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

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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  1. Masayuki Hayakawa
  2. Tetsuya Hiraiwa
  3. Yuko Wada
  4. Hidekazu Kuwayama
  5. Tatsuo Shibata
(2020)
Polar pattern formation induced by contact following locomotion in a multicellular system
eLife 9:e53609.
https://doi.org/10.7554/eLife.53609

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