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Am J Physiol Cell Physiol 286: C65-C72, 2004. First published September 3, 2003; doi:10.1152/ajpcell.00257.2003
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MUSCLE CELL BIOLOGY AND CELL MOTILITY

Mutations that affect flightin expression in Drosophila alter the viscoelastic properties of flight muscle fibers

Josh A. Henkin,1,2,3 David W. Maughan,2,3 and Jim O. Vigoreaux1,2,3

1Department of Biology, 2Department of Molecular Physiology and Biophysics, and 3Cell and Molecular Biology Program, University of Vermont, Burlington, Vermont 05405

Submitted 20 June 2003 ; accepted in final form 31 August 2003

Striated muscles across phyla share a highly conserved sarcomere design yet exhibit broad diversity in contractile velocity, force, power output, and efficiency. Insect asynchronous flight muscles are characterized by high-frequency contraction, endurance, and high-power output. These muscles have evolved an enhanced delayed force response to stretch that is largely responsible for their enhanced oscillatory work and power production. In this study we investigated the contribution of flightin to oscillatory work using sinusoidal analysis of fibers from three flightless mutants affecting flightin expression: 1) fln0, a flightin null mutant, 2) Mhc13, a myosin rod point mutant with reduced levels of flightin, and 3) Mhc6, a second myosin rod point mutant with reduced levels of phosphorylated flightin. Fibers from the three mutants show deficits in their passive and dynamic viscoelastic properties that are commensurate with their effect on flightin expression and result in a significant loss of oscillatory work and power. Passive tension and passive stiffness were significantly reduced in fln0 and Mhc13 but not in Mhc6. The dynamic viscous modulus was significantly reduced in the three mutants, whereas the dynamic elastic modulus was reduced in fln0 and Mhc13 but not in Mhc6. Tension generation under isometric conditions was not impaired in fln0. However, when subjected to sinusoidal length perturbations, work-absorbing processes dominated over work-producing processes, resulting in no net positive work output. We propose that flightin is a major contributor to myofilament stiffness and a key determinant of the enhanced delayed force response to stretch in Drosophila flight muscles.

flight muscles; muscle mutants; myosin



Address for reprint requests and other correspondence: J. Henkin, Dept. of Biology, Univ. of Vermont, Burlington, VT 05405 (E-mail: jhenkin{at}zoo.uvm.edu).




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