Department of Mechanical and Aerospace Engineering, University of California, San Diego, La Jolla, CA 92093, USA.
Department of Pharmacology, School of Medicine, University of California, San Diego, La Jolla, CA 92093, USA.
J Cell Sci. 2024 Sep 1;137(17). doi: 10.1242/jcs.261782. Epub 2024 Sep 9.
Mechanotransduction, which is the integration of mechanical signals from the external environment of a cell to changes in intracellular signaling, governs many cellular functions. Recent studies have shown that the mechanical state of the cell is also coupled to the cellular circadian clock. To investigate possible interactions between circadian rhythms and cellular mechanotransduction, we have developed a computational model that integrates the two pathways. We postulated that translocation of the transcriptional regulators MRTF (herein referring to both MRTF-A and MRTF-B), YAP and TAZ (also known as YAP1 and WWTR1, respectively; collectively denoted YAP/TAZ) into the nucleus leads to altered expression of circadian proteins. Simulations from our model predict that lower levels of cytoskeletal activity are associated with longer circadian oscillation periods and higher oscillation amplitudes, which is consistent with recent experimental observations. Furthermore, accumulation of YAP/TAZ and MRTF in the nucleus causes circadian oscillations to decay in our model. These effects hold both at the single-cell level and within a population-level framework. Finally, we investigated the effects of mutations in YAP or lamin A, the latter of which result in a class of diseases known as laminopathies. In silico, oscillations in circadian proteins are substantially weaker in populations of cells with mutations in YAP or lamin A, suggesting that defects in mechanotransduction can disrupt the circadian clock in certain disease states; however, reducing substrate stiffness in the model restores normal oscillatory behavior, suggesting a possible compensatory mechanism. Thus, our study identifies that mechanotransduction could be a potent modulatory cue for cellular clocks and that this crosstalk can be leveraged to rescue the circadian clock in disease states.
力学转导,即细胞外环境的机械信号整合到细胞内信号变化中,控制着许多细胞功能。最近的研究表明,细胞的力学状态也与细胞的生物钟耦合。为了研究生物钟和细胞力学转导之间可能存在的相互作用,我们开发了一个整合这两个途径的计算模型。我们假设转录调节因子 MRTF(这里指 MRTF-A 和 MRTF-B)、YAP 和 TAZ(也分别称为 YAP1 和 WWTR1,统称 YAP/TAZ)的核易位导致生物钟蛋白表达的改变。我们的模型模拟预测,细胞骨架活性降低与生物钟振荡周期延长和振幅增加有关,这与最近的实验观察结果一致。此外,在我们的模型中,YAP/TAZ 和 MRTF 在核内的积累导致生物钟振荡衰减。这些效应在单细胞水平和群体水平框架内都成立。最后,我们研究了 YAP 或 lamin A 突变的影响,后者导致一类称为层粘连蛋白病的疾病。在计算机模拟中,YAP 或 lamin A 突变的细胞群体中生物钟蛋白的振荡明显减弱,表明力学转导缺陷可能在某些疾病状态下破坏生物钟;然而,在模型中降低基质刚度可以恢复正常的振荡行为,表明存在一种可能的补偿机制。因此,我们的研究表明力学转导可能是细胞时钟的一个有力调节信号,这种串扰可以在疾病状态下用于拯救生物钟。