Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Myosin step size: Estimates from motility assays and shortening muscle

  • 60 Accesses

  • 48 Citations

This is a preview of subscription content, log in to check access.

References

  1. Alexandre, A., Reynafarje, B. &Lehninger, A. L. (1978) Stoichiometry of vectorial H+ movements coupled to electron transport and to ATP synthesis in mitochondria.Proc. Natl. Acad. Sci. USA 75, 5296–5300.

  2. Bagshaw, C. R. (1982)Muscle Contraction. (Outline studies in biology), p. 26. London: Chapman & Hall.

  3. Bennett, P. M. &Elliott, A. (1989) The ‘catch’ mechanism in molluscan muscle: an electron microscopy study of freeze-substituted anterior byssus retractor muscle ofMytilus edulis.J. Muscle Res. Cell Motil. 10, 297–311.

  4. Berman, M. C. (1982) Energy coupling and uncoupling of active calcium transport by sarcoplasmic reticulum membranes.Biochim. Biophys. Acta 694, 95–121.

  5. Brenner, B. (1983) Technique for stabilizing the striation pattern in maximally calcium-activated skinned rabbit psoas fibres.Biophys. J. 41, 99–102.

  6. Brenner, B. (1986) The necessity of using two parameters to describe isotonic shortening velocity of muscle tissues: the effect of various interventions upon initial shortening velocity (vi) and curvature (b).Basic Res. Cardiol. 81, 54–69.

  7. Brenner, B. (1988a) An experimental approach to determine crossbridge turnover kinetics during isometric and isotonic steady state contraction using skinned skeletal muscle fibres of the rabbit.Pflügers Archiv 411 (Suppl. 1), R186.

  8. Brenner, B. (1988b) Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibres: implications for regulation of muscle contraction.Proc. Natl. Acad. Sci. USA 85, 3265–9.

  9. Brenner, B. (1991) Rapid dissociation and reassociation of actomyosin crossbridges during force generation: a newly observed facet of crossbridge action in muscle.Proc. Natl. Acad. Sci. USA 88, 10490–4.

  10. Brenner, B. &Eisenberg, E. (1986) The rate of force generation in muscle: correlation with actomyosin ATPase in solution.Proc. Natl. Acad. Sci. USA 83, 3542–6.

  11. Burton, K. (1989) The magnitude of the force rise after rapid shortening and restretch in fibres isolated from rabbit psoas muscle.J. Physiol. (Lond.) 418, 66P.

  12. Burton, K. (1991) Rapid tension recovery in response to shortening steps following a cycle of ramp shortening and large restretch in skinned rabbit psoas fibres.Biophys. J. 59, 35a.

  13. Burton, K. (1992) Stiffness and crossbridge strain following large step stretches at the end of rapid shortening in rabbit psoas skinned single fibres.Biophys. J. 61, A267.

  14. Burton, K. &Simmons, R. M. (1991) Changes in stiffness during the transition from the isometric state to steady shortening in skinned fibres isolated from rabbit psoas muscle.J. Physiol. (Lond.) 434, 63P.

  15. Cecchi, G., Griffiths, P. J. &Taylor, S. (1982) Muscular contraction: Kinetics of crossbridge attachment studied by high-frequency stiffness measurements.Science 217, 70–2.

  16. Civian, M. M. &Podolsky, R. J. (1966) Contraction kinetics of striated muscle fibres following quick changes in load.J. Physiol. (Lond.) 184, 511–34.

  17. Colomo, F., Lombardi, V. &Piazzesi, G. (1989) The recovery of tension in transients during steady lengthening of frog muscle fibres.Pflügers Archiv 414, 245–7.

  18. Cooke, R. &Bialek, W. (1979) Contraction of glycerinated muscle fibers as a function of the ATP concentration.Biophys. J. 28, 241–58.

  19. Curtin, N. A. &Woledge, R. C. (1978) Energy changes and muscular contraction.Physiol. Rev. 58, 690–761.

  20. Edman, K. A. P. (1980) Depression of mechanical performance by active shortening during twitch and tetanus of vertebrate muscle fibres.Acta Physiol. Scand. 109, 15–26.

  21. Edman, K. A. P., Elzinga, G. &Noble, I. M. (1981) Critical sarcomere extension required to recruit a decaying component of extra force during stretch in tetanic contractions of frog skeletal muscle fibres.J. Gen. Physiol. 78, 365–82.

