A single myosin head moves along an actin filament with regular steps of 5.3 nanometres

Nature

Volumn 397, Issue 6715, 1999, Pages 129-134

  Kitamura, Kazuo ^a,b,c   Tokunaga, Makio ^a,d   Iwane, Atsuko Hikikoshi ^b,c   Yanagida, Toshio ^a,b,c,e  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e Japan Science and Technology Agency   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; MYOSIN;

ACTIN FILAMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CHICKEN; FLUORESCENCE MICROSCOPY; FORCE; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; RABBIT; X RAY CRYSTALLOGRAPHY;

ACTINS; ACTOMYOSIN; ANIMALS; BIOMECHANICS; CHICKENS; MOLECULAR MOTOR PROTEINS; MOLECULAR PROBE TECHNIQUES; MOTION; MYOSINS; RECOMBINANT FUSION PROTEINS;

EID: 0033552942     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/16403     Document Type: Article

References (50)

1. Kabsch, W., Mannherz, H. G., Suck, D., Pai, E. F. & Holmes, K. C. Atomic stucture of the actin: DNase I complex. Nature 347, 37-44 (1990).
2. Rayment, I. et al. Three-dimensional structure of myosin subfragment-1:a molecular motor. Science 261, 50-58 (1993).
3. Huxley, H. E. The mechanism of muscular contraction. Science 164, 1355-1366 (1969).
4. Huxley, A. F. & Simmons, R. M. Proposed mechanism of force generation in striated muscle. Nature 233, 533-538 (1971).
5. Spudich, J. A. How molecular motors work. Nature 372, 515-518 (1994).
6. Rayment, I. et al. Structure of the actin-myosin complex and its implications for muscle contraction. Science 261, 58-65 (1993).
7. 4. Biochemistry 34, 8960-8972 (1995).
8. Cooke, R. Actomyosin interaction in striated muscle. Physiol. Rev. 77, 671-697 (1997).
9. Howard, J. Molecular motors structural adaptations to cellular functions. Nature 389, 561-567 (1997).
10. Kishino, A. & Yanagida, T. Force measurements by micromanipulation of a single actin filament by glass needles. Nature 334, 74-76 (1988).
11. Finer, J. T., Simmons, R. M. & Spudich, J. A. Single myosin molecule mechanics: picanewton forces and nanometre steps. Nature 368, 113-119 (1994).
12. Ishijima, A., Doi, T., Sakurada, K. & Yanagida, T. Sub-piconewton force fluctuations of actomyosin in vitro. Nature 352, 301-306 (1991).
13. Ishijima, A. et al. Single-molecule analysis of the actomyosin motor using nano-manipulation. Biochem. Biophys. Res. Commun. 199, 1057-1063 (1994).
14. Miyata, H. et al. Stepwise motion of an actin filament over a small number of heavy meromyosin molecules is revealed in an in vitro motility assay. J. Biochem. (Takyo) 115, 644-647 (1994).
15. Molloy, J. E., Burns, J. E., Kendrick-Jones, J., Tregear, R. T. & White, D. C. S. Movement and force produced by a single myosin head Nature 378, 209-212 (1995).
16. Guilford, W. H. et al. Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacement in the laser trap. Biophys. J. 72, 1006-1021 (1997).
17. Mebta, A. D., Finer, J. T. & Spudich, J. A. Detection of single-molecule interaction using correlated thermal diffusion. Proc. Natl Acad. Sci. USA 94, 7927-7931 (1997).
18. Ishijima, A. et al. Multiple-and single-molecule analysis of the actomyosin motor by nanometer-piconewton manipulation with a microneedle: unitary steps and forces. Biophys. J. 70, 383-400 (1996).
19. Ishijima, A. et al. Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin. Cell 92, 161-171 (1998).
20. Tanaka, H., Ishijima, A., Honda, M., Saito, K. & Yanagida, T. Orientation dependence of displacements by a single one-headed myosin relative to the actin filament. Biophys. J. 75, 1886-1894 (1998).
21. Yanagida, T., Arata, T. & Oosawa, F. Sliding distance of actin filament induced by a myosin crossbridge during one ATP hydrolysis cycle. Nature 316, 366-369 (1985).
22. Harado, Y., Sakurada, K., Aoki, T., Thomas, D. D. & Yanagida, T. Mechanochemical coupling in actomyosin energy transduction studied by in vitro movement assay. J. Mol. Biol. 216, 49-68 (1990).
