Summary
We found that the lengths of all sarcomeres spontaneously oscillated in an isolated skeletal myofibril, when both ends were fixed, submillimolar to millimolar concentrations of ATP, ADP and inorganic phosphate (Pi) were present, and Ca2+ was removed. Narrowing and widening of an H-zone and an I-band were observed corresponding to the shortening and lengthening of a sarcomere, suggesting that thick and thin filaments slide past each other. The oscillation of each sarcomere was asymmetrical, consisting of a rapid lengthening phase and a slow shortening phase. The period of oscillation was about 3 s; the peak-to-peak amplitude of oscillation reached as much as 30% of the average sarcomere length. The propagation of the sarcomere oscillation along the long axis of the myofibril was observed occasionally in single myofibrils and frequently in bundles of myofibrils. The ‘state’-diagram showing the concentration range of ADP and Pi in which contraction, oscillation or relaxation of myofibrils occurs in the presence of ATP and the absence of Ca2+ suggested that the oscillation is a third state of skeletal muscle located in between the contracting and relaxing states.
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References
Abbott, R. H. &Cage, P. E. (1984) A possible mechanism of length activation in insect fibrillar flight muscle.J. Musc. Res. Cell. Motility 5, 387–97.
Abbott, R. H. &Mannherz, H. G. (1970) Activation by MgADP and the correlation between tensions and ATPase activity in insect fibrillar muscle.Pflügers Arch. 321, 223–32.
Armstrong, C. F., Huxley, A. F. &Julian, F. J. (1966) Oscillatory responses in frog skeletal muscle fibers.J. Physiol. (Lond.) 186, 26–7.
Chalovich, J. M., Chock, P. B. &Eisenberg, E. (1981) Mechanism of action of troponin tropomyosin. Inhibition of actomyosin ATPase activity without inhibition of myosin binding to actin.J. biol. Chem. 256, 575–8.
Cooke, R. &Pate, E. (1985) The effects of ADP and phosphate on the contraction of muscle fibers.Biophys. J. 48, 789–98.
Curtin, N. A. &Davies, R. E. (1973) Chemical and mechanical changes during stretching of activated frog skeletal muscle.Cold Spring Harb. Symp. Quant. Biol. 37, 619–26.
Eisenberg, E. &Hill, T. (1985) Muscle contraction and free energy transduction in biological systems.Science 227, 999–1006.
Endo, M. (1972) Stretch-induced increase in activation of skinned muscle fibres by calcium.Nature 237, 211–3.
Endo, M. (1973) Length dependence of activation of skinned muscle fibers.Cold Spring Harb. Symp. Quant. Biol. 37, 505–10.
Fabiato, A. &Fabiato, F. (1978) Myofilament-generated tension oscillations during partial calcium activation and activation dependence of the sarcomere lengthtension relation of skinned cardiac cells.J. gen Physiol. 72, 667–99.
Goodall, M. C. (1956) Auto-oscillations in extracted muscle fibre systems.Nature 177, 1238–9.
Hibberd, M. G., Dantzig, J. A., Trentham, D. R. &Goldman, Y. E. (1985) Phosphate release and force generation in skeletal muscle fibers.Science 228, 1317–9.
Higuchi, H. &Umazume, Y. (1985) Localization of the parallel elastic components in frog skinned muscle fibers studied by the dissociation of the A- and I-bands.Biophys. J. 48, 137–47.
Horowits, R., Kempner, E. S., Bisher, M. E. &Podolsky, R. J. (1986) A physiological role for titin and nebulin in skeletal muscle.Nature 323, 160–4.
Ishiwata, S. &Funatsu, T. (1985) Does actin bind to the ends of thin filaments in skeletal muscle?J. Cell Biol. 100, 282–91.
Ishiwata, S., Okamura, N. &Shimizu, H. (1987) Spontaneous oscillation of sarcomeres in skeletal myofibril. Observation with a phase-contrast microscope.J. Musc. Res. Cell Motility 8, 275 (Abstr.).
Iwazumi, T. &Pollack, G. H. (1981) The effect of sarcomere non-uniformity on the sarcomere lengthtension relationship of skinned fibers.J. cell. Physiol. 106, 321–37.
