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Muscle filament lattices and stretch-activation: The match-mismatch model reassessed

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Summary

A mechanism for the observed enhanced stretch-activation phenomenon in insect asynchronous flight muscles has been postulated and developed in terms of the matched helical structures of the actin and myosin filaments in the asynchronous flight muscles ofLethocerus. It was suggested that at different sarcomere lengths with different filament overlaps there would be a changing probability of myosin crossbridge attachment to actin according to whether there was match or mismatch between the myosin and actin arrays. Evidence is provided here that, whenLethocerus structure is considered in detail, the explanation appears to fail. Results on other insect asynchronous flight muscles of different structure (e.g.Apis) also seem to contradict the match-mismatch model. All striated muscle types considered here (fish, frog,Lethocerus, Apis, blowfly) appear to be designed to give constant probability of crossbridge attachment to actin as the filaments move axially, apart from the well-known effects of changing total filament overlap. Alternative stretch-activation mechanisms are considered, especially in terms of the unusual thin filament regulatory system in some insect asynchronous flight muscles.

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References

  • Abbott, R. H. &Cage, P.E. (1984) A possible mechanism of length activation in insect fibrillar flight muscle.J. Muscle Res. Cell Motil. 5, 387–97.

    Google Scholar 

  • Auber, J. (1967) Remarques sur la structure des fibrilles des muscles du vol d'Insectes, au niveau de la strie.C.R. Acad. Sci. Ser. D.264, 2916–18.

    Google Scholar 

  • Bullard, B., Leonard, K., Larkins, A. Butcher, G., Karlik, C. &Fyrberg, E. (1988) Troponin of asynchronous flight muscle.J. Mol. Biol. 204, 621–37.

    Google Scholar 

  • Cheng, N. &Deatherage, J. F. (1989) Three-dimensional reconstruction of the Z disk of sectioned bee flight muscle.J. Cell Biol. 108, 1761–74.

    Google Scholar 

  • Deatherage, J. F., Cheng, N. &Bullard, B. (1989) Arrangement of filaments and cross-links in the bee flight muscle Z disk by image analysis of oblique sections.J. Cell Biol. 108, 1775–82.

    Google Scholar 

  • Descherevskii, V. I. (1971) A kinetic theory of striated muscle contraction.Biorheology 7, 147–70.

    Google Scholar 

  • Egelman, E. H., Francis, N. &DeRosier, D. J. (1982) F-actin is a helix with a random variable twist.Nature 298, 131–5.

    Google Scholar 

  • Elliott, G. F. (1965) Low-angle X-ray diffraction patterns from insect flight muscle.J. Mol. Biol. 13, 956–8.

    Google Scholar 

  • Freundlich, A. &Squire, J. M. (1983) 3-dimensional structure of the insect (Lethocerus) flight muscle M-band.J. Mol. Biol. 169, 439–53.

    Google Scholar 

  • Fuller, G. &Squire, J. M. (1987) 4-stranded helical arrangement of myosin heads on insect (Lethocerus) flight muscle thick filaments.J. Muscle Res. Cell Motil. 8, 67.

    Google Scholar 

  • Haselgrove, J. C. (1973) X-ray evidence for a conformational change in the actin-containing filaments of vertebrate striated muscle.Cold Spring Harbor Symp. Quant. Biol. 37, 341–52.

    Google Scholar 

  • Haselgrove, J. C. &Reedy, M. K. (1978) Modelling rigor crossbridge patterns in muscle: I. Initial studies of the rigor lattice of insect flight muscle.Biophys. J. 24, 713–28.

    Google Scholar 

  • Haselgrove, J. C. &Reedy, M. K. (1984) Geometrical constraints affecting crossbridge formation in insect flight muscle.J. Muscle Res. Cell Motil. 5, 3–24.

    Google Scholar 

  • Holmes, K. C., Tregear, R. T. &Barrington-Leigh, J. (1980) Interpretation of the low angle X-ray diffraction from insect flight muscle in rigor.Proc. R. Soc. Lond. B. 207, 13–33.

    Google Scholar 

  • Huxley, H. E. (1973) Structural changes in the actin- and myosin-containing filaments during contraction.Cold Spring Harbor Symp. Quant. Biol. 37, 361–76.

