Persistent cell migration emerges from a coupling between protrusion dynamics and polarized trafficking

  1. Kotryna Vaidžiulytė
  2. Anne-Sophie Macé
  3. Aude Battistella
  4. William Beng
  5. Kristine Schauer  Is a corresponding author
  6. Mathieu Coppey  Is a corresponding author
  1. Institut Curie, France
  2. Institut Gustave Roussy, France

Abstract

Migrating cells present a variety of paths, from random to highly directional ones. While random movement can be explained by basal intrinsic activity, persistent movement requires stable polarization. Here, we quantitatively address emergence of persistent migration in RPE1 cells over long timescales. By live-cell imaging and dynamic micropatterning, we demonstrate that the Nucleus-Golgi axis aligns with direction of migration leading to efficient cell movement. We show that polarized trafficking is directed towards protrusions with a 20 min delay, and that migration becomes random after disrupting internal cell organization. Eventually, we prove that localized optogenetic Cdc42 activation orients the Nucleus-Golgi axis. Our work suggests that polarized trafficking stabilizes the protrusive activity of the cell, while protrusive activity orients this polarity axis, leading to persistent cell migration. Using a minimal physical model, we show that this feedback is sufficient to recapitulate the quantitative properties of cell migration in the timescale of hours.

Data availability

Source data files with numerical data and Source Code for all the graphs in the figures are provided as a zip supplementary file attached to each figure in this submission. Raw imaging data for all the figures are available in the BioImage Archive repository at https://www.ebi.ac.uk/biostudies/studies/S-BIAD365 with BioStudies accession number S-BIAD365.

The following data sets were generated

Article and author information

Author details

  1. Kotryna Vaidžiulytė

    UMR144 / UMR168, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2114-3612
  2. Anne-Sophie Macé

    CNRS / UMR144, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Aude Battistella

    UMR144 / UMR168, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. William Beng

    UMR144 / UMR168, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Kristine Schauer

    Tumor Cell Dynamics Unit, Institut Gustave Roussy, Villejuif, France
    For correspondence
    kristine.schauer@gustaveroussy.fr
    Competing interests
    The authors declare that no competing interests exist.
  6. Mathieu Coppey

    CNRS / UMR168, Institut Curie, Paris, France
    For correspondence
    mathieu.coppey@curie.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8924-3233

Funding

Programme doctoral Interface pour le Vivant

  • Kotryna Vaidžiulytė

Fondation pour la Recherche Médicale (FDT201904008167)

  • Kotryna Vaidžiulytė

Labex CelTisPhyBio (ANR-10-LBX-0038)

  • Kristine Schauer
  • Mathieu Coppey

Labex and Equipex IPGG (ANR-10-NANO0207)

  • Mathieu Coppey

Idex Paris Science et Lettres (ANR-10-IDEX-0001-02 PSL)

  • Kristine Schauer
  • Mathieu Coppey

Centre National de la Recherche Scientifique

  • Kristine Schauer
  • Mathieu Coppey

Institut Curie

  • Kristine Schauer
  • Mathieu Coppey

French National Research Infrastructure France-BioImaging (ANR-10-INBS-04)

  • Anne-Sophie Macé
  • Mathieu Coppey

Institut Convergences Q-life (ANR-17-CONV-0005)

  • Mathieu Coppey

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

Reviewing Editor

  1. Frederic A Bard, Institute of Molecular and Cell Biology, Singapore

Publication history

  1. Preprint posted: March 22, 2021 (view preprint)
  2. Received: April 11, 2021
  3. Accepted: February 26, 2022
  4. Accepted Manuscript published: March 18, 2022 (version 1)
  5. Version of Record published: March 29, 2022 (version 2)

Copyright

© 2022, Vaidžiulytė 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. Kotryna Vaidžiulytė
  2. Anne-Sophie Macé
  3. Aude Battistella
  4. William Beng
  5. Kristine Schauer
  6. Mathieu Coppey
(2022)
Persistent cell migration emerges from a coupling between protrusion dynamics and polarized trafficking
eLife 11:e69229.
https://doi.org/10.7554/eLife.69229
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