Global and local tension measurements in biomimetic skeletal muscle tissues reveals early mechanical homeostasis

  1. Arne D Hofemeier
  2. Tamara Limón
  3. Till Moritz Muenker
  4. Bernhard Wallmeyer
  5. Alejandro Jurado
  6. Mohammad Ebrahim Afshar
  7. Majid Ebrahimi
  8. Roman Tsukanov
  9. Nazar Oleksiievets
  10. Jörg Enderlein
  11. Penney M Gilbert
  12. Timo Betz  Is a corresponding author
  1. University of Münster, Germany
  2. University of Toronto, Canada
  3. Georg August University, Germany
  4. Universtity of Göttingen, Germany

Abstract

Tension and mechanical properties of muscle tissue are tightly related to proper skeletal muscle function, which makes experimental access to the biomechanics of muscle tissue formation a key requirement to advance our understanding of muscle function and development. Recently developed elastic in vitro culture chambers allow for raising 3D muscle tissue under controlled conditions and to measure global tissue force generation. However, these chambers are inherently incompatible with high resolution microscopy limiting their usability to global force measurements, and preventing the exploitation of modern fluorescence based investigation methods for live and dynamic measurements. Here we present a new chamber design pairing global force measurements, quantified from post deflection, with local tension measurements obtained from elastic hydrogel beads embedded in muscle tissue. High resolution 3D video microscopy of engineered muscle formation, enabled by the new chamber, shows an early mechanical tissue homeostasis that remains stable in spite of continued myotube maturation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Programs are published on GitHub.

Article and author information

Author details

  1. Arne D Hofemeier

    Institute for Cell Biology, Center for Molecular Biology of Inflammation, University of Münster, Münster, Germany
    Competing interests
    Arne D Hofemeier, Patent application filed for the chamber. Application number: LU101799.
  2. Tamara Limón

    Institute for Cell Biology, Center for Molecular Biology of Inflammation, University of Münster, Münster, Germany
    Competing interests
    No competing interests declared.
  3. Till Moritz Muenker

    Institute for Cell Biology, Center for Molecular Biology of Inflammation, University of Münster, Münster, Germany
    Competing interests
    No competing interests declared.
  4. Bernhard Wallmeyer

    Institute for Cell Biology, Center for Molecular Biology of Inflammation, University of Münster, Münster, Germany
    Competing interests
    No competing interests declared.
  5. Alejandro Jurado

    Institute for Cell Biology, Center for Molecular Biology of Inflammation, University of Münster, Münster, Germany
    Competing interests
    No competing interests declared.
  6. Mohammad Ebrahim Afshar

    Institute of Biomaterials and Biomedical Engineering, Donnelly Centre for Cellular and Biomolecular Research, Department of Biochemistry, Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
    Competing interests
    No competing interests declared.
  7. Majid Ebrahimi

    Institute of Biomaterials and Biomedical Engineering, Donnelly Centre for Cellular and Biomolecular Research, Department of Biochemistry, Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
    Competing interests
    No competing interests declared.
  8. Roman Tsukanov

    3rd Institute of Physics - Biophysics, Cluster of Excellence Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells" (MBExC)", Georg August University, Göttingen, Germany
    Competing interests
    No competing interests declared.
  9. Nazar Oleksiievets

    3rd Institute of Physics - Biophysics, Cluster of Excellence Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells" (MBExC)", Georg August University, Göttingen, Germany
    Competing interests
    No competing interests declared.
  10. Jörg Enderlein

    3rd Institute of Physics - Biophysics, Cluster of Excellence Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells" (MBExC)", Georg August University, Göttingen, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5091-7157
  11. Penney M Gilbert

    Institute of Biomaterials and Biomedical Engineering, Donnelly Centre for Cellular and Biomolecular Research, Department of Biochemistry, Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5509-9616
  12. Timo Betz

    Third Institute of Physics, Universtity of Göttingen, Göttingen, Germany
    For correspondence
    timo.betz@phys.uni-goettingen.de
    Competing interests
    Timo Betz, Patent application filed for the chamber. Application number: LU101799.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1548-0655

Funding

Human Frontier Science Program (RGP0018/2017)

  • Penney M Gilbert
  • Timo Betz

H2020 European Research Council (771201)

  • Timo Betz

Natural Sciences and Engineering Research Council of Canada (RGPIN-4357)

  • Penney M Gilbert

Natural Sciences and Engineering Research Council of Canada (RGPIN-7144)

  • Penney M Gilbert

Natural Sciences and Engineering Research Council of Canada (Training Program in Organ-on-a-Chip Engineering and Entrepreneurship Scholarship)

  • Mohammad Ebrahim Afshar

University of Toronto (Canada Research Chair in Endogenous Repair)

  • Penney M Gilbert

Deutsche Forschungsgemeinschaft (SFB 803)

  • Roman Tsukanov
  • Nazar Oleksiievets
  • Jörg Enderlein

Deutsche Forschungsgemeinschaft (EXC 2067/1)

  • Jörg Enderlein
  • Timo Betz

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

Reviewing Editor

  1. Patricia Bassereau, Institut Curie, France

Publication history

  1. Received: June 17, 2020
  2. Accepted: January 17, 2021
  3. Accepted Manuscript published: January 18, 2021 (version 1)
  4. Version of Record published: February 25, 2021 (version 2)

Copyright

© 2021, Hofemeier 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. Arne D Hofemeier
  2. Tamara Limón
  3. Till Moritz Muenker
  4. Bernhard Wallmeyer
  5. Alejandro Jurado
  6. Mohammad Ebrahim Afshar
  7. Majid Ebrahimi
  8. Roman Tsukanov
  9. Nazar Oleksiievets
  10. Jörg Enderlein
  11. Penney M Gilbert
  12. Timo Betz
(2021)
Global and local tension measurements in biomimetic skeletal muscle tissues reveals early mechanical homeostasis
eLife 10:e60145.
https://doi.org/10.7554/eLife.60145

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