Abstract
Insect flight is often powered by high wing beat frequencies. Surprisingly, the flight muscles of some insects are capable of driving high wing beats without extensive calcium cycling machinery. Rather than precisely timed signals from motor neurons driving each contraction, nervous stimulation is sporadic, which presumably serves to maintain a moderately elevated intracellular calcium concentration. In this calcium activated state the muscle will also produce a delayed increase in tension that is initiated by a stretch (stretch activation), produced when an antagonist muscle shortens. Although stretch activation is enhanced in insect flight and cardiac muscle, it is a general property of all muscles. Historically, the underlying mechanism of stretch activation has been studied using several model systems. Initial studies relied on mechanical and ultrastructural studies of giant water bug (Lethocerus) flight muscle and vertebrate cardiac muscle. More recently, studies of Drosophila flight muscles have allowed powerful genetic methods to be added to the researcher’s arsenal. Using these systems, several mechanisms have been proposed to explain stretch activation: (i) matching of the thick and thin filament lattices, (ii) passive stress in the connecting filaments,1 (iii) myosin regulatory light chain (RLC) phosphorylation,2, 3 and (iv) stretch sensitive calcium sensitivity.1, 4
While popular, models proposing lattice matching have been challenged by more recent analysis of filament lattice geometries form several insect species.5 Insect flight and cardiac muscle exhibit a high passive stiffness and are therefore very sensitive to applied stretch. Recent results obtained with insect flight and cardiac muscle preparations provide new insight into a possible molecular pathway that explains the effects of thick filament stress on crossbridge formation. Evidence suggests that stress is transmitted through connecting filaments that extend from the Z-band to the thick filament. We propose that thick filament stress relieves an inhibitory conformation of myosin, which has been observed by low angle X-ray diffraction of isolated Lethocerus fiber bundles.6 Release of this inhibition by stretch/stress together with RLC phosphorylation increases the recruitment of force generating crossbridges and leads to stretch activation.
Stretch sensitive calcium sensitivity via the thin filament regulatory system is also an attractive hypothesis that has recently gained experimental support.7 Agianian et al7 showed that isometric tension and stretch activated tension are controlled by different isoforms of troponin C (TnC). Although these results can be explained by a stretch sensitive troponin complex,7 the description does not provide a clear explanation for the large body of evidence suggesting thick filament stress and regulatory light chain phosphorylation are important for stretch activation. Any model for stretch activation must incorporate both thick and thin filament influences. Here it is proposed that Ca++ binding to TnC activates isometric force generation at high calcium levels; however, IFM operate at low “permissive” calcium concentrations and that stretch and/or phosphorylation induced effects on myosin position are required for activation.
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Moore, J.R. (2006). Stretch Activation. In: Nature’s Versatile Engine: Insect Flight Muscle Inside and Out. Molecular Biology Intelligence Unit. Springer, Boston, MA. https://doi.org/10.1007/0-387-31213-7_4
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DOI: https://doi.org/10.1007/0-387-31213-7_4
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