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Traction forces control cell-edge dynamics and mediate distance-sensitivity during cell polarization

Zeno Messi, Alicia Bornert, Franck Raynaud, Alexander Verkhovsky
doi: https://doi.org/10.1101/745687
Zeno Messi
Lab. of Physics of Living Matter, EPFL, Lausanne, Switzerland
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  • For correspondence: zeno.messi@epfl.ch sasha.verkhovsky@epfl.ch
Alicia Bornert
Lab. of Physics of Living Matter, EPFL, Lausanne, SwitzerlandUMR S1255, Etablissement Français du Sang, Strasbourg, France
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Franck Raynaud
Computer Science Department, University of Geneva, Switzerland
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Alexander Verkhovsky
Lab. of Physics of Living Matter, EPFL, Lausanne, Switzerland
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  • For correspondence: zeno.messi@epfl.ch sasha.verkhovsky@epfl.ch
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SUMMARY

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 [1–3]. 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 [4–10]. 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 [11–15]. 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 [16] 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 spontaneous polarization. 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.

Footnotes

  • https://github.com/zenomessi/lattice.git

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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 August 23, 2019.
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Traction forces control cell-edge dynamics and mediate distance-sensitivity during cell polarization
Zeno Messi, Alicia Bornert, Franck Raynaud, Alexander Verkhovsky
bioRxiv 745687; doi: https://doi.org/10.1101/745687
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Traction forces control cell-edge dynamics and mediate distance-sensitivity during cell polarization
Zeno Messi, Alicia Bornert, Franck Raynaud, Alexander Verkhovsky
bioRxiv 745687; doi: https://doi.org/10.1101/745687

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