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Contractility-induced self-organization of smooth muscle cells: from multilayer cell sheets to dynamic three-dimensional clusters

View ORCID ProfileXiuyu Wang, David Gonzalez-Rodriguez, Thomas Vourc’h, Pascal Silberzan, Abdul I. Barakat
doi: https://doi.org/10.1101/2022.01.17.476602
Xiuyu Wang
1Hydrodynamics Laboratory – CNRS UMR 7646, Ecole Polytechnique, Institut Polytechnique de Paris, Palaiseau, France
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David Gonzalez-Rodriguez
2Université de Lorraine, LCP-A2MC, Metz, France
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Thomas Vourc’h
3Laboratoire PhysicoChimie Curie, Institut Curie, PSL Research University, Paris, France
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Pascal Silberzan
3Laboratoire PhysicoChimie Curie, Institut Curie, PSL Research University, Paris, France
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Abdul I. Barakat
1Hydrodynamics Laboratory – CNRS UMR 7646, Ecole Polytechnique, Institut Polytechnique de Paris, Palaiseau, France
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  • For correspondence: abdul.barakat@polytechnique.edu
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Abstract

Smooth muscle cells (SMCs) are mural cells that play a vital contractile function in many tissues. Abnormalities in SMC organization are associated with many diseases including atherosclerosis, asthma, and uterine fibroids. Various studies have reported that SMCs cultured on flat surfaces can spontaneously form three-dimensional clusters whose organization resembles that encountered in some of these pathological settings. Remarkably, how these structures form remains unknown. Here we combine in vitro experiments and physical modeling to show that three-dimensional clusters initiate when cellular contractile forces induce a hole in a flat SMC sheet, a process that can be modeled as the brittle fracture of a viscoelastic material. The subsequent evolution of the nascent cluster can be modeled as an active dewetting process with cluster shape evolution driven by a balance between cluster surface tension, arising from both cell contractility and adhesion, and cluster viscous dissipation. The description of the physical mechanisms governing the spontaneous emergence of these intriguing three-dimensional clusters offers insight into SMC-related disorders.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 20, 2022.
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Contractility-induced self-organization of smooth muscle cells: from multilayer cell sheets to dynamic three-dimensional clusters
Xiuyu Wang, David Gonzalez-Rodriguez, Thomas Vourc’h, Pascal Silberzan, Abdul I. Barakat
bioRxiv 2022.01.17.476602; doi: https://doi.org/10.1101/2022.01.17.476602
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Contractility-induced self-organization of smooth muscle cells: from multilayer cell sheets to dynamic three-dimensional clusters
Xiuyu Wang, David Gonzalez-Rodriguez, Thomas Vourc’h, Pascal Silberzan, Abdul I. Barakat
bioRxiv 2022.01.17.476602; doi: https://doi.org/10.1101/2022.01.17.476602

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