Abstract
MUSCLE contraction is generally thought to be driven by tilting1, 2 of the 19-nm-long myosin head3, part of the thick filament, while attached to actin, part of the thin filament. This motion would produce about 12 nm of filament sliding4, 5. Recent estimates of the sliding distance per ATP molecule hydrolysed by actomyosin in vitro vary widely from 8 nm (ref. 6) to >=200 nm (ref. 7). The latter value is incompatible with a power stroke incorporating a single tilting motion of the head. We have measured the isotonic sliding distance per ATP molecule hydrolysed during the interaction between myosin and actin in skinned muscle fibres. We directly estimated the proportion of simultaneously attached actomyosin complexes and their ATP use. We report here that at low loads the interaction distance is at least 40 nm. This distance corresponds to the length of the power stroke plus the filament sliding while actomyosin crossbridges bear negative drag forces5, 8. If the power stroke is 12 nm, then our results indicate the drag distance to be at least 28 nm. Our results could also be explained by multiple power strokes per ATP molecule hydrolysed.
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References
Reedy, M. K., Holmes, K. C. & Tregear, R. T. Nature 207, 1276–1280 (1965).
Huxley, H. E. Science 164, 1356–1366 (1969).
Elliott, A. & Offer, G. J. molec. Biol. 123, 505–519 (1978).
Huxley, A. F. & Simmons, R. M. Nature 233, 533–538 (1971).
Ford, L. E., Huxley, A. F. & Simmons, R. M. J. Physiol. 269, 441–515 (1977).
Toyoshima, Y. Y., Kron, S. J. & Spudich, J. A. Proc. natn. Acad. Sci. U.S.A. 87, 7130–7134 (1990).
Harada, Y., Sakurada, K., Aoki, T., Thomas, D. D. & Yanagida, T. J. molec. Biol. 216, 49–68 (1990).
Huxley, A. F. Prog. Biophys. biophys. Chem. 7, 255–318 (1957).
Yanagida, T., Arata, T. & Oosawa, F. Nature 316, 366–369 (1985).
Uyeda, T. Q. P., Kron, S. J. & Spudich, J. A. J. molec. Biol. 214, 699–710 (1990).
Huxley, A. F. & Simmons, R. M. Cold Spring Harb. Symp. quant. Biol. 37, 669–680 (1973).
Ferenczi, M. A., Homsher, E. & Trentham, D. R. J. Physiol. 352, 575–599 (1984).
Cecchi, G., Colomo, F. & Lombardi, V. Boll. Soc. ital. biol. Sper. 52, 733–736 (1976).
Goldman, Y. E., Hibberd, M. G. & Trentham, D. R. J. Physiol. 354, 577–604: 605–624 (1984).
Goldman, Y. E. Biophys. J. 52, 57–68 (1987).
Tawada, K. & Kimura, M. Biophys. J. 45, 593–602 (1984).
Vale, R. D. & Oosawa, F. Adv. Biophys. 26, 97–134 (1990).
Lombardi, V. & Piazzesi, G. J. Physiol. 431, 141–171 (1990).
Ishijima, A., Doi, T., Sakurada, K. & Yanagida, T. Nature 352, 301–306 (1991).
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Higuchi, H., Goldman, Y. Sliding distance between actin and myosin filaments per ATP molecule hydrolysed in skinned muscle fibres. Nature 352, 352–354 (1991). https://doi.org/10.1038/352352a0
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DOI: https://doi.org/10.1038/352352a0
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