1. Physics of Living Systems
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Polar pattern formation induced by contact following locomotion in a multicellular system

  1. Masayuki Hayakawa
  2. Tetsuya Hiraiwa
  3. Yuko Wada
  4. Hidekazu Kuwayama
  5. Tatsuo Shibata  Is a corresponding author
  1. RIKEN Center for Biosystems Dynamics Research, Japan
  2. National University of Singapore, Singapore
  3. University of Tsukuba, Japan
Research Article
  • Cited 6
  • Views 1,672
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Cite this article as: eLife 2020;9:e53609 doi: 10.7554/eLife.53609

Abstract

Biophysical mechanisms underlying collective cell migration of eukaryotic cells have been studied extensively in recent years. One mechanism that induces cells to correlate their motions is contact inhibition of locomotion, by which cells migrating away from the contact site. Here, we report that tail-following behavior at the contact site, termed contact following locomotion (CFL), can induce a non-trivial collective behavior in migrating cells. We show the emergence of a traveling band showing polar order in a mutant Dictyostelium cell that lacks chemotactic activity. We find that CFL is the cell–cell interaction underlying this phenomenon, enabling a theoretical description of how this traveling band forms. We further show that the polar order phase consists of subpopulations that exhibit characteristic transversal motions with respect to the direction of band propagation. These findings describe a novel mechanism of collective cell migration involving cell–cell interactions capable of inducing traveling band with polar order.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figure 1, 2, 3 and 4.

Article and author information

Author details

  1. Masayuki Hayakawa

    Laboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Tetsuya Hiraiwa

    Mechanobiology Institute, National University of Singapore, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  3. Yuko Wada

    Laboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Hidekazu Kuwayama

    Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Tatsuo Shibata

    Laboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
    For correspondence
    tatsuo.shibata@riken.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9294-9998

Funding

Japan Society for the Promotion of Science (JP17J05667)

  • Masayuki Hayakawa

Japan Society for the Promotion of Science (JP16K17777)

  • Tetsuya Hiraiwa

Japan Society for the Promotion of Science (JP19K03764)

  • Tetsuya Hiraiwa

Japan Society for the Promotion of Science (JP26610129)

  • Hidekazu Kuwayama

Japan Society for the Promotion of Science (JP19H00996)

  • Tatsuo Shibata

Japan Science and Technology Agency (JPMJCR1852)

  • Tatsuo Shibata

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Tâm Mignot, CNRS-Aix Marseille University, France

Publication history

  1. Received: November 14, 2019
  2. Accepted: April 15, 2020
  3. Accepted Manuscript published: April 30, 2020 (version 1)
  4. Version of Record published: May 11, 2020 (version 2)
  5. Version of Record updated: May 14, 2020 (version 3)

Copyright

© 2020, Hayakawa et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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Further reading

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    2. Physics of Living Systems
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    A monolayer of highly motile cells can establish long-range orientational order, which can be explained by hydrodynamic theory of active gels and fluids. However, it is less clear how cell shape changes and rearrangement are governed when the monolayer is in mechanical equilibrium states when cell motility diminishes. In this work, we report that rat embryonic fibroblasts (REF), when confined in circular mesoscale patterns on rigid substrates, can transition from the spindle shapes to more compact morphologies. Cells align radially only at the pattern boundary when they are in the mechanical equilibrium. This radial alignment disappears when cell contractility or cell-cell adhesion is reduced. Unlike monolayers of spindle-like cells such as NIH-3T3 fibroblasts with minimal intercellular interactions or epithelial cells like Madin-Darby canine kidney (MDCK) with strong cortical actin network, confined REF monolayers present an actin gradient with isotropic meshwork, suggesting the existence of a stiffness gradient. In addition, the REF cells tend to condense on soft substrates, a collective cell behavior we refer to as the 'condensation tendency'. This condensation tendency, together with geometrical confinement, induces tensile prestretch (i.e., an isotropic stretch that causes tissue to contract when released) to the confined monolayer. By developing a Voronoi-cell model, we demonstrate that the combined global tissue prestretch and cell stiffness differential between the inner and boundary cells can sufficiently define the cell radial alignment at the pattern boundary.