Polarity mechanisms such as contact inhibition of locomotion regulate persistent rotational motion of mammalian cells on micropatterns

Significance During the growth of an embryo or the spreading of a tumor, cells may travel collectively. We study a computational model of a simple example of collective migration: two cells confined to a square adhesive pattern. In this confinement, some cell types rotate, whereas others do not. We...

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Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2014-10, Vol.111 (41), p.14770-14775
Hauptverfasser: Camley, Brian A., Zhang, Yunsong, Zhao, Yanxiang, Li, Bo, Ben-Jacob, Eshel, Levine, Herbert, Rappel, Wouter-Jan
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container_end_page 14775
container_issue 41
container_start_page 14770
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 111
creator Camley, Brian A.
Zhang, Yunsong
Zhao, Yanxiang
Li, Bo
Ben-Jacob, Eshel
Levine, Herbert
Rappel, Wouter-Jan
description Significance During the growth of an embryo or the spreading of a tumor, cells may travel collectively. We study a computational model of a simple example of collective migration: two cells confined to a square adhesive pattern. In this confinement, some cell types rotate, whereas others do not. We model these crawling cells, the forces between them, and several possible ways that the cells could choose what direction they will crawl—their “polarity mechanism.” We show that the cell polarity mechanism can control whether the pairs of cells rotate or remain fixed. This suggests that we can learn about how large groups of cells choose their direction by studying the rotation of pairs. Pairs of endothelial cells on adhesive micropatterns rotate persistently, but pairs of fibroblasts do not; coherent rotation is present in normal mammary acini and kidney cells but absent in cancerous cells. Why? To answer this question, we develop a computational model of pairs of mammalian cells on adhesive micropatterns using a phase field method and study the conditions under which persistent rotational motion (PRM) emerges. Our model couples the shape of the cell, the cell’s internal chemical polarity, and interactions between cells such as volume exclusion and adhesion. We show that PRM can emerge from this minimal model and that the cell-cell interface may be influenced by the nucleus. We study the effect of various cell polarity mechanisms on rotational motion, including contact inhibition of locomotion, neighbor alignment, and velocity alignment, where cells align their polarity to their velocity. These polarity mechanisms strongly regulate PRM: Small differences in polarity mechanisms can create significant differences in collective rotation. We argue that the existence or absence of rotation under confinement may lead to insight into the cell’s methods for coordinating collective cell motility.
doi_str_mv 10.1073/pnas.1414498111
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subjects Animal migration behavior
Animals
Biological Sciences
Cell adhesion
Cell adhesion & migration
Cell Count
Cell membranes
Cell motility
Cell Movement
Cell Polarity
Cells
Cellular biology
Contact Inhibition
Endothelial cells
Endothelium
Epithelial cells
Kinetics
Locomotion
Mammals
Mammals - metabolism
Mathematical models
Models, Biological
Motility
Physical Sciences
Rotation
title Polarity mechanisms such as contact inhibition of locomotion regulate persistent rotational motion of mammalian cells on micropatterns
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