Mitotic waves in an import-diffusion model with multiple nuclei in a shared cytoplasm

Nolet, Felix E.; Gelens, Lendert

doi:10.1016/j.biosystems.2021.104478

Cited by 3 publications

(2 citation statements)

References 41 publications

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“…Specifically, as discussed, nuclei appear to play some role in wave formation by acting as pacemakers (13,14). Modeling work demonstrates that explicit and implicit inclusion of pacemakers drives waves at the pacemaker frequency, and that the corresponding wave speed depends on this driving frequency (8,13,20–22). This suggests that compartmentalizing the cytosol and/or introducing pacemakers might affect how the system transitions over time.…”

Section: Resultsmentioning

confidence: 99%

“…Nuclei can drive wave formation by acting as pacemakers 13,14 . Modeling work demonstrates that the inclusion of pacemakers, whether explicitly or implicitly, drives waves at a frequency that correlates with pacemaker activity, with wave speed being dependent on this driving frequency 8,13,[21][22][23] . Therefore, compartmentalizing the cytosol by introducing nuclei might affect how fast the system transitions from phase to trigger waves.…”

Section: Nuclei Speed Up the Transition From Phase Waves To Trigger W...mentioning

confidence: 99%

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Mitotic waves in frog egg extracts: Transition from phase waves to trigger waves

Puls,

Ruiz-Reynés,

Tavella

et al. 2024

Preprint

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The cell cycle clock network centers on the cyclin-dependent kinase (Cdk1), such that its oscillatory rising and falling activity directs the cell through a series of steps which define one mitotic cycle. When a collection of these oscillators couple, they can synchronize. In particular, early embryogenesis is marked by a series of synchronous and fast cell divisions across the length of the embryo in various systems, e.g. Drosophila (approximately 0.5 mm in length) and Xenopus (approximately 1.2 mm in diameter). However, the large size of these embryos implies a faster coordinating effect than diffusion can control by itself. Two types of waves have been suggested as a mechanism for such spatial coordination: phase waves and trigger waves, which can be distinguished by both the speeds at which they propagate and the biochemical mechanisms behind their formation. Here, by using Xenopus laevis egg extracts and a Cdk1 FRET sensor to study the time dependence of mitotic waves, we show a transition from phase waves to trigger waves for the first time. We show how the addition of nuclei entrains the system more quickly to the trigger wave regime. We also demonstrate that the system is entrained almost immediately when metaphase-arrested extracts initiate the waves from the boundary. Finally, we complement experiments with computational modeling showing how the observed cell cycle period and wave speed depend on transient dynamics and underlying cell cycle oscillator properties. Our work argues that the transition of fast phase waves to slower trigger waves in the spatial coordination of the cell division cycle occurs as a transient effect due to the time required for trigger waves to entrain the system. Moreover, we argue that trigger waves play a role in spatial coordination, and that both phase and trigger waves are a manifestation of a common biological process undergoing these transient dynamics.

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Section: Resultsmentioning

confidence: 99%

Section: Nuclei Speed Up the Transition From Phase Waves To Trigger W...mentioning

confidence: 99%

Mitotic waves in frog egg extracts: Transition from phase waves to trigger waves

Puls,

Ruiz-Reynés,

Tavella

et al. 2024

Preprint

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Editorial: Waves in fertilization, cell division and embryogenesis

Santella

Gordon²,

Chen

et al. 2021

Biosystems

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Spatial heterogeneity accelerates phase-to-trigger wave transitions in frog egg extracts

Puls,

Ruiz-Reynés,

Tavella

et al. 2024

Nat Commun

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Cyclin-dependent kinase 1 (Cdk1) activity rises and falls throughout the cell cycle: a cell-autonomous process called mitotic oscillations. Mitotic oscillators can synchronize when spatially coupled, facilitating rapid, synchronous divisions in large early embryos of Drosophila (~0.5 mm) and Xenopus (~1.2 mm). Diffusion alone cannot achieve such long-range coordination. Instead, studies proposed mitotic waves—phase and trigger waves—as mechanisms of the coordination. How waves establish over time remains unclear. Using Xenopus laevis egg extracts and a Cdk1 Förster resonance energy transfer sensor, we observe a transition from phase to trigger wave dynamics in initially homogeneous cytosol. Spatial heterogeneity promotes this transition. Adding nuclei accelerates entrainment. The system transitions almost immediately when driven by metaphase-arrested extracts. Numerical simulations suggest phase waves appear transiently as trigger waves take time to entrain the system. Therefore, we show that both waves belong to a single biological process capable of coordinating the cell cycle over long distances.

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Mitotic waves in an import-diffusion model with multiple nuclei in a shared cytoplasm

Cited by 3 publications

References 41 publications

Mitotic waves in frog egg extracts: Transition from phase waves to trigger waves

Mitotic waves in frog egg extracts: Transition from phase waves to trigger waves

Editorial: Waves in fertilization, cell division and embryogenesis

Spatial heterogeneity accelerates phase-to-trigger wave transitions in frog egg extracts

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