Cell clusters adopt a collective amoeboid mode of migration in confined nonadhesive environments

Author:

Pagès Diane-Laure12ORCID,Dornier Emmanuel1ORCID,de Seze Jean3,Gontran Emilie1ORCID,Maitra Ananyo4ORCID,Maciejewski Aurore12,Wang Li5ORCID,Luan Rui1,Cartry Jérôme1ORCID,Canet-Jourdan Charlotte12,Raingeaud Joël1,Lemahieu Grégoire1,Lebel Marceline1ORCID,Ducreux Michel16,Gelli Maximiliano17,Scoazec Jean-Yves89ORCID,Coppey Mathieu3ORCID,Voituriez Raphaël410,Piel Matthieu5ORCID,Jaulin Fanny1ORCID

Affiliation:

1. Inserm U-1279, Gustave Roussy, Villejuif F-94805, France.

2. Université Paris-Saclay, Inserm, Institut Gustave Roussy, Dynamique des Cellules Tumorales, Villejuif 94800, France.

3. Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, Sorbonne Université, CNRS, Paris 75005, France.

4. Laboratoire Jean Perrin, UMR 8237 CNRS/Sorbonne Université, Paris 75255, France.

5. Institut Curie and Institut Pierre Gilles de Gennes, PSL Research University, CNRS, UMR 144, Paris 75005, France.

6. Département de Médecine Oncologique, Gustave Roussy, Université Paris-Saclay, Villejuif F-94805, France.

7. Département de Chirurgie Viscérale, Gustave Roussy, Villejuif F-94805, France.

8. Service de Pathologie, Département de Biologie et Pathologie Médicale, Gustave Roussy, Villejuif F-94805, France.

9. Faculté de Médecine, Université Paris Saclay, Le Kremlin-Bicêtre F-94270, France.

10. Laboratoire de Physique Théorique de la Matière Condensée, UMR 7600 CNRS/Sorbonne Université, Paris 75255, France.

Abstract

Cell migration is essential to living organisms and deregulated in cancer. Single cell’s migration ranges from traction-dependent mesenchymal motility to contractility-driven propulsive amoeboid locomotion, but collective cell migration has only been described as a focal adhesion–dependent and traction-dependent process. Here, we show that cancer cell clusters, from patients and cell lines, migrate without focal adhesions when confined into nonadhesive microfabricated channels. Clusters coordinate and behave like giant super cells, mobilizing their actomyosin contractility at the rear to power their migration. This polarized cortex does not sustain persistent retrograde flows, of cells or actin, like in the other modes of migration but rather harnesses fluctuating cell deformations, or jiggling. Theoretical physical modeling shows this is sufficient to create a gradient of friction forces and trigger directed cluster motion. This collective amoeboid mode of migration could foster metastatic spread by enabling cells to cross a wide spectrum of environments.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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