Nature’s Strategy for Optimizing Power Generation in Insect Flight Muscle

Maughan, David W.; Vigoreaux, Jim O.

doi:10.1007/0-387-24990-7_12

Cited by 8 publications

(4 citation statements)

References 51 publications

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“…This means that either the IFM myosin isoform enables more F SA force than EMB, and/or another mechanism is operating in the IFM to significantly boost F SA and power. Variation in more than one muscle protein is likely required for prominent SA as IFM has several protein isoform differences compared to other muscles in the fly (30). In particular, evidence is accumulating that a thin filament-based mechanism contributes to IFM SA (10,11).…”

Section: Stretch Activation Of Skinned Drosophila Jump Musclesmentioning

confidence: 99%

An Embryonic Myosin Isoform Enables Stretch Activation and Cyclical Power in Drosophila Jump Muscle

Zhao

Swank

2013

Biophysical Journal

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The mechanism behind stretch activation (SA), a mechanical property that increases muscle force and oscillatory power generation, is not known. We used Drosophila transgenic techniques and our new muscle preparation, the jump muscle, to determine if myosin heavy chain isoforms influence the magnitude and rate of SA force generation. We found that Drosophila jump muscles show very low SA force and cannot produce positive power under oscillatory conditions at pCa 5.0. However, we transformed the jump muscle to be moderately stretch-activatable by replacing its myosin isoform with an embryonic isoform (EMB). Expressing EMB, jump muscle SA force increased by 163% and it generated net positive power. The rate of SA force development decreased by 58% with EMB expression. Power generation is Pi dependent as >4 mM Pi was required for positive power from EMB. Pi increased EMB SA force, but not wild-type SA force. Our data suggest that when muscle expressing EMB is stretched, EMB is more easily driven backward to a weakly bound state than wild-type jump muscle. This increases the number of myosin heads available to rapidly bind to actin and contribute to SA force generation. We conclude that myosin heavy chain isoforms influence both SA kinetics and SA force, which can determine if a muscle is capable of generating oscillatory power at a fixed calcium concentration.

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Section: Stretch Activation Of Skinned Drosophila Jump Musclesmentioning

confidence: 99%

An Embryonic Myosin Isoform Enables Stretch Activation and Cyclical Power in Drosophila Jump Muscle

Zhao

Swank

2013

Biophysical Journal

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“…Although an increase in muscle stiffness theoretically increases the flight system resonance frequency and, therefore, wingbeat frequency (20), the decoupling of fiber stiffness and wingbeat frequency that is evident in our study has been noted previously. Paramyosin phosphorylation site disruption increased wingbeat frequency (44), yet mechanics of IFM skinned fibers exhibited decreased passive, active, and rigor stiffness without affecting kinetics (22). Additional studies at various ages throughout the Drosophila lifespan are required to uncover the detailed relationship between flight ability, protein expression level, mitochondrial performance, and IFM fiber characteristics.…”

Section: Flight Performancementioning

confidence: 99%

Aging Enhances Indirect Flight Muscle Fiber Performance yet Decreases Flight Ability in Drosophila

Miller

Lekkas

Braddock

et al. 2008

Biophysical Journal

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We investigated the effects of aging on Drosophila melanogaster indirect flight muscle from the whole organism to the actomyosin cross-bridge. Median-aged (49-day-old) flies were flight impaired, had normal myofilament number and packing, barely longer sarcomeres, and slight mitochondrial deterioration compared with young (3-day-old) flies. Old (56-day-old) flies were unable to beat their wings, had deteriorated ultrastructure with severe mitochondrial damage, and their skinned fibers failed to activate with calcium. Small-amplitude sinusoidal length perturbation analysis showed median-aged indirect flight muscle fibers developed greater than twice the isometric force and power output of young fibers, yet cross-bridge kinetics were similar. Large increases in elastic and viscous moduli amplitude under active, passive, and rigor conditions suggest that median-aged fibers become stiffer longitudinally. Small-angle x-ray diffraction indicates that myosin heads move increasingly toward the thin filament with age, accounting for the increased transverse stiffness via cross-bridge formation. We propose that the observed protein composition changes in the connecting filaments, which anchor the thick filaments to the Z-disk, produce compensatory increases in longitudinal stiffness, isometric tension, power and actomyosin interaction in aging indirect flight muscle. We also speculate that a lack of MgATP due to damaged mitochondria accounts for the decreased flight performance.

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“…Over the past couple of decades, progress has been made to expand its utility in muscle physiology by developing preparations from two Drosophila thoracic muscles, the indirect flight muscle (IFM) and jump muscle for mechanical evaluation. These two muscles are very interesting as they possess informative and adaptive physiological characteristics [1-3], but combined with the power of Drosophila genetics, their use to answer many interesting and relevant muscle biology questions is greatly enhanced. These muscles have been used to investigate the structure-function characteristics of muscle proteins [4-6], determine mechanisms behind muscle and cardiac diseases [7] and study the molecular basis of muscle fiber type diversity [1, 8].…”

Section: Introductionmentioning

confidence: 99%

Mechanical analysis of Drosophila indirect flight and jump muscles

Swank

2012

Methods

111

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The genetic advantages of Drosophila make it a very appealing choice for investigating muscle development, muscle physiology and muscle protein structure and function. To take full advantage of this model organism, it has been vital to develop isolated Drosophila muscle preparations that can be mechanically evaluated. We describe techniques to isolate, prepare and mechanically analyze skinned muscle fibers from two Drosophila muscle types, the indirect flight muscle and the jump muscle. The function of the indirect flight muscle is similar to vertebrate cardiac muscle, to generate power in an oscillatory manner. The indirect flight muscle is ideal for evaluating the influence of protein mutations on muscle and cross-bridge stiffness, oscillatory power, and deriving cross-bridge rate constants. Jump muscle physiology and structure are more similar to skeletal vertebrate muscle than indirect flight muscle, and it is ideal for measuring maximum shortening velocity, force-velocity characteristics and steady-state power generation.

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Nature’s Strategy for Optimizing Power Generation in Insect Flight Muscle

Cited by 8 publications

References 51 publications

An Embryonic Myosin Isoform Enables Stretch Activation and Cyclical Power in Drosophila Jump Muscle

An Embryonic Myosin Isoform Enables Stretch Activation and Cyclical Power in Drosophila Jump Muscle

Aging Enhances Indirect Flight Muscle Fiber Performance yet Decreases Flight Ability in Drosophila

Mechanical analysis of Drosophila indirect flight and jump muscles

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