Jewell, B. R. &Rüegg, J. C. (1966) Oscillatory contraction of insect fibrillar muscle after glycerol extraction.Proc. Roy. Soc. B. 164, 428–59.
Kawai, M. (1986) The role of orthophosphate in crossbridge kinetics in chemically skinned rabbit psoas fibres as detected with sinusoidal and step length alterations.J. Musc. Res. Cell Motility 7, 421–34.
Kushmerick, M. J. &Podolsky, R. J. (1969) Ionic mobility in muscle cells.Science 166, 1297–8.
Lienhard, G. E. &Secemski, I. I. (1973) P1, P5Di (adenosine-5′) pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase.J. biol. Chem. 248, 1121–3.
Lorand, L. &Moos, C. (1956) Auto-oscillations in extracted muscle fibre systems.Nature 177, 1239.
Magid, A. &Law, D. J. (1985) Myofibrils bear most of the resting tension in frog skeletal muscle.Science 230, 1280–2.
Mannherz, H. G. (1968) ATP-spaltung und ATP-diffusion in oscillierenden extrahierten muskelfasern.Pflügers Arch. 303, 230–48.
Mooseker, M. S., Pratt, M., Kiehart, D. P. &Stephens, R. E. (1977) Cyclic contraction and relaxation of sarcomeres in isolated myofibrils.Biophys. J. 17, 173a (Abstr.).
Murase, M., Tanaka, H., Nishiyama, K. &Shimizu, H. (1986) A three-state model for oscillation in muscle: sinusoidal analysis.J. Musc. Res. Cell Motility 7, 2–10.
Natori, R. (1954) The role of myofibrils, sarcoplasma and sarcolemma in muscle contraction.Jikei Med. J. 1, 18–28.
Onodera, N. &Umazume, Y. (1984) Periodic contraction of skinned muscle fiber under high pH.Biophys. (Jpn) 24, S84 (Abstr.).
Pratt, M. M., Mooseker, M. S., Kiehart, D. P. &Stephens, R. E. (1976) Cyclic contraction and relaxation of glycerinated myofibrils isolated from skeletal muscle.Biol. Bull. 151, 426 (Abstr.).
Pringle, J. W. (1978) Stretch activation of muscle: function and mechanism.Proc. Roy. Soc. B201, 107–30.
Rüegg, J. C., Steiger, G. J. &Schädler, M. (1971) Mechanical activation of the contractile system in skeletal muscle.Pflügers Arch. 319, 139–45.
Schädler, M., Steiger, G. &Rüegg, J. C. (1969) Tension transients in glycerol-extracted fibres of insect fibrillar muscle (Lethocerus maximus).Experientia 25, 942–3.
Steiger, G. J. (1977) Stretch activation and tension transients in cardiac, skeletal and insect flight muscle. InInsect Flight Muscle (edited byR. T. Tregear) pp. 221–68. Amsterdam: North-Holland.
Stephenson, D. G. &Williams, D. A. (1982) Effects of sarcomere length on the force-pCa relation in fast- and slow-twitch skinned muscle fibres from the rat.J. Physiol. (Lond.) 333, 637–53.
Stephenson, D. G. &Wendt, I. R. (1984) Length dependence of changes in sarcoplasmic calcium concentration and myofibrillar calcium sensitivity in striated muscle fibres.J. Musc. Res. Cell Motility 5, 243–72.
Sugi, H. (1972) Tension changes during and after stretch in frog muscle fibres.J. Physiol. (Lond.) 225, 237–53.
Weber, A. &Murray, J. M. (1973) Molecular control mechanisms in muscle contraction.Physiol. Rev. 53, 612–73.
White, D. C. S. &Thorson, J. (1972) Phosphate starvation and the nonlinear dynamics of insect fibrillar flight muscle.J. gen. Physiol. 60, 307–36.
White, D. C. S. &Thorson, J. (1973) The kinetics of muscle contraction.Prog. Biophys. molec. Biol. 27, 173–255.
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Okamura, N., Ishiwata, S. Spontaneous oscillatory contraction of sarcomeres in skeletal myofibrils. J Muscle Res Cell Motil 9, 111–119 (1988). https://doi.org/10.1007/BF01773733
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DOI: https://doi.org/10.1007/BF01773733