Three-Dimensional Structural Analysis of Individual Myosin Heads Under Various Functional States

  • Eisaku Katayama
  • Norihiko Ichise
  • Naoki Yaeguchi
  • Tsuyoshi Yoshizawa
  • Shinsaku Maruta
  • Norio Baba
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 538)

Abstract

Half a century has passed since the dedicated studies on the contraction mechanisms of muscle began, with considerable knowledge on its molecular architecture. Two major hypotheses were raised very early, one, ”sliding filament theory”,1,2 and the other, “crossbridge theory”. 3 The former was readily accepted, because the phenomenon was apparently visible under optical microscope. The latter, however, has been hindered from thorough experimental proof even now, though nothing other than crossbridges connect thick and thin filaments enabling force development. The original idea postulated the rowing movement of actin-bound myosin head coupled with ATP hydrolysis, but it was later replaced by swinging of the “lever-arm” moiety,4 according to the discovery of intramolecular bending by X-ray crystallography.5-8 One of the major reasons for such persistent difficulty to prove this simple hypothesis might be the lack of means to directly observe the actual structural change of working crossbridges with time and spatial resolution enough to visualize the fine details of the molecular nano-machine. Though the crystal structure of each component; actin9, 10 and myosin subfragment-1 (S1) with or without various nucleotides,5-8 was determined ten years ago, none of their complexed form was solved nor might be the subject matter for easy crystallization.

