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Alternate energy transduction routes in chemically skinned rabbit psoas muscle fibres: a further study of the effect of MgATP over a wide concentration range

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Summary

Complex stiffness data were studied over an extended range of MgATP concentrations (3 µm-5mm) in single fibres of Ca2+-activated, chemically skinned adult rabbit psoas. The data were analysed in terms of a model involving three exponential processes, the presence of which was previously observed in fully activated muscles. As fibres were transferred from a rigor solution into solutions of gradually increasing MgATP concentration, the three processes appeared sequentially, each with a uniqueK m. The order of appearance as MgATP increases is (1) the slowest of the three processes [designated process (A)], (2) the fastest of the three processes [designated (C)], and (3) process (B), which occupies the middle range of frequencies; theK ms are approximately 10 µm, 0.2mm, and 0.8mm, respectively. The single phase advance [process (A)] remaining at very low substrate concentrations was found to be better described by a distribution of rate constants than by a single rate constant. The influence of substrate concentration on these processes is examined and two parallel hydrolysis routes are suggested as a possible mechanism.

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References

  • ABBOTT, R. H. (1973) The effects of fibre length and calcium ion concentration on the dynamic response of glycerol extracted insect fibrillar muscle.J. Physiol. 231, 195–208.

    Google Scholar 

  • BÖTTCHER, C. J. P. (1952)Theory of Electrical Polarization, pp. 363–374. Amsterdam: Elsevier.

    Google Scholar 

  • BRANDT, P. W., CHAPPELL, E. & JEWELL, B. R. (1976) A robust transducer suitable for measuring forces of 1 µN.J. Physiol. 258, 43–4P (abstract).

    Google Scholar 

  • BRANDT, P. W., COX, R. N. & KAWAI, M. (1980) Can the binding of Ca2+ to two regulatory sites on troponin-C determine the steep pCa/tension relation of skeletal muscle?Proc. natn. Acad. Sci. U.S.A. 77, 4717–20.

    Google Scholar 

  • BREMEL, R. D. & WEBER, A. (1972) Cooperation within actin filament in vertebrate skeletal muscle.Nature New Biol. 238, 97–101.

    Google Scholar 

  • CHAPLAIN, R. A. & FROMMELT, B. (1968) On the contractile mechanism of insect fibrillar flight muscle. I. The dynamics and energetics of the linearized system.Kybernetick 5, 1–17.

    Google Scholar 

  • COLE, K. S. & COLE, R. H. (1941) Dispersion and absorption in dielectrics. I. Alternating current characteristics.J. Chem. Phys. 9, 341–51.

    Google Scholar 

  • EASTWOOD, A. B., WOOD, D. S., BOCK, K. L. & SORENSON, M. M. (1979) Chemically skinned mammalian skeletal muscle. I. The structure of skinned rabbit psoas.Tiss. Cell 11, 553–66.

    Google Scholar 

  • EISENBERG, E. & GREENE, L. E. (1980) The relation of muscle biochemistry to muscle physiology.Ann. Rev. Physiol. 42, 293–309.

    Google Scholar 

  • HUXLEY, A. F. (1957) Muscle structure and theories of contraction.Prog. Biophys. 7, 255–318.

    Google Scholar 

  • HUXLEY, A. F. (1974) Muscular contraction.J. Physiol. 243, 1–43.

    Google Scholar 

  • HUXLEY, A. F. & SIMMONS, R. M. (1971) Proposed mechanism of force generation in striated muscle.Nature 233, 533–8.

    Google Scholar 

  • JULIAN, F. J., SOLLINS, K. R. & SOLLINS, M. R. (1974) A model for the transient and steady-state mechanical behavior of contracting muscle.Biophys. J. 14, 546–62.

    Google Scholar 

  • KAWAI, M. (1978) Head rotation or dissociation? A study of exponential rate processes in chemically skinned rabbit muscle fibers when MgATP concentration is changed.Biophys. J. 22, 97–103.

