Directionality of developing skeletal muscles is set by mechanical forces

Kazunori Sunadome, Alek G. Erickson, Delf Kah, Ben Fabry, Csaba Adori, Polina Kameneva, Louis Faure, Shigeaki Kanatani, Marketa Kaucka, Ivar Dehnisch Ellström, Marketa Tesarova, Tomas Zikmund, Jozef Kaiser, Steven Edwards, Koichiro Maki, Taiji Adachi, Takuya Yamamoto, Kaj Fried () and Igor Adameyko ()
Additional contact information
Kazunori Sunadome: Karolinska Institutet
Alek G. Erickson: Karolinska Institutet
Delf Kah: University of Erlangen-Nuremberg
Ben Fabry: University of Erlangen-Nuremberg
Csaba Adori: Karolinska Institutet
Polina Kameneva: Medical University Vienna
Louis Faure: Medical University Vienna
Shigeaki Kanatani: Karolinska Institutet
Marketa Kaucka: Max Planck Institute for Evolutionary Biology
Ivar Dehnisch Ellström: Spinalis Foundation
Marketa Tesarova: Brno University of Technology
Tomas Zikmund: Brno University of Technology
Jozef Kaiser: Brno University of Technology
Steven Edwards: KTH Royal Institute of Technology
Koichiro Maki: Kyoto University
Taiji Adachi: Kyoto University
Takuya Yamamoto: Kyoto University
Kaj Fried: Karolinska Institutet
Igor Adameyko: Karolinska Institutet

Nature Communications, 2023, vol. 14, issue 1, 1-24

Abstract: Abstract Formation of oriented myofibrils is a key event in musculoskeletal development. However, the mechanisms that drive myocyte orientation and fusion to control muscle directionality in adults remain enigmatic. Here, we demonstrate that the developing skeleton instructs the directional outgrowth of skeletal muscle and other soft tissues during limb and facial morphogenesis in zebrafish and mouse. Time-lapse live imaging reveals that during early craniofacial development, myoblasts condense into round clusters corresponding to future muscle groups. These clusters undergo oriented stretch and alignment during embryonic growth. Genetic perturbation of cartilage patterning or size disrupts the directionality and number of myofibrils in vivo. Laser ablation of musculoskeletal attachment points reveals tension imposed by cartilage expansion on the forming myofibers. Application of continuous tension using artificial attachment points, or stretchable membrane substrates, is sufficient to drive polarization of myocyte populations in vitro. Overall, this work outlines a biomechanical guidance mechanism that is potentially useful for engineering functional skeletal muscle.

Date: 2023
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DOI: 10.1038/s41467-023-38647-7

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