Generation of stress fibers through myosin-driven re-organization of the actin cortex

Abstract

Contractile actomyosin bundles, stress fibers, govern key cellular processes including migration, adhesion, and mechanosensing. Stress fibers are thus critical for developmental morphogenesis. The most prominent actomyosin bundles, ventral stress fibers, generated through coalescence of pre-existing stress fiber precursors. However, whether stress fibers can assemble through other mechanisms has remained elusive. We report that stress fibers can also form without requirement of pre-existing actomyosin bundles. These structures, which we named cortical stress fibers, are embedded in the cell cortex and assemble preferentially underneath the nucleus. In this process, non-muscle myosin II pulses orchestrate the reorganization of cortical actin meshwork into regular bundles, which promote reinforcement of nascent focal adhesions, and subsequent stabilization of the cortical stress fibers. These results identify a new mechanism by which stress fibers can be generated de novo from the actin cortex, and establish role for stochastic myosin pulses in the assembly of functional actomyosin bundles.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files for pulse quantification are provided in GitHub (https://github.com/UH-LMU/lmu-users/tree/master/jaakko/NMIIA_pulses).

Article and author information

Author details

  1. Jaakko I Lehtimäki

    Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    For correspondence
    jaakko.lehtimaki@helsinki.fi
    Competing interests
    No competing interests declared.
  2. Eeva Kaisa Rajakylä

    Department of Veterinary Biosciences, University of Helsinki, Helsinki, Finland
    For correspondence
    kaisa.rajakyla@helsinki.fi
    Competing interests
    No competing interests declared.
  3. Sari Tojkander

    Department of Veterinary Biosciences, University of Helsinki, Helsinki, Finland
    For correspondence
    sari.tojkander@helsinki.fi
    Competing interests
    No competing interests declared.
  4. Pekka Lappalainen

    Program in Cell and Molecular Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    For correspondence
    pekka.lappalainen@helsinki.fi
    Competing interests
    Pekka Lappalainen, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6227-0354

Funding

Sigrid Juselius Foundation (4708344)

  • Pekka Lappalainen

Aatos Erkko Foundation (4704407)

  • Pekka Lappalainen

Academy of Finland (294174)

  • Sari Tojkander

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

Reviewing Editor

  1. Reinhard Fässler, Max Planck Institute of Biochemistry, Germany

Version history

  1. Received: July 3, 2020
  2. Accepted: January 27, 2021
  3. Accepted Manuscript published: January 28, 2021 (version 1)
  4. Accepted Manuscript updated: January 29, 2021 (version 2)
  5. Version of Record published: February 11, 2021 (version 3)
  6. Version of Record updated: April 20, 2022 (version 4)

Copyright

© 2021, Lehtimäki 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. Jaakko I Lehtimäki
  2. Eeva Kaisa Rajakylä
  3. Sari Tojkander
  4. Pekka Lappalainen
(2021)
Generation of stress fibers through myosin-driven re-organization of the actin cortex
eLife 10:e60710.
https://doi.org/10.7554/eLife.60710

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https://doi.org/10.7554/eLife.60710

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