RRC ID 30807
Author Weitkunat M, Kaya-Çopur A, Grill SW, Schnorrer F.
Title Tension and force-resistant attachment are essential for myofibrillogenesis in Drosophila flight muscle.
Journal Curr. Biol.
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.
Volume 24(7)
Pages 705-16
Published 2014-3-31
DOI 10.1016/j.cub.2014.02.032
PII S0960-9822(14)00200-0
PMID 24631244
MeSH Animals Biomechanical Phenomena Drosophila / anatomy & histology* Drosophila / physiology Flight, Animal / physiology* Muscle Development* Muscles / anatomy & histology Muscles / physiology
IF 8.851
Times Cited 25
WOS Category BIOCHEMISTRY & MOLECULAR BIOLOGY CELL BIOLOGY
Resource
Drosophila 10275R-1 10275R-3