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Myosin head movements are synchronous with the elementary force-generating process in muscle

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An Erratum to this article was published on 25 June 1992

Abstract

MOTOR proteins such as myosin, dynein and kinesin use the free energy of ATP hydrolysis to produce force or motion, but despite recent progress1–4 their molecular mechanism is unknown. The best characterized system is the myosin motor which moves actin filaments in muscle5–12. When an active muscle fibre is rapidly shortened the force first decreases, then partially recovers over the next few milliseconds5. This elementary force-generating process is thought to be due to a structural 'working stroke' in the myosin head domain5–9, although structural studies have not provided definitive support for this10–12. X-ray diffraction has shown that shortening steps produce a large decrease in the intensity of the 14.5 nm reflection arising from the axial repeat of the myosin heads along the filaments13,14. This was interpreted as a structural change at the end of the working stroke, but the techniques then available did not allow temporal resolution of the elementary force-generating process itself. Using improved measurement techniques, we show here that myosin heads move by about 10 nm with the same time course as the elementary force-generating process.

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References

  1. Ishijima, A., Doi, T., Sakurada, K. & Yanagida, T. Nature 352, 301–306 (1991).

    Article  ADS  CAS  Google Scholar 

  2. Uyeda, T. Q. P., Warrick, H. M., Kron, S. J. & Spudich, J. A. Nature 352, 307–311 (1991).

    Article  ADS  CAS  Google Scholar 

  3. Schroer, T. A., Steuer, E. R. & Sheetz, M. P. Cell 56, 937–946 (1989).

    Article  CAS  Google Scholar 

  4. Block, S. M., Goldstein, L. S. B. & Schnapp, B. J. Nature 348, 348–352 (1990).

    Article  ADS  CAS  Google Scholar 

  5. Huxley, A. F. & Simmons, R. M. Nature 233, 533–538 (1971).

    Article  ADS  CAS  Google Scholar 

  6. Reedy, M. K., Holmes, K. C. & Tregear, R. T. Nature 207, 1276–1280 (1965).

    Article  ADS  CAS  Google Scholar 

  7. Huxley, H. E. Science 164, 1356–1366 (1969).

    Article  ADS  CAS  Google Scholar 

  8. Lymn, R. W. & Taylor, E. W. Biochemistry 10, 4617–4624 (1971).

    Article  CAS  Google Scholar 

  9. Huxley, A. F. Prog. Biophys. biophys. Chem. 7, 255–318 (1957).

    Article  CAS  Google Scholar 

  10. Cooke, R. CRC Crit. Rev. Biochem. 21, 53–118 (1986).

    Article  CAS  Google Scholar 

  11. Thomas, D. D. A. Rev. Biochem 49, 691–709 (1987).

    CAS  Google Scholar 

  12. Irving, M. in Fibrous Protein Structure (eds Squire, J. M. & Vibert, P. J.) 495–528, (Academic, London, 1987).

    Google Scholar 

  13. Huxley, H. E. et al. J. molec. Biol. 169, 469–506 (1983).

    Article  CAS  Google Scholar 

  14. Huxley, H. E., Faruqi, A. R., Kress, M., Bordas, J. & Koch, M. H. J. J. molec. Biol. 159, 637–684 (1982).

    Article  Google Scholar 

  15. Ford, L. E., Huxley, A. F. & Simmons, R. M. J. Physiol., Lond. 269, 441–515 (1977).

    Article  CAS  Google Scholar 

  16. Ford, L. E., Huxley, A. F. & Simmons, R. M. J. Physiol., Lond. 311, 219–249 (1981).

    Article  CAS  Google Scholar 

  17. Lombardi, V., Piazzesi, G. & Linari, M. Nature 355, 638–641 (1992).

    Article  ADS  CAS  Google Scholar 

  18. Yanagida, T., Arata, T. & Oosawa, F. Nature 316, 366–369 (1985).

    Article  ADS  CAS  Google Scholar 

  19. Harada, Y., Sakurada, K., Aoki, T., Thomas, D. D. & Yanagida, T. J. molec. Biol. 216, 49–68 (1990).

    Article  CAS  Google Scholar 

  20. Uyeda, T. Q. P., Kron, S. J. & Spudich, J. A. J. molec. Biol. 214, 699–710 (1990).

    Article  CAS  Google Scholar 

  21. Huxley, H. E. J. biol. Chem. 265, 8347–8350 (1990).

    CAS  PubMed  Google Scholar 

  22. Irving, M. Nature 352, 284–286 (1991).

    Article  ADS  CAS  Google Scholar 

  23. Kushmerick, M. J. & Davis, R. E. Proc. R. Soc. B174, 315–353 (1969).

    ADS  CAS  Google Scholar 

  24. Lombardi, V. & Piazzesi, G. J. Physiol., Lond. 431, 141–171 (1990).

    Article  CAS  Google Scholar 

  25. Piazzesi, G., Francini, F., Linari, M. & Lombardi, V. J. Physiol., Lond. 445, 659–711 (1992).

    Article  CAS  Google Scholar 

  26. Matsubara, I. & Yagi, N. J. Physiol., Lond. 361, 151–163 (1985).

    Article  CAS  Google Scholar 

  27. Cecchi, G., Colomo, F. & Lombardi, V. Boll. Soc. ital. Biol. Sper. 52, 733–736 (1976).

    CAS  PubMed  Google Scholar 

  28. Huxley, A. F. & Lombardi, V. J. Physiol., Lond. 305, 15–16P (1981).

    Google Scholar 

  29. Huxley, A. F., Lombardi, V. & Peachey, L. D. J. Physiol., Lond. 317, 12–13P (1981).

    Google Scholar 

  30. Towns-Andrews, E. et al. Rev. sci. Instrum. 60, 2346–2349 (1989).

    Article  ADS  CAS  Google Scholar 

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Irving, M., Lombardi, V., Piazzesi, G. et al. Myosin head movements are synchronous with the elementary force-generating process in muscle. Nature 357, 156–158 (1992). https://doi.org/10.1038/357156a0

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