Modeling multicellular dynamics regulated by extracellular-matrix-mediated mechanical communication via active particles with polarized effective attraction

Yu Zheng, Qihui Fan, Christopher Z. Eddy, Xiaochen Wang, Bo Sun, Fangfu Ye, and Yang Jiao
Phys. Rev. E 102, 052409 – Published 20 November 2020
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Abstract

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.

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  • Received 3 April 2020
  • Revised 23 June 2020
  • Accepted 2 November 2020

DOI:https://doi.org/10.1103/PhysRevE.102.052409

©2020 American Physical Society

Physics Subject Headings (PhySH)

Statistical Physics & ThermodynamicsPhysics of Living Systems

Authors & Affiliations

Yu Zheng1,*, Qihui Fan2,3,*, Christopher Z. Eddy4, Xiaochen Wang2,3, Bo Sun4,†, Fangfu Ye2,3,5,‡, and Yang Jiao6,1,§

  • 1Department of Physics, Arizona State University, Tempe, Arizona 85287, USA
  • 2Beijing National Laboratory for Condensed Matte Physics and CAS Key Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing 100190, China
  • 3School of Physical Sciences, University of Chinese Academy of Sciences, Beijing 100049, China
  • 4Department of Physics, Oregon State University, Corvallis, Oregon 97331, USA
  • 5Wenzhou Institute, University of Chinese Academy of Sciences, Wenzhou, Zhejiang 325001, China
  • 6Materials Science and Engineering, Arizona State University, Tempe, Arizona 85287, USA

  • *These authors contributed equally to this work.
  • sunb@physics.oregonstate.edu
  • fye@iphy.ac.cn
  • §yang.jiao.2@asu.edu

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Issue

Vol. 102, Iss. 5 — November 2020

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