    Google Scholar 

  • KAWAI, M. (1979) Effect of MgATP on cross-bridge kinetics in chemically skinned rabbit psoas fibers as measured by sinusoidal analysis technique. InCross-bridge Mechanism in Muscle Contraction (edited by SUGI, H. and POLLACK, G. H.), pp. 149–169. Tokyo: University of Tokyo Press.

    Google Scholar 

  • KAWAI, M. & BRANDT, P. W. (1976) Two rigor states in skinned crayfish single muscle fibers.J. gen. Physiol. 68, 267–80.

    Google Scholar 

  • KAWAI, M. & BRANDT, P. W. (1977) Effect of MgATP on stiffness measured at two frequencies in Ca2+-activated fibres.Proc. natn. Acad. Sci. 74, 4073–5.

    Google Scholar 

  • KAWAI, M. & BRANDT, P. W. (1979) Effect of ATP buffer concentration on the mechanical rate constants in chemically skinned rabbit psoas fibers.Biophys. J. 25, 270a (abstract).

    Google Scholar 

  • KAWAI, M. & BRANDT, P. W. (1980) Sinusoidal analysis; a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfish.J. Mus. Res. Cell Motil. 1, 279–303.

    Google Scholar 

  • KAWAI, M., BRANDT, P. W. & ORENTLICHER, M. (1977) Dependence of energy transduction in intact skeletal muscles on the time in tension.Biophys. J. 18, 161–72.

    Google Scholar 

  • KAWAI, M., COX, R. N. & BRANDT, P. W. (1981) Effect of Ca ion concentration on crossbridge kinetics in rabbit psoas fibres: Evidence for the presence of two Ca-activated states of thin filament.Biophys. J. (in press).

  • LYMN, R. W. & TAYLOR, E. W. (1971) The mechanism of adenosine triphosphate hydrolysis by actomyosin.Biochemistry 10, 4617–24.

    Google Scholar 

  • MARTELL, A. E. (1964)Stability Constants of Metal-ion Complexes. London: The Chemical Society.

    Google Scholar 

  • PODOLSKY, R. J. & NOLAN, A. C. (1973) Muscle contraction transients, cross-bridge kinetics, and the Fenn effect.Cold Spring Harb. Symp. quant. Biol. 37, 661–8.

    Google Scholar 

  • PRINGLE, J. W. S. (1967) The contractile mechanism of insect fibrillar muscle.Prog. biophys. molec. Biol. 17, 1–60.

    Google Scholar 

  • REUBEN, J. P., BRANDT, P. W., BERMAN, M. & GRUNDFEST, H. (1971) Regulation of tension in the skinned crayfish muscle fiber. I. Contraction and relaxation in the absence of Ca (pCa>9).J. gen. Physiol. 57, 385–407.

    Google Scholar 

  • STEIGER, G. J., BRADY, A. J. & TAN, S. T. (1978) Intrinsic regulatory properties of contractility in the myocardium.Circulation Res. 42, 339–50.

    Google Scholar 

  • STEIN, L. A., SCHWARZ, R. P., CHOCK, P. B. & EISENBERG, E. (1979) Mechanism of actomyosin adenosine triphosphatase. Evidence that adenosine 5′-triphosphate hydrolysis can occur without dissociation of the actomyosin complex.Biochemistry 18, 3895–909.

    Google Scholar 

  • TONOMURA, Y. (1978) Functional implications of the two-headed structure of myosin.Sixth Int. Biophys. Cong. Abst. 74.

  • WHITE, D. C. S. & THORSON, J. (1972) Phosphate starvation and the nonlinear dynamics of insect fibrillar flight muscle.J. gen. Physiol. 60, 307–36.

    Google Scholar 

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Cox, R.N., Kawai, M. Alternate energy transduction routes in chemically skinned rabbit psoas muscle fibres: a further study of the effect of MgATP over a wide concentration range. J Muscle Res Cell Motil 2, 203–214 (1981). https://doi.org/10.1007/BF00711870

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