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Epithelial colonies in vitro elongate through collective effects

View ORCID ProfileJordi Comelles, SS Soumya, Linjie Lu, Emilie Le Maout, S. Anvitha, Guillaume Salbreux, Frank Jülicher, Mandar M. Inamdar, Daniel Riveline
doi: https://doi.org/10.1101/755181
Jordi Comelles
1Laboratory of Cell Physics ISIS/IGBMC, CNRS and University of Strasbourg, Strasbourg, France; Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France; Centre National de la Recherche Scientifique, UMR7104, Illkirch, France; Institut National de la Santé et de la Recherche Médicale, U964, Illkirch, France; Université de Strasbourg, Illkirch, France
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  • ORCID record for Jordi Comelles
SS Soumya
2Department of Civil Engineering, Indian Institute of Technology Bombay, Powai, Mumbai 400076, INDIA
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Linjie Lu
1Laboratory of Cell Physics ISIS/IGBMC, CNRS and University of Strasbourg, Strasbourg, France; Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France; Centre National de la Recherche Scientifique, UMR7104, Illkirch, France; Institut National de la Santé et de la Recherche Médicale, U964, Illkirch, France; Université de Strasbourg, Illkirch, France
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Emilie Le Maout
1Laboratory of Cell Physics ISIS/IGBMC, CNRS and University of Strasbourg, Strasbourg, France; Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France; Centre National de la Recherche Scientifique, UMR7104, Illkirch, France; Institut National de la Santé et de la Recherche Médicale, U964, Illkirch, France; Université de Strasbourg, Illkirch, France
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S. Anvitha
3Department of Mechanical Engineering, Indian Institute of Technology Bombay, Powai, Mumbai 400076, INDIA
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Guillaume Salbreux
4The Francis Crick Institute, 1 Midland Road, London NW1 1AT, United Kingdom
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Frank Jülicher
5Max Planck Institute for the Physics of Complex Systems, Nöthnitzer Str. 38, 01187 Dresden, Germany
6Cluster of Excellence Physics of Life, TU Dresden, Germany
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Mandar M. Inamdar
2Department of Civil Engineering, Indian Institute of Technology Bombay, Powai, Mumbai 400076, INDIA
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Daniel Riveline
1Laboratory of Cell Physics ISIS/IGBMC, CNRS and University of Strasbourg, Strasbourg, France; Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France; Centre National de la Recherche Scientifique, UMR7104, Illkirch, France; Institut National de la Santé et de la Recherche Médicale, U964, Illkirch, France; Université de Strasbourg, Illkirch, France
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  • For correspondence: riveline@unistra.fr
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Abstract

Epithelial tissues of the developing embryos elongate by different mechanisms, such as neighbor exchange, cell elongation, and oriented cell division. Since autonomous tissue self-organization is influenced by external cues such as morphogen gradients or neighboring tissues, it is difficult to distinguish intrinsic from directed tissue behavior. The mesoscopic processes leading to the different mechanisms remain elusive. Here, we study the spontaneous elongation behavior of spreading circular epithelial colonies in vitro. By quantifying deformation kinematics at multiple scales, we report that global elongation happens primarily due to cell elongations, and its direction correlates with the anisotropy of the average cell elongation. By imposing an external time-periodic stretch, the axis of this global symmetry breaking can be modified and elongation occurs primarily due to orientated neighbor exchange. These different behaviors are confirmed using a vertex model for collective cell behavior, providing a framework for understanding autonomous tissue elongation and its origins.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • In this version of the manuscript new experiments and an updated version of the in silicon model have been incorporated

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-ND 4.0 International license.
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Posted November 30, 2020.
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Epithelial colonies in vitro elongate through collective effects
Jordi Comelles, SS Soumya, Linjie Lu, Emilie Le Maout, S. Anvitha, Guillaume Salbreux, Frank Jülicher, Mandar M. Inamdar, Daniel Riveline
bioRxiv 755181; doi: https://doi.org/10.1101/755181
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Epithelial colonies in vitro elongate through collective effects
Jordi Comelles, SS Soumya, Linjie Lu, Emilie Le Maout, S. Anvitha, Guillaume Salbreux, Frank Jülicher, Mandar M. Inamdar, Daniel Riveline
bioRxiv 755181; doi: https://doi.org/10.1101/755181

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