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Curr Biol. 2014 Mar 31;24(7):705-16. doi: 10.1016/j.cub.2014.02.032. Epub 2014 Mar 13.

Tension and force-resistant attachment are essential for myofibrillogenesis in Drosophila flight muscle.

Author information

1
Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany.
2
Max Planck Institute for the Physics of Complex Systems, Nöthnitzer Strasse 38, 01187 Dresden, Germany; Max Planck Institute for Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany.
3
Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany. Electronic address: schnorrer@biochem.mpg.de.

Abstract

BACKGROUND:

Higher animals generate an elaborate muscle-tendon network to perform their movements. To build a functional network, developing muscles must establish stable connections with tendons and assemble their contractile apparatuses. Current myofibril assembly models do not consider the impact of muscle-tendon attachment on myofibrillogenesis. However, if attachment and myofibrillogenesis are not properly coordinated, premature muscle contractions can destroy an unstable myotendinous system, leading to severe myopathies.

RESULTS:

Here, we use Drosophila indirect flight muscles to investigate how muscle-tendon attachment and myofibrillogenesis are coordinated. We find that flight muscles first stably attach to tendons and then assemble their myofibrils. Interestingly, this myofibril assembly is triggered simultaneously throughout the entire muscle, suggesting a self-assembly mechanism. By applying laser-cutting experiments, we show that muscle attachment coincides with an increase in mechanical tension before periodic myofibrils can be detected. We manipulated tension buildup within the myotendinous system either by genetically compromising attachment initiation and integrin recruitment to the myotendinous junction or by optically severing tendons from muscle. Both treatments cause strong myofibrillogenesis defects. We find that myosin motor activity is required for both tension formation and myofibril assembly, suggesting that myofibril assembly itself contributes to tension buildup.

CONCLUSIONS:

Our results demonstrate that force-resistant attachment enables a stark tension increase in the myotendinous system. Subsequently, this tension increase triggers simultaneous myofibril self-assembly throughout the entire muscle fiber. As myofibril and sarcomeric architecture as well as their molecular components are evolutionarily conserved, we propose a similar tension-based mechanism to regulate myofibrillogenesis in vertebrates.

PMID:
24631244
DOI:
10.1016/j.cub.2014.02.032
[Indexed for MEDLINE]
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