  22. Eisenberg, E. &Kielley, W. W. (1973) Evidence for a refractory state of heavy meromyosin and subfragment-1 unable to bind to actin in the presence of ATP.Cold Spring Harbor Symp. Quant. Biol. 37, 145–52.

  23. Fajer, P. J., Fajer, E. A., Brunsvold, N. J. &Thomas, D. D. (1988) Effects of AMPPNP on the orientation and rotational dynamics of spin-labelled muscle crossbridges.Biophys. J. 53, 513–24.

  24. Fenn, W. O. (1923) A quantitative comparison between the energy liberated and the work performed by the isolated sartorius of the frog.J. Physiol. (Lond.) 58, 175–203.

  25. Flitney, F. W. &Hirst, D. G. (1978) Crossbridge detachment and sarcomere ‘give’ during stretch of active frog's muscle.J. Physiol. (Lond.) 276, 449–65.

  26. Ford, L. E., Huxley, A. F. & Simmons, R. M. (1974) Mechanism of early tension recovery after a quick release in tetanized muscle fibres.J. Physiol. (Lond.) 240, 42P.

  27. Ford, L. E., Huxley, A. F. &Simmons, R. M. (1977) Tension responses to sudden length change in stimulated frog muscle fibres near slack length.J. Physiol. (Lond.) 269, 441–515.

  28. Ford, L. E., Huxley, A. F. &Simmons, R. M. (1985) Tension transients during steady shortening of frog muscle fibres.J. Physiol. (Lond.) 361, 131–50.

  29. Ford, L. E., Huxley, A. F. &Simmons, R. M. (1986) Tension transients during the rise of tetanic tension in frog muscle fibres.J. Physiol. (Lond.) 372, 595–609.

  30. Geeves, M. A. (1991) The dynamics of actin and myosin association and the crossbridge model of muscle contraction.Biochem. J. 274, 1–14.

  31. Geeves, M. A., Goody, R. S. &Gutfreund, H. (1984) Kinetics of acto-S1 interaction as a guide to a model for the cross-bridge cycle.J. Muscle Res. Cell Motil. 5, 351–61.

  32. Griffiths, P. J., Güth, K., Kuhn, H. J. &Rüegg, J. C. (1980) Crossbridge slippage in skinned frog muscle fibres.Biophys. Struct. Mech,7, 107–24.

  33. Hanson, J. &Huxley, H. E. (1955) The structural basis of contraction in striated muscle.Symp. Soc. Exp. Biol. 9, 228–58.

  34. Harada, Y. &Yanagida, T. (1988) Direct observation of molecular motility by light microscopy.Cell Motil. Cytoskel. 10, 71–6.

  35. Harada, Y., Sakurada, K., Aoki, T., Thomas, D. D. &Yanagida, T. (1990) Mechanochemical coupling in actomyosin energy transduction studied byin vitro movement assay.J. Mol. Biol. 216, 49–68.

  36. Haselgrove, J. C. &Huxley, H. E. (1973) X-ray evidence for radial crossbridge movement and for the sliding filament model in actively contracting skeletal muscle.J. Mol. Biol. 77, 549–68.

  37. Hasselbach, W. (1978) The reversibility of the sarcoplasmic calcium pump.Biochim. Biophys. Acta 515, 23–53.

  38. Higuchi, H. &Goldman, Y. (1991) Sliding distance between actin and myosin filaments per ATP molecule hydrolysed in skinned muscle fibres.Nature 352, 352–4.

  39. Hill, A. V. (1938) The heat of shortening and the dynamic constants of muscle.Proc. R. Soc. Lond. B. 126, 136–95.

  40. Hill, A. V. (1964) The effect of load on the heat of shortening of muscle.Proc. R. Soc. Lond. B. 159, 518–45.

  41. Hill, T. L. (1973) Theory of muscular contraction extended to groups of actin sites.Proc. Natl. Acad. Sci. USA 70, 2732–6.

  42. Hill, T. L. (1975) Theoretical formalism for the sliding filament model of contraction of striated muscle. Part II.Prog. Biophys. Mol. Biol. 29, 105–59.

  43. Homsher, E. (1987) Muscle enthalpy production and its relationship to actomyosin ATPase.Ann. Rev. Physiol. 49, 673–90.

  44. Homsher, E. &Yamada, T. (1988) The effect of shortening velocity on the shortening heat and its relationship to the distance shortened. InMolecular Mechanism of Muscle Contraction (edited bySugi, H. &Pollack, G.) pp. 689–97. New York: Plenum Press.

