Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamics

  1. Kai Weißenbruch  Is a corresponding author
  2. Justin Grewe
  3. Marc Hippler
  4. Magdalena Fladung
  5. Moritz Tremmel
  6. Kathrin Stricker
  7. Ulrich Sebastian Schwarz  Is a corresponding author
  8. Martin Bastmeyer  Is a corresponding author
  1. Karlsruhe Institute of Technology, Germany
  2. University of Heidelberg, Germany
  3. Karlsruhe Institute of, Germany
  4. Heidelberg University, Germany

Abstract

Nonmuscle myosin II (NM II) is an integral part of essential cellular processes, including adhesion and migration. Mammalian cells express up to three isoforms termed NM IIA, B, and C. We used U2OS cells to create CRISPR/Cas9-based knockouts of all three isoforms and analyzed the phenotypes on homogenously-coated surfaces, in collagen gels, and on micropatterned substrates. In contrast to homogenously-coated surfaces, a structured environment supports a cellular phenotype with invaginated actin arcs even in the absence of NM IIA-induced contractility. A quantitative shape analysis of cells on micropatterns combined with a scale-bridging mathematical model reveals that NM IIA is essential to build up cellular tension during initial stages of force generation, while NM IIB is necessary to elastically stabilize NM IIA-generated tension. A dynamic cell stretch/release experiment in a three-dimensional scaffold confirms these conclusions and in addition reveals a novel role for NM IIC, namely the ability to establish tensional homeostasis.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source files with the raw data are provided for all Figures, where quantifications are carried out.

Article and author information

Author details

  1. Kai Weißenbruch

    Zoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany
    For correspondence
    kai.weissenbruch@kit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9463-6725
  2. Justin Grewe

    University of Heidelberg, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Marc Hippler

    Karlsruhe Institute of, Karlsruhe, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Magdalena Fladung

    Zoological Institute - Cell and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4213-2891
  5. Moritz Tremmel

    Zoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8901-9362
  6. Kathrin Stricker

    Zoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Ulrich Sebastian Schwarz

    Institute for Theoretical Physics, Heidelberg University, Heidelberg, Germany
    For correspondence
    schwarz@thphys.uni-heidelberg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1483-640X
  8. Martin Bastmeyer

    Zoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, Germany
    For correspondence
    bastmeyer@kit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3471-8400

Funding

Deutsche Forschungsgemeinschaft (EXC 2082/1-390761711)

  • Ulrich Sebastian Schwarz
  • Martin Bastmeyer

Deutsche Forschungsgemeinschaft (EXC 2181/1 - 390900948)

  • Ulrich Sebastian Schwarz

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

Reviewing Editor

  1. Pekka Lappalainen, University of Helsinki, Finland

Publication history

  1. Preprint posted: October 9, 2020 (view preprint)
  2. Received: July 2, 2021
  3. Accepted: August 9, 2021
  4. Accepted Manuscript published: August 10, 2021 (version 1)
  5. Version of Record published: August 26, 2021 (version 2)

Copyright

© 2021, Weißenbruch 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. Kai Weißenbruch
  2. Justin Grewe
  3. Marc Hippler
  4. Magdalena Fladung
  5. Moritz Tremmel
  6. Kathrin Stricker
  7. Ulrich Sebastian Schwarz
  8. Martin Bastmeyer
(2021)
Distinct roles of nonmuscle myosin II isoforms for establishing tension and elasticity during cell morphodynamics
eLife 10:e71888.
https://doi.org/10.7554/eLife.71888

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