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

Author

Listed:
  • Owen Puls

    (University of Michigan
    University of Michigan)

  • Daniel Ruiz-Reynés

    (Department of Cellular and Molecular Medicine, University of Leuven
    IFISC (CSIC-UIB). Instituto de Física Interdisciplinar y Sistemas Complejos)

  • Franco Tavella

    (University of Michigan
    University of Michigan)

  • Minjun Jin

    (University of Michigan
    University of Michigan)

  • Yeonghoon Kim

    (University of Michigan)

  • Lendert Gelens

    (Department of Cellular and Molecular Medicine, University of Leuven)

  • Qiong Yang

    (University of Michigan
    University of Michigan
    University of Michigan)

Abstract

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.

Suggested Citation

  • Owen Puls & Daniel Ruiz-Reynés & Franco Tavella & Minjun Jin & Yeonghoon Kim & Lendert Gelens & Qiong Yang, 2024. "Spatial heterogeneity accelerates phase-to-trigger wave transitions in frog egg extracts," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54752-7
    DOI: 10.1038/s41467-024-54752-7
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    References listed on IDEAS

    as
    1. Johanna Bischof & Christoph A. Brand & Kálmán Somogyi & Imre Májer & Sarah Thome & Masashi Mori & Ulrich S. Schwarz & Péter Lénárt, 2017. "A cdk1 gradient guides surface contraction waves in oocytes," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    2. Zhanghan Wu & Maohan Su & Cheesan Tong & Min Wu & Jian Liu, 2018. "Membrane shape-mediated wave propagation of cortical protein dynamics," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Jeremy B. Chang & James E. Ferrell Jr, 2013. "Mitotic trigger waves and the spatial coordination of the Xenopus cell cycle," Nature, Nature, vol. 500(7464), pages 603-607, August.
    Full references (including those not matched with items on IDEAS)

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