Department of Biomedical Engineering, University of California, Irvine, Irvine, California, United States of America.
UCI Edwards Lifesciences Foundation Cardiovascular Innovation and Research Center (CIRC), University of California, Irvine, Irvine, California, United States of America.
PLoS Comput Biol. 2024 Aug 5;20(8):e1012321. doi: 10.1371/journal.pcbi.1012321. eCollection 2024 Aug.
Understanding muscle contraction mechanisms is a standing challenge, and one of the approaches has been to create models of the sarcomere-the basic contractile unit of striated muscle. While these models have been successful in elucidating many aspects of muscle contraction, they fall short in explaining the energetics of functional phenomena, such as rigor, and in particular, their dependence on the concentrations of the biomolecules involved in the cross-bridge cycle. Our hypothesis posits that the stochastic time delay between ATP adsorption and ADP/Pi release in the cross-bridge cycle necessitates a modeling approach where the rates of these two reaction steps are controlled by two independent parts of the total free energy change of the hydrolysis reaction. To test this hypothesis, we built a two-filament, stochastic-mechanical half-sarcomere model that separates the energetic roles of ATP and ADP/Pi in the cross-bridge cycle's free energy landscape. Our results clearly demonstrate that there is a nontrivial dependence of the cross-bridge cycle's kinetics on the independent concentrations of ATP, ADP, and Pi. The simplicity of the proposed model allows for analytical solutions of the more basic systems, which provide novel insight into the dominant mechanisms driving some of the experimentally observed contractile phenomena.
理解肌肉收缩机制是一个长期存在的挑战,其中一种方法是创建肌节模型——横纹肌的基本收缩单位。虽然这些模型在阐明肌肉收缩的许多方面取得了成功,但它们在解释功能现象的能量学方面存在不足,例如僵硬,特别是它们对参与横桥循环的生物分子浓度的依赖性。我们的假设假设,在横桥循环中,ATP 吸附和 ADP/Pi 释放之间的随机时间延迟需要一种建模方法,其中这两个反应步骤的速率由水解反应总自由能变化的两个独立部分控制。为了验证这个假设,我们构建了一个双丝、随机力学半肌节模型,该模型将 ATP 和 ADP/Pi 在横桥循环自由能景观中的能量作用分开。我们的结果清楚地表明,横桥循环的动力学对 ATP、ADP 和 Pi 的独立浓度有重要的依赖关系。所提出的模型的简单性允许对更基本系统的解析解,这为一些实验观察到的收缩现象的主导机制提供了新的见解。