Abstract：
Cells dynamically remodel their internal structures by modulating the arrangement of actin filaments (AFs). In this process, individual AFs exhibit stochastic behavior without knowing the macroscopic higher-order structures they are meant to create or disintegrate, but the mechanism allowing for such stochastic process-driven remodeling of subcellular structures remains incompletely understood. Here we employ percolation theory to explore how AFs interacting only with neighboring ones without recognizing the overall configuration can nonetheless create a substantial structure referred to as stress fibers (SFs) at particular locations. We determined the interaction probabilities of AFs undergoing cellular tensional homeostasis, a fundamental property maintaining intracellular tension. We showed that the duration required for the creation of SFs is shortened by the increased amount of preexisting actin meshwork, while the disintegration occurs independently of the presence of actin meshwork, suggesting that the coexistence of tension-bearing and non-bearing elements allows cells to promptly transition to new states in accordance with transient environmental changes. The origin of this asymmetry between creation and disintegration, consistently observed in actual cells, is elucidated through a minimal model analysis by examining the intrinsic nature of mechano-signal transmission. Specifically, unlike the symmetric case involving biochemical communication, physical communication to sense environmental changes is facilitated via AFs under tension, while other free AFs dissociated from tension-bearing structures exhibit stochastic behavior. Thus, both the numerical and minimal models demonstrate the essence of intracellular percolation, in which macroscopic asymmetry observed at the cellular level emerges not from microscopic asymmetry in the interaction probabilities of individual molecules, but rather only as a consequence of the manner of the mechano-signal transmission. These results provide novel insights into the role of the mutual interplay between distinct subcellular structures with and without tension-bearing capability. Insight: Cells continuously remodel their internal elements or structural proteins in response to environmental changes. Despite the stochastic behavior of individual structural proteins, which lack awareness of the larger subcellular structures they are meant to create or disintegrate, this self-assembly process somehow occurs to enable adaptation to the environment. Here we demonstrated through percolation simulations and minimal model analyses that there is an asymmetry in the response between the creation and disintegration of subcellular structures, which can aid environmental adaptation. This asymmetry inherently arises from the nature of mechano-signal transmission through structural proteins, namely tension-mediated information exchange within cells, despite the stochastic behavior of individual proteins lacking asymmetric characters in themselves.
摘要：
细胞通过调节肌动蛋白丝（AF）的排列来动态地重塑其内部结构。在这个过程中,个体AF表现出随机行为，而不知道它们要创建或分解的宏观高阶结构，但是允许这种随机过程驱动的亚细胞结构重塑的机制仍未完全了解。在这里，我们采用渗流理论来探索AF如何仅与相邻的AF相互作用而不认识整体配置，仍然可以在特定位置创建称为应力纤维（SF）的实质性结构。我们确定了AF经历细胞张力稳态的相互作用概率，维持细胞内张力的基本属性。我们表明，SFs创建所需的持续时间因预先存在的肌动蛋白网的数量增加而缩短，虽然崩解的发生与肌动蛋白网的存在无关，这表明，张力承载和非承载元素的共存允许细胞根据瞬时环境变化迅速过渡到新的状态。创造和解体之间这种不对称的起源，在实际细胞中始终观察到，通过检查机械信号传输的内在性质，通过最小模型分析来阐明。具体来说,与涉及生化通信的对称案例不同，通过张力下的AF促进物理交流以感知环境变化，而与张力承载结构分离的其他自由AF表现出随机行为。因此，数值模型和最小模型都证明了细胞内渗滤的本质，在细胞水平上观察到的宏观不对称性不是来自单个分子相互作用概率的微观不对称性，而是仅作为机械信号传输方式的结果。这些结果为具有和不具有张力承载能力的不同亚细胞结构之间的相互作用的作用提供了新的见解。洞察力：细胞不断重塑其内部元素或结构蛋白以响应环境变化。尽管单个结构蛋白的随机行为，它们缺乏对它们要创造或分解的更大的亚细胞结构的认识，这种自组装过程以某种方式发生，以适应环境。在这里，我们通过渗流模拟和最小模型分析证明，亚细胞结构的产生和分解之间的反应存在不对称性，可以帮助环境适应。这种不对称性固有地源于通过结构蛋白的机械信号传递的性质，即细胞内紧张介导的信息交换，尽管单个蛋白质本身缺乏不对称特征的随机行为。