  45. Homsher, E., Irving, M. &Wallner, A. (1981) High-energy phosphate metabolism and energy liberation associated with rapid shortening in frog skeletal muscle.J. Physiol. (Lond.) 321, 423–36.

  46. Homsher, E., Irving, M. &Yamada, T. (1984) The effect of shortening on energy liberation and high energy phosphate hydrolysis in frog skeletal muscle. InContractile Mechanisms in Muscle (edited byPollack, G. &Sugi, H.).Adv. Exptl. Med. Biol. 170, 865–76.

  47. Huxley, A. F. (1957) Molecular structure and theories of contraction.Prog. Biophys. Biophys. Chem. 7, 255–318.

  48. Huxley, A. F. (1971) The activation of striated muscle and its mechanical response (The Croonian Lecture, 1967).Proc. R. Soc. Lond. B. 178, 1–27.

  49. Huxley, A. F. (1973) A note suggesting that the crossbridge attachment during muscle contraction may take place in two stages.Proc. R. Soc. Lond. B. 183, 83–6.

  50. Huxley, A. F. &Simmons, R. M. (1971) Proposed mechanism of force generation in striated muscle.Nature 233, 533–8.

  51. Huxley, H. E. (1964) Structural arrangements and the contraction mechanism in striated muscle.Proc. R. Soc. B. 160, 442–8.

  52. Huxley, H. E. (1969) The mechanism of muscular contraction.Science 164, 1356–66.

  53. Huxley, H. E. (1979) Time resolved X-ray diffraction studies on muscle. InCross-Bridge Mechanism in Muscle Contraction (edited bySugi, H. &Pollack, G.) pp. 391–401. Baltimore: University Park Press.

  54. Huxley, H. E. (1990) Sliding filaments and molecular motile systems.J. Biol. Chem. 265, 8347–50.

  55. Huxley, H. E. &Kress, M. (1985) Crossbridge behaviour during muscle contraction.J. Muscle Res. Cell Motil. 6, 153–61.

  56. Huxley, H. E., Simmons, R. M., Faruqi, A. R., Kress, M., Bordas, J. &Koch, M. H. J. (1983) Changes in the X-ray reflections from contracting muscle during rapid mechanical transients and their structural implications.J. Mol. Biol. 169, 469–506.

  57. Huxley, H. E., Kress, M., Faruqi, A. R. &Simmons, R. M. (1988) X-ray diffraction studies on muscle during rapid shortening and their implications concerning crossbridge behaviour. InMolecular Mechanism of Muscle Contraction (edited bySugi, H. &Pollack, G.) pp. 347–352. New York: Plenum Press.

  58. Huxley, H. E., Simmons, R. M. &Faruqi, A. R. (1989) Timecourse of spacing change of 143 Å meridional crossbridge reflection during rapid shortening.Biophys. J. 55, 12a.

  59. Irving, M. (1991) Biomechanics goes quantum.Nature 352, 284–6.

  60. Irving, M. &Woledge, R. C. (1981) The dependence on extent of shortening of the extra energy liberated by rapidly shortening frog skeletal muscle.J. Physiol. (Lond.) 321, 411–22.

  61. Irving, M., Lombardi, V., Piazzesi, G. &Ferenczi, M. A. (1992) Myosin head movements are synchronous with the elementary force-generating process in muscle.Nature 357, 156–8.

  62. Uno, M. &Simmons, R. M. (1982) Tension responses to double step length changes in frog skinned muscle fibres.J. Physiol. (Lond.) 332, 55P.

  63. Ishijima, A., Doi, T., Sakurada, K. &Yanagida, T. (1991) Sub-piconewton force fluctuations of actomyosinin vitro.Nature 352, 301–6.

  64. Julian, F. F. &Sollins, M. R. (1975) Variation of muscle stiffness with force at increasing speeds of shortening.J. Gen. Physiol. 66, 287–302.

  65. Kishino, A. &Yanagida, T. (1988) Force measurements by micromanipulation of a single actin filament by glass needles.Nature 334, 74–6.

  66. Kodama, T. &Yamada, K. (1979) An explanation of the shortening heat based on the enthalpy profile of the myosin ATPase reaction. InCross-bridge Mechanism in Muscle Contraction (edited bySugi, H. &Pollack, G.) pp. 481–488. Baltimore: University Press Park.

  67. Kron, S. J. &Spudich, J. A. (1986) Fluorescent actin filaments move on myosin fixed to a glass surface.Proc. Natl. Acad. Sci. USA 83, 6272–6.

