Global and local tension measurements in biomimetic skeletal muscle tissues reveals early mechanical homeostasis
- University of Münster, Germany
- University of Toronto, Canada
- Georg August University, Germany
- 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
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.
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.
Metrics
-
- 5,332
- views
-
- 570
- downloads
-
- 27
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Global and local tension measurements in biomimetic skeletal muscle tissues reveals early mechanical homeostasis
eLife 10:e60145.
https://doi.org/10.7554/eLife.60145
Further reading
-
- Neuroscience
- Physics of Living Systems
Recent experimental studies showed that electrically coupled neural networks like in mammalian inferior olive nucleus generate synchronized rhythmic activity by the subthreshold sinusoidal-like oscillations of the membrane voltage. Understanding the basic mechanism and its implication of such phenomena in the nervous system bears fundamental importance and requires preemptively the connectome information of a given nervous system. Inspired by these necessities of developing a theoretical and computational model to this end and, however, in the absence of connectome information for the inferior olive nucleus, here we investigated interference phenomena of the subthreshold oscillations in the reference system Caenorhabditis elegans for which the structural anatomical connectome was completely known recently. We evaluated how strongly the sinusoidal wave was transmitted between arbitrary two cells in the model network. The region of cell-pairs that are good at transmitting waves changed according to the wavenumber of the wave, for which we named a wavenumber-dependent transmission map. Also, we unraveled that (1) the transmission of all cell-pairs disappeared beyond a threshold wavenumber, (2) long distance and regular patterned transmission existed in the body-wall muscles part of the model network, and (3) major hub cell-pairs of the transmission were identified for many wavenumber conditions. A theoretical and computational model presented in this study provided fundamental insight for understanding how the multi-path constructive/destructive interference of the subthreshold oscillations propagating on electrically coupled neural networks could generate wavenumber-dependent synchronized rhythmic activity.
-
- Developmental Biology
- Physics of Living Systems
Shape changes of epithelia during animal development, such as convergent extension, are achieved through the concerted mechanical activity of individual cells. While much is known about the corresponding large-scale tissue flow and its genetic drivers, fundamental questions regarding local control of contractile activity on the cellular scale and its embryo-scale coordination remain open. To address these questions, we develop a quantitative, model-based analysis framework to relate cell geometry to local tension in recently obtained time-lapse imaging data of gastrulating Drosophila embryos. This analysis systematically decomposes cell shape changes and T1 rearrangements into internally driven, active, and externally driven, passive, contributions. Our analysis provides evidence that germ band extension is driven by active T1 processes that self-organize through positive feedback acting on tensions. More generally, our findings suggest that epithelial convergent extension results from the controlled transformation of internal force balance geometry which combines the effects of bottom-up local self-organization with the top-down, embryo-scale regulation by gene expression.
