Regulation and Molecular Mechanics of Asynchronous Flight Muscle

DICKINSON, M; GORDON, S; IRVING, T; MAUGHAN, D; FARMAN, G; FRYE, M; BEKYAROVA, T; Caltech; UC, Berkeley; Illinois Inst. of Tech.; Univ. of Vermont; Illinois Inst. of Tech.; Caltech; Illinois Inst. of Tech.; : Regulation and Molecular Mechanics of Asynchronous Flight Muscle

The extraordinary success of many insect is due in large part to the evolution of powerful asynchronous flight muscles. Unlike twitch muscles, which contract one-for-one with motor spikes, these specialized muscles exhibit an accentuated form of stretch-dependent activation. The use of stretch as the primary means of activation and deactivation enables muscles to contract cyclically at high frequency without the requirement of large internal membrane compartments for calcium release and uptake. Although important both for the evolutionary radiation of insects and as a model system for muscle physiology, the physiology of asynchronous muscles is still poorly understood in many regards. Research reported here relates to two critical issues: (1) the means by which the power output of these muscles is regulated by the nervous system, and (2) the molecular basis of stretch activation. We studied the neural control of power output by recording muscle spikes in tethered fruit flies, Drosophila, subjected to visual stimuli that elicited changes in lift. We then constructed transgenic flies expressing the calcium reporter, cameleon, in the asynchronous muscles to measure the steady-state Ca2+ levels produced by different frequencies of neural activation. The results suggest that flies may regulate power in asynchronous muscles by recruiting crossbridges via changes in sacroplasmic Ca2+. We studied the structural basis of stretch activation by aiming a narrow high energy x-ray beam at the flight muscles of Drosophila flying within a visual closed-loop flight arena. This technique makes it possible to measure the motion of structural proteins within an active muscle as it cyclically shortens and lengthens in a living animal. The results are consistent with recent independent research on the molecular basis of stretch-activation.

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