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Geometry-Driven Polarity in Motile Amoeboid Cells

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Listed:
  • Oliver Nagel
  • Can Guven
  • Matthias Theves
  • Meghan Driscoll
  • Wolfgang Losert
  • Carsten Beta

Abstract

Motile eukaryotic cells, such as leukocytes, cancer cells, and amoeba, typically move inside the narrow interstitial spacings of tissue or soil. While most of our knowledge of actin-driven eukaryotic motility was obtained from cells that move on planar open surfaces, recent work has demonstrated that confinement can lead to strongly altered motile behavior. Here, we report experimental evidence that motile amoeboid cells undergo a spontaneous symmetry breaking in confined interstitial spaces. Inside narrow channels, the cells switch to a highly persistent, unidirectional mode of motion, moving at a constant speed along the channel. They remain in contact with the two opposing channel side walls and alternate protrusions of their leading edge near each wall. Their actin cytoskeleton exhibits a characteristic arrangement that is dominated by dense, stationary actin foci at the side walls, in conjunction with less dense dynamic regions at the leading edge. Our experimental findings can be explained based on an excitable network model that accounts for the confinement-induced symmetry breaking and correctly recovers the spatio-temporal pattern of protrusions at the leading edge. Since motile cells typically live in the narrow interstitial spacings of tissue or soil, we expect that the geometry-driven polarity we report here plays an important role for movement of cells in their natural environment.

Suggested Citation

  • Oliver Nagel & Can Guven & Matthias Theves & Meghan Driscoll & Wolfgang Losert & Carsten Beta, 2014. "Geometry-Driven Polarity in Motile Amoeboid Cells," PLOS ONE, Public Library of Science, vol. 9(12), pages 1-20, December.
  • Handle: RePEc:plo:pone00:0113382
    DOI: 10.1371/journal.pone.0113382
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    References listed on IDEAS

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    1. Tim Lämmermann & Bernhard L. Bader & Susan J. Monkley & Tim Worbs & Roland Wedlich-Söldner & Karin Hirsch & Markus Keller & Reinhold Förster & David R. Critchley & Reinhard Fässler & Michael Sixt, 2008. "Rapid leukocyte migration by integrin-independent flowing and squeezing," Nature, Nature, vol. 453(7191), pages 51-55, May.
    2. Kerry Wilson & Alexandre Lewalle & Marco Fritzsche & Richard Thorogate & Tom Duke & Guillaume Charras, 2013. "Mechanisms of leading edge protrusion in interstitial migration," Nature Communications, Nature, vol. 4(1), pages 1-12, December.
    3. Robert M Cooper & Ned S Wingreen & Edward C Cox, 2012. "An Excitable Cortex and Memory Model Successfully Predicts New Pseudopod Dynamics," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-12, March.
    4. Liang Li & Simon F Nørrelykke & Edward C Cox, 2008. "Persistent Cell Motion in the Absence of External Signals: A Search Strategy for Eukaryotic Cells," PLOS ONE, Public Library of Science, vol. 3(5), pages 1-11, May.
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