  68. Kushmerick, M. J. &Davies, R. E. (1969) The chemical energetics of muscle contraction. II. The chemistry, efficiency, and power of maximally working sartorius muscle.Proc. R. Soc. 174, 315–50.

  69. Lombardi, V. &Piazzesi, G. (1990) The contractile response during steady lengthening of stimulated frog muscle fibres.J. Physiol. (Lond) 431, 141–71.

  70. Lombardi, V., Piazzesi, G. &Linari, M. (1992) Rapid regeneration of the actin—myosin power stroke in contracting muscle.Nature 355, 638–41.

  71. Lowy, J. &Poulsen, F. R. (1990) Studies of the diffuse X-ray scattering from contracting frog skeletal muscles.Biophys. J. 57, 977–85.

  72. Matsubara, I. &Yagi, N. (1978) A time-resolved X-ray diffraction study of muscle during twitch.J. Physiol. (Lond.) 278, 297–307.

  73. Matsubara, I. &Yagi, N. (1985) Movements of crossbridges during and after slow length changes in active frog skeletal muscle.J. Physiol. (Lond.) 361, 151–63.

  74. Matsubara, I., Yagi, N. &Hashizume, H. (1975) Use of an X-ray television for diffraction of the frog striated muscle.Nature 255, 728–9.

  75. Mitsui, T. &Ohshima, H. (1988) A self-induced translation model of myosin head motion in contracting muscle. I. Force—velocity relation and energy liberationJ. Muscle Res. Cell Motil. 9, 248–60.

  76. Ohno, T. &Kodama, T. (1991) Kinetics of adenosine triphosphate hydrolysis by shortening myofibrils from rabbit psoas muscle.J. Physiol. 441, 685–702.

  77. Oiwa, K., Chaen, S. &Sugi, H. (1991) Measurement of work done by ATP-induced sliding between rabbit muscle myosin and algal cell actin cablesin vitro.J. Physiol. (Lond.) 437, 751–63.

  78. Oosawa, H. &Hayashi, S. (1986) The loose-coupling mechanism in molecular machines of living cells.Adv. Biophys. 22, 151–83.

  79. Padrón, R., Alamo, L., Craig, R. &Caputo, C. (1988) A method for quick-freezing live muscles at known instants during contraction with simultaneous recording of mechanical tension.J. Micros. 151, 81–102.

  80. Pate, E. &Cooke, R. (1991) Simulation of stochastic processes in motile crossbridge systems.J. Muscle Res. Cell Motil. 12, 376–93.

  81. Podolsky, R. J. &Nolan, A. C. (1971) Crossbridge properties derived from physiological studies of frog muscle fibers. InContractility of Muscle Cells and Related Processes (edited byPodolsky, R. J.) pp. 247–60. New Jersey: Prentice-Hall.

  82. Podolsky, R. J. &Nolan, A. C. (1973) Muscle contraction transients, crossbridge kinetics, and the Fenn effect.Cold Spring Harbor Symp. Quant. Biol. 37, 661–8.

  83. Rall, J. A., Homsher, E., Wallner, A. &Mommaerts, W. F. H. M. (1976) A temporal dissociation of energy liberation and high energy phosphate splitting during shortening in frog skeletal muscle.J. Gen. Physiol. 68, 13–27.

  84. Schoenberg, M. (1985) Equilibrium muscle crossbridge behavior. Theoretical considerations.Biophys. J. 48, 467–75.

  85. Sellers, J. R. &Homsher, E. (1991) A giant step for myosin.Current Biology 1, 347–9.

  86. Sellers, J. R. &Kachar, B. (1990) Polarity and velocity of sliding filaments: control of direction by actin and of speed by myosin.Science 249, 406–8.

  87. Simmons, R. M. (1992) Structural changes accompanying mechanical events in muscle contraction. InMuscular Contraction (edited bySimmons, R. M.). Cambridge: Cambridge University Press.

  88. Simmons, R. M. &Jewell, B. R. (1974) Mechanics and models of muscular contraction. InRecent Advances in Physiology, No. 9 (edited byLinden, R. J.) pp. 87–145. Edinburgh: Churchill Livingstone.

  89. Sugi, H. &Tsuchiya, T. (1981) Isotonic velocity transients in frog muscle fibres following quick changes in load.J. Physiol. 319, 219–38.

