Light-induced cortical excitability reveals programmable shape dynamics in starfish oocytes

Jinghui Liu, Tom Burkart, Alexander Ziepke, John Reinhard, Yu-Chen Chao, Tzer Han Tan, S. Zachary Swartz, Erwin Frey, Nikta Fakhri
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Abstract

Chemo-mechanical waves on active deformable surfaces are a key component for many vital cellular functions. In particular, these waves play a major role in force generation and long-range signal transmission in cells that dynamically change shape, as encountered during cell division or morphogenesis. Reconstituting and controlling such chemically controlled cell deformations is a crucial but unsolved challenge for the development of synthetic cells. Here, we develop an optogenetic method to elucidate the mechanism responsible for coordinating surface contraction waves that occur in oocytes of the starfish Patiria miniata during meiotic cell division. Using spatiotemporally-patterned light stimuli as a control input, we create chemo-mechanical cortical excitations that are decoupled from meiotic cues and drive diverse shape deformations ranging from local pinching to surface contraction waves and cell lysis. We develop a quantitative model that entails the hierarchy of chemical and mechanical dynamics, which allows to relate the variety of mechanical responses to optogenetic stimuli. Our framework systematically predicts and explains transitions of programmed shape dynamics. Finally, we qualitatively map the observed shape dynamics to elucidate how the versatility of intracellular protein dynamics can give rise to a broad range of mechanical phenomenologies. More broadly, our results pave the way toward real-time control over dynamical deformations in living organisms and can advance the design of synthetic cells and life-like cellular functions.
光诱导皮层兴奋性揭示了海星卵母细胞的可编程形状动力学
活性可变形表面上的化学机械波是许多重要细胞功能的关键组成部分。特别是在细胞分裂或形态发生过程中,这些波在动态改变形状的细胞中起着产生力和远距离信号传输的重要作用。重建和控制这种化学控制的细胞变形是开发合成细胞的一个关键但尚未解决的挑战。在这里,我们开发了一种光遗传学方法来阐明海星(Patiria miniata)卵母细胞在减数分裂过程中发生的表面收缩波的协调机制。利用时空图案光刺激作为控制输入,我们产生了与减数分裂线索脱钩的化学机械皮层兴奋,并驱动了从局部挤压到表面收缩波和细胞溶解等各种形状的变形。我们建立了一个包含化学和机械动力学层次的定量模型,可以将各种机械反应与光遗传刺激联系起来。我们的框架系统地预测并解释了程序化形状动力学的转变。最后,我们对观察到的形状动力学进行了定性描绘,以阐明细胞内蛋白质动力学的多功能性是如何产生各种机械现象的。更广泛地说,我们的研究成果为实时控制生物体内的动态变形铺平了道路,并能推动合成细胞和类生命细胞功能的设计。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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