Aging enhances indirect flight muscle fiber performance yet decreases flight ability in Drosophila |
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Authors: | Miller Mark S Lekkas Panagiotis Braddock Joan M Farman Gerrie P Ballif Bryan A Irving Thomas C Maughan David W Vigoreaux Jim O |
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Institution: | * Department of Molecular Physiology and Biophysics, 121 HSRF Building, University of Vermont, Burlington, Vermont † Department of Biology, 120A Marsh Life Sciences Building, University of Vermont, Burlington, Vermont ‡ Vermont Genetics Network Proteomics Facility, 216 Marsh Life Science Building, University of Vermont, Burlington, Vermont § Biophysics Collaborative Access Team and Center for Synchrotron Radiation Research and Instrumentation, Department of Biological, Chemical, and Physical Sciences, Illinois Institute of Technology, Chicago, Illinois |
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Abstract: | 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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