  90. Sugi, H. &Tsuchiya, T. (1988) Stiffness changes during enhancement and deficit of isometric force by slow length changes in frog skeletal muscle fibres.J. Physiol. 407, 215–29.

  91. Tawada, K. &Sekimoto, K. (1991) A physical model of ATP-induced actin-myosin movementin vitro.Biophys. J. 59, 343–56.

  92. Taylor, E. W. (1989) Actomyosin ATPase mechanism and muscle contraction. InMuscle Energetics. pp. 9–14. New York: Alan R. Liss.

  93. Taylor, E. W. (1991) Kinetic studies on the association and dissociation of myosin subfragment 1 and actin.J. Biol. Chem. 266, 294–302.

  94. Trinick, J. &Elliott, A. (1982) Effect of substrate on freeze-dried and shadowed protein structures.J. Micros. 126, 151–6.

  95. Toyoshima, Y. Y., Toyoshima, C. &Spudich, J. A. (1989) Bidirectional movement of actin filaments along tracks of myosin heads.Nature 341, 154–6.

  96. Toyoshima, Y. Y., Kron, S. J. &Spudich, J. A. (1990) The myosin step size: measurement of the unit displacement per ATP hydrolyzed in anin vitro assay.Proc. Natl. Acad. Sci. USA 87, 7130–4.

  97. Tsuchiya, T., Güth, K., Kuhn, H. J. &Rüegg, C. (1982) Decrease in stiffness during shortening in calcium activated skinned muscle fibres.Pflügers Archiv 392, 322–6.

  98. Tsukita, S. &Yano, M. (1985) Actomyosin structure in contracting muscle detected by rapid freezing.Nature 317, 182–4.

  99. Uyeda, T. Q. P., Kron, S. J. &Spudich, J. A. (1990) Myosin step size estimation from slow sliding movement of actin over low densities of heavy meromyosin.J. Mol. Biol. 214, 699–710.

  100. Uyeda, T. Q. P., Warrick, H. M., Kron, S. J. &Spudich, J. A. (1991) Quantized velocities at low myosin densities in anin vitro motility assay.Nature 352, 307–11.

  101. Vale, R. D. &Oosawa, F. (1990) Protein motors and Maxwell's demons: does mechanochemical transduction involve a thermal ratchet?Adv. Biophys. 26, 97–134.

  102. Vale, R. D., Soll, D. R. &Gibbons, I. R. (1989) One-dimensional diffusion of microtubules bound to flagellar dynein.Cell 59, 915–25.

  103. Walzthöny, D., Eppenberger, H. M., Ueno, H., Harrington, W. F. &Wallimann, T. (1986) Melting of myosin rod as revealed by electron microscopy. II. Effects of temperature and pH on length and stability of myosin rod and its fragments.Eur. J. Cell Biol. 41, 38–43.

  104. White, H., Belknap, B. &Wei, J. (1992) Kinetics of binding and hydrolysis of the nucleoside triphosphates ATP, CTP 1-N6 Etheno-2-aza ATP, and GTP by rabbit skeletal actomyosin-S1: Measurement of the average distance that the crossbridge remains attached during unloaded shortening.Biophys. J. 61, A140.

  105. Woledge, R. C., Curtin, N. A. &Homsher, E. (1985)Energetic Aspects of Muscle Contraction. (Monographs of the Physiological Society, No. 41) London: Academic Press.

  106. Woledge, R. C., Wilson, M. G. A., Howarth, J. V., Elzinga, G. &Kometani, K. (1988) The energetics of work and heat production by single muscle fibres from the frog. InMolecular Mechanism of Muscle Contraction (edited bySugi, H. &Pollack, G.) pp. 677–687. New York: Plenum Press.

  107. Yanagida, T., Arata, T. &Oosawa, F. (1985) Sliding distance of actin filament induced by a myosin crossbridge during one ATP hydrolysis cycle.Nature 316, 366–9.

  108. Yanagida, T., Harada, Y. &Kodama, T. (1991) Chemomechanical coupling in actomyosin system: An approach byin vitro movement assay and kinetic analysis of ATP hydrolysis by shortening myofibrils.Adv. Biophys. 27, 237–57.

Download references

Author information

Correspondence to Kevin Burton.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Burton, K. Myosin step size: Estimates from motility assays and shortening muscle. J Muscle Res Cell Motil 13, 590–607 (1992). https://doi.org/10.1007/BF01738249

Download citation

Keywords

  • Motility Assay
  • Myosin Step
  • Myosin Step Size