Keywords

Hydrolysis Crystallization Fluoride Glycine Cystein 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    A.F. Huxley, and R. Niedergerke, Structural changes in muscle during contraction. Interference microscopy of living muscle fibres, Nature, 173, 971–973 (1954).PubMedCrossRefGoogle Scholar
  2. 2.
    H.E. Huxley, and J. Hanson, Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation, Nature, 173, 973–976 (1954)PubMedCrossRefGoogle Scholar
  3. 3.
    A.F. Huxley, and R.M. Simmons, Proposed mechanism of force generation in striated muscle, Nature, 233, 533–538 (1971).PubMedCrossRefGoogle Scholar
  4. 4.
    R.D. Vale, and R.D. Milligan, The way things move: looking under the hood of molecular motors, Science, 288, 88–95 (2000).PubMedCrossRefGoogle Scholar
  5. 5.
    I. Rayment, W.R. Rypniewski, K. Schmidt-Bäse, R. Smith, D.R. Tomchick, M.M. Benning, D.A. Winkelman, G. Wesenberg, and H.M. Holden, Three-dimensional structure of myosin subfragment-1: A molecular motor, Science, 261, 50–58 (1993).PubMedCrossRefGoogle Scholar
  6. 6.
    A.J. Fisher, C.A. Smith, J. Thoden, R. Smith, K. Sutoh, H.M. Holden, and I. Rayment, X-ray structures of the myosin motor domain of dictyostelium discoideum complexed with MgADP. BeFx and MgADP. A1F4; Biochemistry, 34, 8960–8972 (1995).CrossRefGoogle Scholar
  7. 7.
    R. Dominguez, Y. Freyzon, K.M. Trybus, and C. Cohen, Crystal structure of vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: Visualizatioin of the pre-power stroke state, Cell, 94, 559–571 (1998).PubMedCrossRefGoogle Scholar
  8. 8.
    A. Houdusse, A.G. Szent-Gyorgyi, and C. Cohen, Three conformational states of scallop myosin S1, Proc. Natl. Acad. Sci.USA, 97, 11238–11243 (2000).PubMedCrossRefGoogle Scholar
  9. 9.
    W. Kabsch, H.G. Mannherz, D. Suck, E.F. Pai and K.C. Holmes, Atomic structure of the actin: DNase I complex, Nature, 347, 37–44 (1990).PubMedCrossRefGoogle Scholar
  10. 10.
    K.C. Holmes, D. Popp W. Gebhard, and W. Kabsch, Atomic model of the actin filament, Nature, 347, 44–49 (1990).PubMedCrossRefGoogle Scholar
  11. 11.
    J. Kron, and J.A. Spudich, Fluorescent actin filaments move on myosin fixed to a glass surface, Proc. Natl. Acad. Sci. USA, 83, 6272–6276 (1986).PubMedCrossRefGoogle Scholar
  12. 12.
    Y. Harada, A. Noguchi, A. Kishino, and T. Yanagida, Sliding movement of single actin filaments on one-headed myosin filaments, Nature, 326, 805–808 (1987).PubMedCrossRefGoogle Scholar
  13. 13.
    J.E. Heuser, Procedure for freeze-drying molecules adsorbed to mica flakes, J. Mol. Biol, 169, 155–195 (1983).PubMedCrossRefGoogle Scholar
  14. 14.
    E. Katayama, Quick-freeze deep-etch electron microscopy of the actin-heavy meromyosin complex during the in vitro motility assay, J. Mol. Biol., 278(2), 349–367 (1998).PubMedCrossRefGoogle Scholar
  15. 15.
    E. Katayama, G. Ohmori and N. Baba, Three-dimensional image analysis of myosin head in function as captured by quick-freeze deep-etch replica electron microscopy, Adv. Exp. Med. Biol., 453, 37–45 (1998)PubMedCrossRefGoogle Scholar
  16. 16.
    E. Katayama, T. Shiraishi, K. Oosawa, N. Baba and S. Aizawa, Geometry of the flagellar motor in the cytoplasmic membrane of Salmonella Typhimurium as determined by stereo-photogrammetry of quick-freeze deep-etch replica images, J. Mol. Biol., 255, 458–475 (1996).PubMedCrossRefGoogle Scholar
  17. 17.
    S. Maruta, G.D. Henry, B.D. Sykes and M. Ikebe, Formation of the stable myosin-ADP-aluminium fluoride and myosin-ADP-beryllium fluoride complexes and their analysis using 19F-NMR, J. Biol. Chem., 268, 7093–7100 (1993).PubMedGoogle Scholar
  18. 18.
    S. Maruta, Y. Uyehara, K. Homma, Y. Sugimoto and K. Wakabayashi, Formation of the myosin-ADP-gallium fluoride complex and its solution structure by small-angle synchrotron X-ray scattering, J. Biochem., 125, 177–185 (1999).PubMedCrossRefGoogle Scholar
  19. 19.
    S. Maruta, T. Aihara, Y. Uyehara, K. Homma, Y. Sugimoto, and K. Wakabayashi, Solution structure of myosin-ADP-MgFn ternary complex by fluorescent probes and small-angle synchrotron X-ray scattering, J. Biochem., 128, 677–684 (2000).CrossRefGoogle Scholar
  20. 20.
    E. Reisler, M. Burke, S. Himmelfarb, and WJF. Harrington, Spatial proximity of the two essential sulfhydryl groups of myosin, Biochemistry, 13, 3837–3840 (1974).PubMedCrossRefGoogle Scholar
  21. 21.
    J.A. Wells and R.G. Yount, Chemical modification of myosin by active-site trapping of metal-nucleotides with thiol crosslinking reagents, Methods. Enzymol., 85, 93–116 (1982).PubMedCrossRefGoogle Scholar
  22. 22.
    D.M. Himmel, S. Gourinath, L. Reshetnikova, Y. Shen, A.G, Szent-Gyorgyi, and C. Cohen, Crystallographic findings on the internally uncoupled and near-rigor states of myosin: further insights into the mechanics of the motor, Proc. Natl. Acad. Sci. USA, 99, 12645–12650 (2002).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2003

Authors and Affiliations

  • Eisaku Katayama
    • 1
  • Norihiko Ichise
    • 1
  • Naoki Yaeguchi
    • 2
  • Tsuyoshi Yoshizawa
    • 3
  • Shinsaku Maruta
    • 3
  • Norio Baba
    • 2
  1. 1.Division of Biomolecular Imaging, Institute of Medical ScienceThe University of TokyoMinato-ku, TokyoJapan
  2. 2.Department of Electric EngineeringKogakuin UniversityHachioji, TokyoJapan
  3. 3.Department of Bioengineering, Faculty of EngineeringSoka UniversityHachioji, TokyoJapan

Personalised recommendations