highlights

In the amphibian Xenopus laevis, embryogenesis begins when the sperm penetrates the cell cycle-arrested egg, initiating a wave of elevated cytoplasmic calcium that brings about the completion of meiosis II, and allows the mitotic cell cycles to begin (Gerhart, 1980; Hausen and Riebesell, 1991)
We found that the model becomes most susceptible to transitions into chaos when the cell cycle oscillations have a very short pulse duration of cyclin-dependent kinase 1 (Cdk1) activation, probably shorter than in the physiological case (Pomerening et al, 2003; Tsai et al, 2014; Yang and Ferrell, 2013)
Xenopus embryos with slow calcium waves show no evidence of chaotic cell division We hypothesized that one way to slow the initial calcium wave would be to transiently cool the fertilized egg

Summary

Introduction

In the amphibian Xenopus laevis, embryogenesis begins when the sperm penetrates the cell cycle-arrested egg, initiating a wave of elevated cytoplasmic calcium that brings about the completion of meiosis II, and allows the mitotic cell cycles to begin (Gerhart, 1980; Hausen and Riebesell, 1991). The first mitotic cleavage occurs approximately 85 min after fertilization, and is followed by 11 rapid, 25-min cell cycles that lead up to the mid-blastula transition. These rapid early embryonic cell cycles are remarkably regular, with the cell cycle period varying little from cycle to cycle and from cell to cell. These cell cycle oscillations are driven by a biochemical oscillator circuit centered on the cyclin B-cyclin-dependent kinase 1 (Cdk1) complex (Minshull et al, 1989; Murray and Kirschner, 1989). The strengths and response functions of the different feedback loops have been experimentally measured using Xenopus extracts (Kim and Ferrell, 2007; Pomerening et al, 2005; Pomerening et al, 2003; Trunnell et al, 2011; Tsai et al, 2014; Yang and Ferrell, 2013), providing a detailed quantitative accounting of the biochemical reactions of the cell cycle oscillator

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