Nonlinear dynamics of cell migration in anisotropic microenvironment

doi:10.1088/1674-1056/ac11d5

中国物理B ›› 2021, Vol. 30 ›› Issue (9): 90505-090505.doi: 10.1088/1674-1056/ac11d5

Nonlinear dynamics of cell migration in anisotropic microenvironment

Yanping Liu(刘艳平)^1,†, Da He(何达)^2,†, Yang Jiao(焦阳)^3,4, Guoqiang Li(李国强)¹, Yu Zheng(郑钰)³, Qihui Fan(樊琪慧)⁵, Gao Wang(王高)¹, Jingru Yao(姚静如)¹, Guo Chen(陈果)¹, Silong Lou(娄四龙)⁶, and Liyu Liu(刘雳宇)^1,‡

1 Chongqing Key Laboratory of Soft Condensed Matter Physics and Smart Materials, College of Physics, Chongqing University, Chongqing 401331, China;
2 Spine Surgery, Beijing Jishuitan Hospital, Beijing 100035, China;
3 Department of Physics, Arizona State University, Tempe, Arizona 85287, USA;
4 Materials Science and Engineering, Arizona State University, Tempe, Arizona 85287, USA;
5 Beijing National Laboratory for Condensed Matter Physics and CAS Key Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences(CAS), Beijing 100190, China;
6 Department of Neurosurgery, Chongqing University Cancer Hospital, Chongqing 400030, China

收稿日期:2021-06-01 修回日期:2021-06-27 接受日期:2021-07-07 出版日期:2021-08-19 发布日期:2021-09-02
通讯作者: Yanping Liu E-mail:lyliu@cqu.edu.cn
基金资助:
Project supported by the National Natural Science Foundation of China (Grant Nos. 11974066, 11674043, 11675134, and 11874310), the Natural Science Foundation of Chongqing, China (Grant Nos. cstc2019jcyj-msxmX0477 and cstc2018jcyjA3679), and the Capital Health Development Research Project, China (Grant No. 2020-2-2072).

Nonlinear dynamics of cell migration in anisotropic microenvironment

1 Chongqing Key Laboratory of Soft Condensed Matter Physics and Smart Materials, College of Physics, Chongqing University, Chongqing 401331, China;
2 Spine Surgery, Beijing Jishuitan Hospital, Beijing 100035, China;
3 Department of Physics, Arizona State University, Tempe, Arizona 85287, USA;
4 Materials Science and Engineering, Arizona State University, Tempe, Arizona 85287, USA;
5 Beijing National Laboratory for Condensed Matter Physics and CAS Key Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences(CAS), Beijing 100190, China;
6 Department of Neurosurgery, Chongqing University Cancer Hospital, Chongqing 400030, China

Received:2021-06-01 Revised:2021-06-27 Accepted:2021-07-07 Online:2021-08-19 Published:2021-09-02
Contact: Yanping Liu E-mail:lyliu@cqu.edu.cn
Supported by:
Project supported by the National Natural Science Foundation of China (Grant Nos. 11974066, 11674043, 11675134, and 11874310), the Natural Science Foundation of Chongqing, China (Grant Nos. cstc2019jcyj-msxmX0477 and cstc2018jcyjA3679), and the Capital Health Development Research Project, China (Grant No. 2020-2-2072).

摘要/Abstract

摘要： Cell migration in anisotropic microenvironment plays an important role in the development of normal tissues and organs as well as neoplasm progression, e.g., osteogenic differentiation of embryonic stem cells was facilitated on stiffer substrates, indicating that the mechanical signals greatly affect both early and terminal differentiation of embryonic stem cells. However, the effect of anisotropy on cell migration dynamics, in particular, in terms of acceleration profiles which is important for recognizing dynamics modes of cell migration and analyzing the regulation mechanisms of microenvironment in mechanical signal transmission, has not been systematically investigated. In this work, we firstly rigorously investigate and quantify the differences between persistent random walk and anisotropic persistent random walk models based on the analysis of cell migration trajectories and velocity auto-covariance function, both qualitatively and quantitatively. Secondly, we introduce the concepts of positive and negative anisotropy based on the motility parameters to study the effect of anisotropy on acceleration profiles, especially the nonlinear decrease and non-monotonic behaviors. We particularly elaborate and discuss the mechanisms, and physical insights of non-monotonic behaviors in the case of positive anisotropy, focusing on the force exerted on migrating cells. Finally, we analyze two types of in vitro cell migration experiments and verify the universality of nonlinear decrease and the consistence of non-monotonic behaviors with numerical results. We conclude that the anisotropy of microenvironment is the cause of the non-monotonic and nonlinear dynamics, and the anisotropic persistent random walk can be as a suitable tool to analyze in vitro cell migration with different combinations of motility parameters. Our analysis provides new insights into the dynamics of cell migration in complex microenvironment, which also has implications in tissue engineering and cancer research.

关键词: cell migration, nonlinear behavior, motility parameter, acceleration profile, anisotropic microenvironment

Abstract: Cell migration in anisotropic microenvironment plays an important role in the development of normal tissues and organs as well as neoplasm progression, e.g., osteogenic differentiation of embryonic stem cells was facilitated on stiffer substrates, indicating that the mechanical signals greatly affect both early and terminal differentiation of embryonic stem cells. However, the effect of anisotropy on cell migration dynamics, in particular, in terms of acceleration profiles which is important for recognizing dynamics modes of cell migration and analyzing the regulation mechanisms of microenvironment in mechanical signal transmission, has not been systematically investigated. In this work, we firstly rigorously investigate and quantify the differences between persistent random walk and anisotropic persistent random walk models based on the analysis of cell migration trajectories and velocity auto-covariance function, both qualitatively and quantitatively. Secondly, we introduce the concepts of positive and negative anisotropy based on the motility parameters to study the effect of anisotropy on acceleration profiles, especially the nonlinear decrease and non-monotonic behaviors. We particularly elaborate and discuss the mechanisms, and physical insights of non-monotonic behaviors in the case of positive anisotropy, focusing on the force exerted on migrating cells. Finally, we analyze two types of in vitro cell migration experiments and verify the universality of nonlinear decrease and the consistence of non-monotonic behaviors with numerical results. We conclude that the anisotropy of microenvironment is the cause of the non-monotonic and nonlinear dynamics, and the anisotropic persistent random walk can be as a suitable tool to analyze in vitro cell migration with different combinations of motility parameters. Our analysis provides new insights into the dynamics of cell migration in complex microenvironment, which also has implications in tissue engineering and cancer research.

Key words: cell migration, nonlinear behavior, motility parameter, acceleration profile, anisotropic microenvironment

中图分类号: (Stochastic analysis methods)

05.10.Gg

05.40.-a (Fluctuation phenomena, random processes, noise, and Brownian motion) 05.40.Fb (Random walks and Levy flights)

Yanping Liu(刘艳平), Da He(何达), Yang Jiao(焦阳), Guoqiang Li(李国强), Yu Zheng(郑钰), Qihui Fan(樊琪慧), Gao Wang(王高), Jingru Yao(姚静如), Guo Chen(陈果), Silong Lou(娄四龙), and Liyu Liu(刘雳宇). Nonlinear dynamics of cell migration in anisotropic microenvironment[J]. 中国物理B, 2021, 30(9): 90505-090505.

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Nonlinear dynamics of cell migration in anisotropic microenvironment

Nonlinear dynamics of cell migration in anisotropic microenvironment

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