23. Higuchi, H. & Goldman, Y. E. Sliding distance between actin and myosin filaments per ATP molecule hydrolysed in skinned muscle fibres. Nature 352, 352-354 (1991).
24. Lombardi, V., Piazzesi, G. & Linari, M. Rapid regeneration of the actin-myosin power stroke in contracting muscle. Nature 355, 638-641 (1992).
25. Kitano, M., Hamabe, T., Maeda, S. & Okabe, T. Growth of large tetrapod-like ZnO crystals. J. Crystal Growth 102, 965-973 (1990).
26. Kado, H., Yokoyama, K. & Tohda, T. Atomic force microscopy using ZnO whisker tip. Rev. Sci. Inrstrum. 63, 3330-3332 (1992).
27. Tokunaga, M., Kitamura, K., Saito, K., Iwane, A. H. & Yanagida, T. Single molecule imaging of fluorophores and enzymatic reactions achieved by objective-type total internal reflection fluorescence microscopy. Biochem. Biophys. Res. Commun. 235, 47-53 (1997).
28. Funatsa, T., Harada, Y., Tokunaga, M., Saito, K. & Yanagida, T. Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature 374, 555-559 (1995).
29. Huxley, A. F. & Tideswell, S. Filament compliance and tension transients in muscle. J. Muscle Res. Cell Motil. 17, 507-511 (1996).
30. Woledge, R. C., Curtin, N. A. & Homsher, R. Energetic Aspects of Muscle Contraction Ch. 3 (Academic, London, 1985).
31. Svoboda, K., Schmidt, C. F., Schnapp, B. J. & Block, S. M. Direct observation of kinesin stepping by optical trapping interferometry. Nature 365, 721-727 (1993).
32. Harada, Y., Noguchi, A., Kishino, A. & Yanagida, T. Sliding movement of single actin filaments on one-headed myosin filaments. Nature 326, 805-808 (1987).
33. Iwane, A. H., Kitamura, K., Yokunaga, M. & Yanagida, T. Myosin subfragment-1 is fully equipped with factors essential for motor function. Biochem. Biophys. Res. Commun. 230, 76-80 (1997).
34. Bagshaw, C. R. Muscle Contraction (Chapman & Hall, London, 1993).
35. Kojima, H., Muto, E., Higuchi, H. & Yanagida, T. Mechanics of single kinesin molecules measured by optical trapping nanometry. Biophys. J. 73, 2012-2022 (1997).
36. Schnitzer, M. J. & Block, S. M. Kinesin hydrolyses one ATP per 8-nm step. Nature 388, 386-390 (1997).
37. c steps. Cell 93, 1117-1124 (1998).
38. Huxley, H. E. & Brown, W. The low-angle x-ray diagram of vertebrate striated muscle and its behavior during contraction and rigor. J. Mol. Biol. 30, 383-434 (1967).
39. Astumian, R. D. Thermodynamics and kinetics of a brownian motor. Science 276, 917-922 (1997).
40. Egelman, E. H., Francis, N. & DeRosier, D. J. F-actin is a helix with a random variable twist. Nature 298, 131-135 (1982).
41. Yanagida, T., Nakase, M., Nishiyama, K. & Oosawa, F. Direct observation of motion of single F-actin filaments in the presence of myosin. Nature 307, 58-60 (1984).
42. Lymn, R. W. & Taylor, E. W. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10, 4617-4624 (1971).
43. Klibanov, A. M. Enzyme memory. What is remembered and why? Nature 374, 596 (1995).
44. Margossian, S. S. & Lowey, S. Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol. 85, 55-71 (1982).
45. Spudich, J. A. & Watt, S. The regulation of rabbit skeletal muscle contraction. 1. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246, 4866-4871 (1971).
46. Craig, S. W., Lancashire, C. L. & Cooper, J. A. Preparation of smooth muscle α-actinin. Methods Enzymol. 85, 316-321 (1982).
47. Tokunaga, M., Aoki, T., Hiroshima, M., Kitamura, K. & Yanagida, T. Subpiconewton intermolecular force microscopy. Biochem. Biophys. Res. Commun. 231, 566-569 (1997).
48. Saito, K., Tokunaga, M., Iwane, A. H. & Yanagida, T. Dual color microscopy of single fluorophores bound to myosin interacting with fluorescently-labelled actin using anti-Stokes fluorescence, J. Microsc. 188, 255-263 (1997).
49. Bevington, P. R. & Robinson, D. K. Data Reduction and Error Analysis for the Physical Sciences (McGraw-Hill, New York, 1992).
50. Wand, M. P. & Jones, M. C. Kernel Smoothing (Chapman & Hall, London, 1995).