Summary
The specific feature of stretch activation of the indirect flight muscle of the tropical waterbugLethocerus was used to correlate mechanical and structural aspects of muscle contraction. The time courses of the changes in intensities of the strongest equatorial reflections, the (10) and (20) and of the first meridional reflection at 14.5 nm−1 were monitored using synchrotron radiation as a high intensity X-ray source. The ratio of the intensities of the equatorial reflections, (I20/I10), which reflects the mass distribution within the filament lattice array, increases by about 10% relative to the Ca2+-activated level when a rapid stretch is imposed, compared with a 200% change seen when fibres change from the relaxed to the rigor state, while the spacing of the lattice planes decreases by about 1%. The intensity of the first meridional reflection at 14.5 nm−1 decreases by about 35% during stretch activation with a slightly faster time course than the delayed tension increase. The results suggest that the average structure of cycling crossbridges is different from that present in the rigor state.
Similar content being viewed by others
References
Armitage, P. M., Miller, A., Rodger, C. D. &Tregear, R. T. (1973) The structure and function of insect flight muscle.Cold Spring Harbor Symp. on Quant. Biol. 37, 379–87.
Armitage, P. M., Tregear, R. T. &Miller, A. (1975) Effect of activation by calcium on the X-ray diffraction pattern from insect flight muscle.J. Molec. Biol. 92, 39–53.
Eisenberg, E. &Hill, T. L. (1985) Muscle contraction and free energy transduction in biological systems.Science 227, 999–1006.
Goody, R. S., Holmes, K. C., Mannherz, H. G., Barrington-Leigh, J. &Rosenbaum, G. (1975) Cross-bridge conformation as revealed by X-ray diffraction studies on insect flight muscle with ATP analogues.Biophys. J. 15, 687–705.
Goody, R. S., Reedy, M. K., Hofmann, W., Holmes, K. C. &Reedy, M. C. (1985) Binding of myosin subfragment 1 to glycerinated insect flight muscle in the rigor state.Biophys. J. 47, 151–69.
Güth, K., Kuhn, H. J., Tsuchiya, T. &Rüegg, J. C. (1981) Length dependent state of activation- length change dependent kinetics of crossbridges in skinned insect flight muscle.Biophys. Struct. Mech 7, 139–69.
Hendrix, J., Koch, M. H. J. &Brodas, J. (1979) A double focussing X-ray camera for use with synchrotron radiation.Acta Cryst. 12, 467–72.
Hendrix, J., Fürst, H., Hartfield, B. &Dainton, D. (1982) A wire per wire detector system for high counting rate X-ray experiments.Nuclear Instr. and Methods 201, 139–44.
Holmes, K. C. &Blow, D. M. (1980)The Use of X-ray Diffraction in the Study of Protein and Nuclei Acid Structure. New York: Robert Krieger Publ. Comp. Inc.
Huxley, A. F. (1957) Muscle structure and theories of contraction.Prog. Biophys. 7, 255–318.
Huxley, H. E., Faruqi, A. R., Kress, M., Bordas, J. &Koch, M. H. J. (1982) Time-resolved X-ray diffraction studies of the myosin layer-line reflection during muscle contraction.J. Mol. Biol. 158, 637–84.
Huxley, H. E. &Faruqi, A. R. (1983) Time-resolved X-ray diffraction studies on vertebrate striated muscle.Ann. Rev. Biophys. Bioeng. 12, 381–417.
Jewell, B. R. &Rüegg, J. C. (1966) Oscillatory contraction of insect fibrillar muscle after glycerol-extraction.Proc. R. Soc. (Lond.) B164, 429–59.
Lovell, S. J., Knight, P. J. &Harrington, W. F. (1981) Fraction of myosin heads bound to thin filaments in rigor fibrils from insect flight and vertebrate muscle.Nature 293, 664–6.
Miller, A. &Tregear, R. T. (1970) Evidence concerning crossbridge attachment during muscle contraction.Nature 226, 1060–61.
Poole, K. J. V., Rapp, G., Maeda, Y. &Goody, R. S. (1988) Synchrotron radiation studies on insect flight muscle. In:Topics in Current Chemistry 147 (edited byMandelkow, E.) p. 1–129. Heidelberg: Springer.
Pringle, J. W. S. (1981) The evolution of fibrillar muscle in insects.J. Exp. Biol. 94, 1–14.
Rapp, G., Poole, K. J. V., Maeda, Y., Ellis-Davies, G. C. R., Kaplan, J. H., Mccray, J. &Goody, R. S. (1989) Lasers and flashlamps in research on the mechanism of muscle contraction.Ber. Bunsenges. Phys. Chem. 93, 410–15.
Reedy, M. C., Reedy, M. K. &Goody, R. S. (1983) Co-ordinated electron microscopy and X-ray studies of glycerinated insect flight muscle. II. Electron microscopy and image reconstruction of muscle fibres in rigor, in ATP and in MgAMPPPNP.J. Muscle Res. Cell Motil. 4, 55–81.
Reedy, M. C., Reedy, M. K. &Goody, R. S. (1987) The structure of insect flight muscle in the presence of APPNP.J. Muscle Res. Cell Motil. 8, 473–503.
Tregear, R. T. &Miller, A. (1969) Evidence of crossbridge movement during contraction of insect flight muscle.Nature 222, 1185–86.
Wakabayashi, K., Ueno, Y., Amemiya, Y. &Tanaka, H. (1988) Intensity changes of actin-based layer lines from frog skeletal muscles during an isometric contraction. In:Molecular Mechanics of Muscle Contraction (edited bySugi, H. &Pollack, G. H.) pp. 353–67. London: Plenum.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rapp, G., Güth, K., Maeda, Y. et al. Time-resolved X-ray diffraction studies on stretch-activated insect flight muscle. J Muscle Res Cell Motil 12, 208–215 (1991). https://doi.org/10.1007/BF01774040
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01774040