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Spontaneous migration of cellular aggregates from giant keratocytes to running spheroids

Beaune, Grégory and Blanch-Mercader, Carles and Douezan, Stéphane and Dumond, Julien and Gonzalez-Rodriguez, David and Cuvelier, Damien and Ondarçuhu, Thierry and Sens, Pierre and Dufour, Sylvie and Murrell, Michael P. and Brochard-Wyart, Françoise Spontaneous migration of cellular aggregates from giant keratocytes to running spheroids. (2018) Proceedings of the National Academy of Sciences, 115 (51). 12926-12931. ISSN 0027-8424

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Official URL: https://doi.org/10.1073/pnas.1811348115

Abstract

Despite extensive knowledge on the mechanisms that drive singlecell migration, those governing the migration of cell clusters, as occurring during embryonic development and cancer metastasis,remain poorly understood. Here, we investigate the collective migration of cell on adhesive gels with variable rigidity, using 3D cellular aggregates as a model system. After initial adhesion to the substrate, aggregates spread by expanding outward a cell monolayer, whose dynamics is optimal in a narrowrange of rigidities. Fast expansion gives rise to the accumulation of mechanical tension that leads to the rupture of cell–cell contacts and the nucleation of holes within the monolayer, which becomes unstable and undergoes dewetting like a liquid film. This leads to a symmetry breaking and causes the entire aggregate to move as a single entity. Varying the substrate rigidity modulates the extent of dewetting and induces different modes of aggregate motion: “giant keratocytes,” where the lamellipodium is a cell monolayer that expands at the front and retracts at the back; “penguins,” characterized by bipedal locomotion; and “running spheroids,” for nonspreading aggregates. We characterize these diverse modes of collectivemigration by quantifying the flows and forces that drive them, andwe unveil the fundamental physical principles that govern these behaviors, which underscore the biological predisposition of living material to migrate, independent of length scale.

Item Type:Article
HAL Id:hal-02324990
Audience (journal):International peer-reviewed journal
Uncontrolled Keywords:
Institution:French research institutions > Centre National de la Recherche Scientifique - CNRS (FRANCE)
Université de Toulouse > Institut National Polytechnique de Toulouse - Toulouse INP (FRANCE)
French research institutions > Institut National de la Santé et de la Recherche Médicale - INSERM (FRANCE)
Other partners > Sorbonne Université (FRANCE)
Other partners > Université Paris Est Créteil Val de Marne - UPEC (FRANCE)
Other partners > Université Pierre et Marie Curie, Paris 6 - UPMC (FRANCE)
Université de Toulouse > Université Toulouse III - Paul Sabatier - UT3 (FRANCE)
Other partners > Université de Genève (SWITZERLAND)
Other partners > PSL Research University (FRANCE)
Other partners > Université de Lorraine (FRANCE)
Other partners > Yale University (USA)
Laboratory name:
Funders:
Multidisciplinary University Research Initiative - MURI (USA) - Agence Nationale de Recherche - ANR (FRANCE)
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Deposited On:26 Feb 2019 13:32

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