    Google Scholar 

  • Huxley, H. E. &Brown, W. (1967) The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor.J. Mol. Biol. 30, 383–434.

    Google Scholar 

  • Jewell, B. R. &Ruegg, C. (1966) Oscillatory contraction of insect fibrillar muscle after glycerol extraction.Proc. R. Soc. Lond. B. 164, 428–59.

    Google Scholar 

  • Luther, P. K. &Squire, J. M. (1980) 3-dimensional structure of the vertebrate muscle A-band. II: The myosin filament superlattice.J. Mol. Biol. 141, 409–39.

    Google Scholar 

  • Luther, P. K., Munro, P. M. G. &Squire, J. M. (1981) 3-dimensional structure of the vertebrate muscle A-band. III: M-region structure and myosin filament symmetry.J. Mol. Biol. 151, 703–30.

    Google Scholar 

  • Morris, E. P., Squire, J. M. &Fuller, G. (1992) The 4-stranded helical arrangement of myosin heads on insect (Lethocerus) thick filaments.J. Struct. Biol. (in press).

  • Parry, D. A. D. &Squire, J. M. (1973) Structural role of tropomyosin in muscle regulation: Analysis of the X-ray diffraction patterns from relaxed and contracting muscles.J. Mol. Biol. 75, 33–55.

    Google Scholar 

  • Pringle, J. W. S. (1967) The contractile mechanism of insect fibrillar muscle.Prog. Biophys. Mol. Biol. 17, 1–60.

    Google Scholar 

  • Pringle, J. W. S. (1978) Croonian Lecture 1977: Stretch activation of muscle-function and mechanism.Proc. R. Soc. Lond. B.201, 107–30.

    Google Scholar 

  • Reedy, M. K. (1968) Ultrastructure of insect flight muscle I: Screw sense and structural grouping in the rigor crossbridge lattice.J. Mol. Biol. 31, 155–76.

    Google Scholar 

  • Reedy, M. K., Bahr, G. F. &Fischman, D. A. (1973) How many myosins per cross-bridge? I. Flight muscle myofibrils from the blowfly,Sarcophaga bullata.Cold Spring Harbor Symp. Quant. Biol. 37, 397–421.

    Google Scholar 

  • Reedy, M. K., Leonard, K. R., Freeman, R. &Arad, T. (1981) Thick filament mass determination by electron scattering measurements with the scanning transmission electron microscope.J. Muscle Res. Cell Motil. 2, 45–64.

    Google Scholar 

  • Squire, J. M. (1972) General model of myosin filament structure. II. Myosin filaments and cross-bridge interactions in vertebrate striated and insect flight muscles.J. Mol. Biol. 72, 125–38.

    Google Scholar 

  • Squire, J. M. &Harford, J. J. (1988) Actin filament organisation and myosin head labelling patterns in vertebrate skeletal muscles in the rigor and weak binding states.J. Muscle Res. Cell Motil. 9, 344–58.

    Google Scholar 

  • Steiger, G. J. (1977) Stretch activation and tension transients in cardiac, skeletal and insect flight muscle. InInsect Flight Muscle (edited by Tregear, R. T.) pp. 221–68. Amsterdam: North-Holland.

    Google Scholar 

  • Trombitas, K., Baatsen, P. H. W. W. &Pollack, G. H. (1986) Rigor bridge angle: Effects of applied stress and preparative procedure.J. Ultrastruct. Mol. Struct. Res. 97, 39–49.

    Google Scholar 

  • White, D. C. S. &Thorson, J. (1973) The kinetics of muscle contraction.Prog. Biophys. 27, 175–255.

    Google Scholar 

  • Wray, J. S. (1979a) Structure of the backbone in myosin filaments of muscle.Nature 277, 37–40.

    Google Scholar 

  • Wray, J. S. (1979b) Filament geometry and the activation of insect flight muscle.Nature 280, 325–6.

    Google Scholar 

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Squire, J.M. Muscle filament lattices and stretch-activation: The match-mismatch model reassessed. J Muscle Res Cell Motil 13, 183–189 (1992). https://doi.org/10.1007/BF01874155

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  • DOI: https://doi.org/10.1007/BF01874155

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