A 35-Å movement of smooth muscle myosin on ADP release (original) (raw)

Nature volume 378, pages 748–751 (1995)Cite this article

Abstract

MYOSIN II crossbridges interact with F-actin producing power-strokes of around 100 Å (refs 1, 2), during which the products of ATP hydrolysis are released3–5. This has been postulated to involve an articulation of the myosin head (S1) on actin, or substantial conformational changes in S1 itself6–8. Small movements of the regulatory light chain have been detected (see, for example, refs 9, 10), but most data suggest that the bulk of S1 does not move on actin during crossbridge cycling8,11. Here we present three-dimensional maps of S1-decorated F-actin in the presence and absence of MgADP. The myosin motor domain is similar in both states but there are major orientational differences in the light-chain-binding domain. This domain acts as a rigid level arm12,13 pivoting about the end of the motor domain and swinging ∼23°, resulting in a ∼35-Å step. Small, nucleotide-mediated conformational changes in the motor domain14–16may thus be converted by the light-chain domain into large movement steps.

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References

  1. Huxley, A. F. & Simmons, R. M. Nature 233, 533–538 (1971).
    Article ADS CAS PubMed Google Scholar
  2. Finer, J. T., Simmons, R. M. & Spudich, J. A. Nature 368, 113–119 (1994).
    Article ADS CAS PubMed Google Scholar
  3. Goldman, Y. E. A. Rev. Physiol. 49, 637–654 (1987).
    Article CAS Google Scholar
  4. Brenner, B. A. Rev. Physiol. 49, 655–672 (1987).
    Article ADS CAS Google Scholar
  5. Geeves, M. A. Biochem. J. 274, 1–14 (1991).
    Article CAS PubMed PubMed Central Google Scholar
  6. Reedy, M. K., Holmes, K. C. & Tregear, R. T. Nature 207, 1276–1280 (1965).
    Article ADS CAS PubMed Google Scholar
  7. Huxley, H. E. Science 164, 1356–1366 (1969).
    Article ADS CAS PubMed Google Scholar
  8. Huxley, H. E. & Kress, M. J. J. Muscle Res. Cell Motil. 6, 153–161 (1985).
    Article CAS PubMed Google Scholar
  9. Hambly, B., Franks, K. & Cooke, R. Biophys. J. 63, 1306–1313 (1992).
    Article ADS CAS PubMed PubMed Central Google Scholar
  10. Irving, M. et al. Nature 375, 688–691 (1995).
    Article ADS CAS PubMed Google Scholar
  11. Thomas, D. D. A. Rev. Physiol. 49, 691–709 (1987).
    Article CAS Google Scholar
  12. Rayment, I. et al. Science 261, 50–58 (1993).
    Article ADS CAS PubMed Google Scholar
  13. Rayment, I. et al. Science 261, 58–65 (1993).
    Article ADS CAS PubMed Google Scholar
  14. Fisher, A. J. et al. Biophys. J. 68, 19s–28s (1995).
    CAS PubMed PubMed Central Google Scholar
  15. Fisher, A. J. et al. Biochemistry 34, 8960–8972 (1995).
    Article CAS PubMed Google Scholar
  16. Smith, C. A. & Rayment, I. Biochemistry 34, 8973–8981 (1995).
    Article CAS PubMed Google Scholar
  17. Dantzig, J. A., Hibberd, M. G., Trentham, D. R. & Goldman, Y. E. J. Physiol., Lond. 432, 639–680 (1991).
    Article CAS PubMed PubMed Central Google Scholar
  18. Nishiye, E., Somlyo, A. V., Török, K. & Somlyo, A. P. J. Physiol., Lond. 460, 247–271 (1993).
    Article CAS PubMed PubMed Central Google Scholar
  19. Dantzig, J. A. & Goldman, Y. E. J. gen. Physiol. 86, 305–327 (1985).
    Article CAS PubMed Google Scholar
  20. Milligan, R. A. & Flicker, P. F. J. Cell Biol. 105, 29–39 (1987).
    Article CAS PubMed Google Scholar
  21. Milligan, R. A., Whittaker, M. & Safer, D. Nature 348, 217–221 (1990).
    Article ADS CAS PubMed Google Scholar
  22. Whittaker, M., Carragher, B. O. & Milligan, R. A. Ultramicroscopy 58, 245–260 (1995).
    Article CAS PubMed Google Scholar
  23. Sweeney, H. L. et al. Biophys. J. (meeting abstract) (in the press).
  24. Milligan, R. A. Proc. natn. Acad. Sci. U.S.A. (in the press).
  25. Helper, D. J., Lash, J. A. & Hathaway, D. R. J. biol. Chem. 263, 15748–15753 (1988).
    CAS PubMed Google Scholar
  26. Rayment, I., Holden, H. M., Sellers, J. R., Fananapazir, L. & Epstein, N. D. Proc. natn. Acad. Sci. U.S.A. 92, 3864–3868 (1995).
    Article ADS CAS Google Scholar
  27. Spudich, J. A. & Watt, S. J. biol. Chem. 246, 4866–4871 (1971).
    CAS PubMed Google Scholar
  28. Sweeney, H. L., Straceski, A., Leinwand, L., Tikunov, B. & Faust, L. J. biol. Chem. 269, 1603–1605 (1994).
    CAS PubMed Google Scholar
  29. Hopp, T. P. et al. Biotechnology 6, 1205–1210 (1988).
    Google Scholar
  30. Hessler, D. et al. Microscopy 22, 73–82 (1992).
    Google Scholar
  31. Jones, T. A., Zou, J. Y., Cowan, S. & Kjeldgaard, M. Acta. crystallogr. A47, 110–119 (1991).
    Article Google Scholar
  32. Kraulis, P. J. J. appl. Cryst. 24, 946–950 (1991).
    Article Google Scholar

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Authors and Affiliations

  1. Department of Cell Biology, The Scripps Research Institute, 10666 North Torrey Pines Road, La Jolla, California, 92037, USA
    Michael Whittaker & Elizabeth M. Wilson-Kubalek
  2. Department of Physiology, University of Pennsylvania School of Medicine, 37th Street & Hamilton Walk, Philadelphia, Pennsylvania, 19104, USA
    Joseph E. Smith, Lynn Faust & H. Lee Sweeney

Authors

  1. Michael Whittaker
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  2. Elizabeth M. Wilson-Kubalek
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  3. Joseph E. Smith
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  4. Lynn Faust
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  5. Ronald A. Milligan
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  6. H. Lee Sweeney
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Whittaker, M., Wilson-Kubalek, E., Smith, J. et al. A 35-Å movement of smooth muscle myosin on ADP release.Nature 378, 748–751 (1995). https://doi.org/10.1038/378748a0

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