Popov Konstantin, Komianos James, Papoian Garegin A
Department of Chemistry and Biochemistry, University of Maryland, College Park, Maryland, United States of America.
Institute for Physical Science and Technology, University of Maryland, College Park, Maryland, United States of America.
PLoS Comput Biol. 2016 Apr 27;12(4):e1004877. doi: 10.1371/journal.pcbi.1004877. eCollection 2016 Apr.
Active matter systems, and in particular the cell cytoskeleton, exhibit complex mechanochemical dynamics that are still not well understood. While prior computational models of cytoskeletal dynamics have lead to many conceptual insights, an important niche still needs to be filled with a high-resolution structural modeling framework, which includes a minimally-complete set of cytoskeletal chemistries, stochastically treats reaction and diffusion processes in three spatial dimensions, accurately and efficiently describes mechanical deformations of the filamentous network under stresses generated by molecular motors, and deeply couples mechanics and chemistry at high spatial resolution. To address this need, we propose a novel reactive coarse-grained force field, as well as a publicly available software package, named the Mechanochemical Dynamics of Active Networks (MEDYAN), for simulating active network evolution and dynamics (available at www.medyan.org). This model can be used to study the non-linear, far from equilibrium processes in active matter systems, in particular, comprised of interacting semi-flexible polymers embedded in a solution with complex reaction-diffusion processes. In this work, we applied MEDYAN to investigate a contractile actomyosin network consisting of actin filaments, alpha-actinin cross-linking proteins, and non-muscle myosin IIA mini-filaments. We found that these systems undergo a switch-like transition in simulations from a random network to ordered, bundled structures when cross-linker concentration is increased above a threshold value, inducing contraction driven by myosin II mini-filaments. Our simulations also show how myosin II mini-filaments, in tandem with cross-linkers, can produce a range of actin filament polarity distributions and alignment, which is crucially dependent on the rate of actin filament turnover and the actin filament's resulting super-diffusive behavior in the actomyosin-cross-linker system. We discuss the biological implications of these findings for the arc formation in lamellipodium-to-lamellum architectural remodeling. Lastly, our simulations produce force-dependent accumulation of myosin II, which is thought to be responsible for their mechanosensation ability, also spontaneously generating myosin II concentration gradients in the solution phase of the simulation volume.
活性物质系统,尤其是细胞骨架,展现出复杂的机械化学动力学,目前人们对此仍未完全理解。虽然先前关于细胞骨架动力学的计算模型已经带来了许多概念性的见解,但仍有一个重要的空白需要用一个高分辨率的结构建模框架来填补,该框架包括一套最小完整的细胞骨架化学体系,能在三个空间维度上随机处理反应和扩散过程,能准确且高效地描述在分子马达产生的应力作用下丝状网络的机械变形,并在高空间分辨率下深度耦合力学和化学。为满足这一需求,我们提出了一种新颖的反应性粗粒化力场,以及一个名为活性网络机械化学动力学(MEDYAN)的公开可用软件包,用于模拟活性网络的演化和动力学(可在www.medyan.org获取)。该模型可用于研究活性物质系统中的非线性、远离平衡的过程,特别是由嵌入具有复杂反应扩散过程的溶液中的相互作用半柔性聚合物组成的系统。在这项工作中,我们应用MEDYAN来研究由肌动蛋白丝、α - 辅肌动蛋白交联蛋白和非肌肉肌球蛋白IIA微丝组成的收缩性肌动球蛋白网络。我们发现,当交联剂浓度增加到阈值以上时,这些系统在模拟中会经历从随机网络到有序、成束结构的类似开关的转变,从而引发由肌球蛋白II微丝驱动的收缩。我们的模拟还展示了肌球蛋白II微丝与交联剂协同作用如何能产生一系列肌动蛋白丝极性分布和排列,这关键取决于肌动蛋白丝周转速率以及肌动蛋白丝在肌动球蛋白 - 交联剂系统中产生的超扩散行为。我们讨论了这些发现对片足到片层结构重塑中弧形形成的生物学意义。最后,我们的模拟产生了与力相关的肌球蛋白II积累,这被认为是其机械传感能力的原因,同时在模拟体积的溶液相中也自发产生了肌球蛋白II浓度梯度。