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Traction Forces Control Cell-Edge Dynamics and Mediate Distance-Sensitivity During Cell Polarization

22 Pages Posted: 23 Aug 2019 Sneak Peek Status: Review Complete

See all articles by Zeno Messi

Zeno Messi

Ecole Polytechnique Fédérale de Lausanne - Lab of Physics of Living Matter

Alicia Bornert

Etablissement Français du Sang

Franck Raynaud

University of Geneva - Department of Computer Science

Alexander B. Verkhovsky

Ecole Polytechnique Fédérale de Lausanne - Lab of Physics of Living Matter

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Abstract

Traction forces are generated by cellular actin-myosin system and transmitted to the environment through adhesions. They are believed to drive cell motion, shape changes, and extracellular matrix remodeling. However, most of the traction force analysis has been performed on stationary cells, investigating forces at the level of individual focal adhesions or linking them to static cell parameters such as area and edge curvature. It is not well understood how traction forces are related to shape changes and motion, e.g. forces were reported to either increase or drop prior to cell retraction. Here, we analyze the dynamics of traction forces during the protrusion-retraction cycle of polarizing fish epidermal keratocytes and find that forces fluctuate in concert with the cycle, increasing during the protrusion phase and reaching maximum at the beginning of retraction. We relate force dynamics to the recently discovered phenomenological rule that governs cell edge behavior during keratocyte polarization: both traction forces and the probability of switch from protrusion to retraction increase with the distance from the cell center. Diminishing traction forces with cell contractility inhibitor leads to decreased edge fluctuations and abnormal polarization, while externally applied force can induce protrusion-retraction switch. These results suggest that forces mediate distance-sensitivity of the edge dynamics and ultimately organize cell-edge behavior leading to spontaneouspolarization. Actin flow rate did not exhibit the same distance-dependence as traction stress, arguing against its role in organizing edge dynamics. Finally, using a simple model of actin-myosin network, we show that force-distance relationship may be an emergent feature of such networks.

Keywords: Cell motility, Cell polarization, Traction forces, Actin flow

Suggested Citation

Messi, Zeno and Bornert, Alicia and Raynaud, Franck and Verkhovsky, Alexander B., Traction Forces Control Cell-Edge Dynamics and Mediate Distance-Sensitivity During Cell Polarization (August 22, 2019). CURRENT-BIOLOGY-D-19-01384. Available at SSRN: https://ssrn.com/abstract=3441418 or http://dx.doi.org/10.2139/ssrn.3441418
This is a paper under consideration at Cell Press and has not been peer-reviewed.

Zeno Messi (Contact Author)

Ecole Polytechnique Fédérale de Lausanne - Lab of Physics of Living Matter ( email )

Lausanne
Switzerland

Alicia Bornert

Etablissement Français du Sang

Créteil
France

Franck Raynaud

University of Geneva - Department of Computer Science

1211 Geneva 4 – Suisse
Geneva
Switzerland

Alexander B. Verkhovsky

Ecole Polytechnique Fédérale de Lausanne - Lab of Physics of Living Matter ( email )

Lausanne
Switzerland

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