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Modeling multicellular dynamics regulated by extracellular-matrix-mediated mechanical communication via active particles with polarized effective attraction
Physical Review E ( IF 2.4 ) Pub Date : 2020-11-20 , DOI: 10.1103/physreve.102.052409 Yu Zheng 1 , Qihui Fan 2, 3 , Christopher Z Eddy 4 , Xiaochen Wang 2, 3 , Bo Sun 4 , Fangfu Ye 2, 3, 5 , Yang Jiao 1, 6
Physical Review E ( IF 2.4 ) Pub Date : 2020-11-20 , DOI: 10.1103/physreve.102.052409 Yu Zheng 1 , Qihui Fan 2, 3 , Christopher Z Eddy 4 , Xiaochen Wang 2, 3 , Bo Sun 4 , Fangfu Ye 2, 3, 5 , Yang Jiao 1, 6
Affiliation
Collective cell migration is crucial to many physiological and pathological processes such as embryo development, wound healing, and cancer invasion. Recent experimental studies have indicated that the active traction forces generated by migrating cells in a fibrous extracellular matrix (ECM) can mechanically remodel the ECM, giving rise to bundlelike mesostructures bridging individual cells. Such fiber bundles also enable long-range propagation of cellular forces, leading to correlated migration dynamics regulated by the mechanical communication among the cells. Motivated by these experimental discoveries, we develop an active-particle model with polarized effective attractions (APPA) to investigate emergent multicellular migration dynamics resulting from ECM-mediated mechanical communications. In particular, the APPA model generalizes the classic active-Brownian-particle (ABP) model by imposing a pairwise polarized attractive force between the particles, which depends on the instantaneous dynamic states of the particles and mimics the effective mutual pulling between the cells via the fiber bundle bridge. The APPA system exhibits enhanced aggregation behaviors compared to the classic ABP system, and the contrast is more apparent at lower particle densities and higher rotational diffusivities. Importantly, in contrast to the classic ABP system where the particle velocities are not correlated for all particle densities, the high-density phase of the APPA system exhibits strong dynamic correlations, which are characterized by the slowly decaying velocity correlation functions with a correlation length comparable to the linear size of the high-density phase domain (i.e., the cluster of particles). The strongly correlated multicellular dynamics predicted by the APPA model is subsequently verified in in vitro experiments using MCF-10A cells. Our studies indicate the importance of incorporating ECM-mediated mechanical coupling among the migrating cells for appropriately modeling emergent multicellular dynamics in complex microenvironments.
中文翻译:
通过具有极化有效吸引力的活性粒子模拟由细胞外基质介导的机械通讯调节的多细胞动力学
集体细胞迁移对许多生理和病理过程至关重要,例如胚胎发育、伤口愈合和癌症侵袭。最近的实验研究表明,在纤维细胞外基质 (ECM) 中迁移细胞所产生的主动牵引力可以机械地重塑 ECM,从而产生桥接单个细胞的束状细观结构。这种纤维束还可以实现细胞力的长距离传播,从而导致由细胞之间的机械通讯调节的相关迁移动力学。受这些实验发现的启发,我们开发了一种具有极化有效吸引力 (APPA) 的活性粒子模型,以研究由 ECM 介导的机械通信引起的紧急多细胞迁移动力学。特别是,APPA 模型通过在粒子之间施加成对极化吸引力来概括经典的活性布朗粒子 (ABP) 模型,该吸引力取决于粒子的瞬时动态状态并模拟细胞之间通过纤维束桥的有效相互牵引. 与经典的 ABP 系统相比,APPA 系统表现出增强的聚集行为,并且在较低的粒子密度和较高的旋转扩散率下对比更加明显。重要的是,与经典的 ABP 系统相比,在经典 ABP 系统中,所有粒子密度的粒子速度都不相关,APPA 系统的高密度相表现出很强的动态相关性,其特征在于缓慢衰减的速度相关函数,其相关长度与高密度相域(即粒子簇)的线性尺寸相当。APPA 模型预测的强相关多细胞动力学随后在使用 MCF-10A 细胞进行体外实验。我们的研究表明在迁移细胞之间结合 ECM 介导的机械耦合对于在复杂微环境中适当地模拟紧急多细胞动力学的重要性。
更新日期:2020-11-21
中文翻译:
通过具有极化有效吸引力的活性粒子模拟由细胞外基质介导的机械通讯调节的多细胞动力学
集体细胞迁移对许多生理和病理过程至关重要,例如胚胎发育、伤口愈合和癌症侵袭。最近的实验研究表明,在纤维细胞外基质 (ECM) 中迁移细胞所产生的主动牵引力可以机械地重塑 ECM,从而产生桥接单个细胞的束状细观结构。这种纤维束还可以实现细胞力的长距离传播,从而导致由细胞之间的机械通讯调节的相关迁移动力学。受这些实验发现的启发,我们开发了一种具有极化有效吸引力 (APPA) 的活性粒子模型,以研究由 ECM 介导的机械通信引起的紧急多细胞迁移动力学。特别是,APPA 模型通过在粒子之间施加成对极化吸引力来概括经典的活性布朗粒子 (ABP) 模型,该吸引力取决于粒子的瞬时动态状态并模拟细胞之间通过纤维束桥的有效相互牵引. 与经典的 ABP 系统相比,APPA 系统表现出增强的聚集行为,并且在较低的粒子密度和较高的旋转扩散率下对比更加明显。重要的是,与经典的 ABP 系统相比,在经典 ABP 系统中,所有粒子密度的粒子速度都不相关,APPA 系统的高密度相表现出很强的动态相关性,其特征在于缓慢衰减的速度相关函数,其相关长度与高密度相域(即粒子簇)的线性尺寸相当。APPA 模型预测的强相关多细胞动力学随后在使用 MCF-10A 细胞进行体外实验。我们的研究表明在迁移细胞之间结合 ECM 介导的机械耦合对于在复杂微环境中适当地模拟紧急多细胞动力学的重要性。