Summary
The kinetics of dissociation of myosin from both ends of thick filaments in glycerinated skeletal muscle fibres and myofibrils was studied in the presence of MgATP by use of an optical diffraction method and phase-contrast microscopy. The dissociation velocity,v (=-dL/dt where L is the length of thick filaments at timet), increased with increasing KCl concentration (0.225 to 0.5 m), or increasing pH (6.5 to 8.0) but hardly changed with temperature (5 and 25° C), micromolar concentrations of Ca2+ or sarcomere length (2.4 and 2.75 μm). Over a wide range of filament length, the dissociation velocity could be expressed byv 0exp(αL), wherev 0 andα are positive constants depending upon the dissociation condition. When the effects of crossbridge formation are minimized it was thus shown that the structural stability of thick filaments in a muscle fibre and a myofibril gradually decreases from the central part to the tips of the filaments. On the basis of these results we propose that the length of thick filaments is largely regulated by an accumulated strain mechanism in which the free energy of association of myosin molecules increases with filament length.
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References
Caspar, D. L. D. (1963) Assembly and stability of the tobacco mosaic virus particle.Adv. Protein Chem. 18, 37–121.
Caspar, D. L. D. (1980) Movement and self-control in protein assemblies. Quasi-equivalence revisited.Biophys. J. 32, 103–38.
Craig, R. (1977) Structure of A-segments from frog and rabbit skeletal muscle.J. molec. Biol. 109, 69–81.
Davis, J. S. (1981a) The influence of pressure on the self-assembly of the thick filament from the myosin of vertebrate skeletal muscle.Biochem. J. 197, 301–8.
Davis, J. S. (1981b) Pressure-jump studies on the length-regulation kinetics of the self-assembly of myosin from vertebrate skeletal muscle into thick filament.Biochem. J. 197, 309–14.
Davis, J. S., Buck, J. &Greene, E. P. (1982) The myosin dimer: an intermediate in the self-assembly of the thick filament of vertebrate skeletal muscle.FEBS Lett. 140, 293–7.
Fujime, S. (1975) Optical diffraction study of muscle fibers.Biochim. biophys. Acta 379, 227–38.
Fujime, S. (1984) An intensity expression of optical diffraction from striated muscle fibres.J. Musc. Res. Cell Motility 5, 577–87.
Fujime, S. &Yoshino, S. (1978) Optical diffraction study of muscle fibers. I. A theoretical basis.Biophys. Chem. 8, 305–15.
Godfrey, J. E. &Harrington, W. F. (1970) Selfassociation in the myosin system at high ionic strength. II. Evidence for the presence of a monomerdimer equilibrium.Biochemistry 9, 894–908.
Harrington, W. F. &Rodgers, M. E. (1984) Myosin.A. Rev. Biochem. 53, 35–73.
Higuchi, H. &Ishiwata, S. (1982) Dissociation and reconstruction of thick filaments in muscle fibres.Biophysics 22, S207.
Higuchi, H. &Ishiwata, S. (1985) Disassembly kinetics of thick filaments in a rabbit skeletal muscle fiber. Effects of ionic strength, Ca2+ concentration, pH, temperature and cross-bridges on the stability of thick filament structure.Biophys. J. 47, 267–75.
Higuchi,. H. &Umazume, Y. (1985) Localization of the parallel elastic components in frog skinned muscle fibers studied by the dissociation of thick and thin filaments.Biophys. J. 48, 137–47.
Huxley, H. E. (1963) Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle.J. molec. Biol. 7, 281–308.
Ishiwata, S. (1981) Melting from both ends of an A-band in a myofibril. Observation with a phase-contrast microscope.J. Biochem., Tokyo 89, 1647–50.
Ishiwata, S., Muramatsu, K. &Higuchi, H. (1985) Disassembly from both ends of thick filaments in a rabbit skeletal muscle fiber. An optical diffraction study.Biophys. J. 47, 257–66.
Josephs, R. &Harrington, W. F. (1966) Studies on the formation and physical chemical properties of synthetic myosin filaments.Biochemistry 5, 3474–87.
Josephs, R. &Harrington, W. F. (1968) On the stability of myosin filaments.Biochemistry 7, 2834–47.
Kaminer, B. &Bell, A. L. (1966) Myosin filamentogenesis: Effects of pH and ionic concentration.J. molec. Biol. 20, 391–401.
Katsura, I. &Noda, H. (1973) Assembly of myosin molecules into the structure of thick filaments of muscle.Adv. Biophys. 5, 177–202.
Kawamura, M. &Maruyama, K. (1970) Electron microscopic particle length of F-actin polymerized invitro.J. Biochem. Tokyo 67, 437–57.
Kellenberger, E. (1969) Polymorphic assemblies of the same major virus protein subunit. InSymmetry and Function of Biological Systems at the Macromolecular Level (edited byEngstrom, A. andStranberg, B.), pp. 349–66. Stockholm: Almquist & Wicksell.
Niederman, R. &Peters, L. K. (1982) Native bare zone assemblage nucleates myosin filaments assembly.J. molec. Biol. 161, 505–17.
Offer, G. (1972) C-protein and the periodicity in the thick filaments of vertebrate skeletal muscle.Cold Spring Harbor Symp. quant. Biol. 37, 87–93.
Oosawa, F. (1970) Size distribution of protein polymers.J. Theoret. Biol. 27, 69–86.
Oosawa, F. &Asakura, S. (1975)Thermodynamics of the Polymerization of Protein, P. 31. London, New York: Academic Press.
Pepe, F. A. (1967) The myosin filament. I. Structural organization from antibody staining observed in electron microscopy.J. molec. Biol. 27, 203–25.
Squire, J. (1981)The Structural Basis of Muscular Contraction, pp. 471–521. New York: Plenum Press.
Trinick, J. &Cooper, J. (1980) Sequential disassembly of vertebrate muscle thick filaments.J. molec. biol. 141, 315–21.
Wagenknecht, T. &Bloomfield, V. A. (1975) Equilibrium mechanisms of length regulation in linear protein aggregates.Biopolymers 14, 2297–309.
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Higuchi, H., Funatsu, T., Ishijima, A. et al. Accumulated strain mechanism for length determination of thick filaments in skeletal muscle. I. Experimental bases. J Muscle Res Cell Motil 7, 491–500 (1986). https://doi.org/10.1007/BF01753565
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DOI: https://doi.org/10.1007/BF01753565