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Quantal Motor Action in Muscle Contraction

Published online by Cambridge University Press:  15 February 2011

G. H. Pollack
Affiliation:
Dept. of Bioengineering, Box 35-7962, University of Washington, Seattle WA 98195
F. Blyakhman
Affiliation:
Current address: Dept. of Physics, Ural State Univ. Ekaterinburg, Russia
T. Shklyar
Affiliation:
Current address: Dept. of Physics, Ural State Univ. Ekaterinburg, Russia
A. Tourovskaia
Affiliation:
Dept. of Bioengineering, Box 35-7962, University of Washington, Seattle WA 98195
T. Tameyasu
Affiliation:
Current address: Dept. of Physiology, St. Marianna University, Kawasaki, Japan.
P. Yang
Affiliation:
Dept. of Bioengineering, Box 35-7962, University of Washington, Seattle WA 98195
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Abstract

It is becoming clear that quantal behavior is a central feature of contractile systems. Steplike behavior has been demonstrated in the kinesin - microtubule system and in the myosin - actin filament system-both on molecular scale. We show here that step-like features appear also in the single intact sarcomere. We studied single sarcomeres of single bumblebee myofibrils. Motorimposed ramp length changes on activated myofibrils resulted in sarcomere-length changes that were stepwise. Computer analysis of the stepwise shortening patterns revealed a step-size distribution containing multiple peaks. The peaks were separated by 2.7 nm per half-sarcomere which is the linear actin-subunit spacing. Thus, translation steps are an integer multiple of the actin-subunit spacing. This result parallels the one observed in the kinesin-tubulin spacing where step size is a multiple of the tubulin-subunit spacing. In the muscle system, however, the steps are preserved on a macroscopic scale, implying high synchrony. The quantal steps are easily explained by a model in which the actin filament propels itself over stationary cross-bridges: if actin binds to the cross-bridges between steps, then the observed quantal result is inevitable.

Type
Research Article
Copyright
Copyright © Materials Research Society 1998

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References

1. Gelles, J., Schnapp, B.J., and Sheetz, M.P. Nature 331, 450453 (1988).Google Scholar
2. Hua, W., Young, E.C., Fleming, M.L., and Gelles, J. Nature 388, 390393 (1997).Google Scholar
3. Schnitzer, M.J. and Block, S.M. Nature 388, 386390 (1997).Google Scholar
4. Kojima, H., Muto, E., Higuchi, H., and Yanagida, T. Biophys. J. 73, 20122022 (1997).Google Scholar
5. Warshaw, D. News in Physiol. Sci. 11, 16 (1996).Google Scholar
6. Tskhovrebova, L., Trinick, J., Sleep, J.A., and Simmons, R.M. Nature 387, 308312 (1997).Google Scholar
7. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J.M., and Gaub, H.E. Science 276, 11091112 (1997).Google Scholar
8. Baba, S. A. Nature 282, 717720 (1979).Google Scholar
9. Baba, S. A., Mogami, Y., and Nonaka, K. in Biological Motion eds. Alt, W. and Hoffman, G., Springer, (1990).Google Scholar
10. Yang, P., Tameyasu, T., and Pollack, G.H. Biophys., J. accepted. (1998)Google Scholar
11. Blyakhman, R, Shklyar, T., and Pollack, G.H. (submitted).Google Scholar
12. Saito, K., Aoki, T. Aoki, T. and Yanagida, T., Biophys J. 66, 769777 (1994).Google Scholar
13. Finer, J.T., Mehta, A.D., and Spudich, D. Biophys. J. 68, 291297 (1995).Google Scholar
14. Molloy, J.E., Bums, J.E., Kendrick-Jones, J., Tregear, R.T., White, D.C. Nature 378, 209212 (1995).Google Scholar
15. Pollack, G.H., Iwazumi, T., ter Keurs, H.E.D.J.and Shibata, E.F. Nature 268, 757759 (1977).Google Scholar
16. Delay, M.J., Ishide, N., Jacobson, R.C., Pollack, G.H. and Tirosh, R. Science 213, 15231525 (1981).Google Scholar
17. Jacobson, R.C., Tirosh, R., Delay, M.J. and Pollack, G.H. J. Mus. Res. Cell Motility 4, 529542 (1983).Google Scholar
18. Granzier, H.L.M., Myers, J.A. and Pollack, G.H. J. Mus. Res. & Cell Motility 8, 242251 (1987).Google Scholar
19. Granzier, H.L.M., Mattiazzi, A. and Pollack, G.H. Am. J. Physiol. (Cell) 259, C266s781 (1990).Google Scholar
20. Fauver, M., Dunaway, D., Lilienfield, D., Craighead, H., and Pollack, G.H. IEEE Trans. Biomed. Eng. (in press).Google Scholar
21. Squire, J. The Structural Basis of Muscle Contraction (Plenum Press, New York, 1981).Google Scholar
22. Trombit´s, K., Baatsen, P.H.W.W., and Pollack, G.H. J. Utras. & Mol. Str. Res. 100, 1330 (1988).Google Scholar
23. R¨del, R. and Zite-Frenczy, F. Nature 278, 573575 (1979).Google Scholar
24. Huxley, A. F. Nature 309 (5970), 713714 (1984).Google Scholar
25. Huxley, A. F. Circ. Res. 59, 914 (1986).Google Scholar
26. Altringham, J. D., Bottinelli, R. and Lacktis, J. W.L. Nature 307, 653655 (1984).Google Scholar
27. Goldman, Y E. and Simmons, R. M. J. Physiol. (London) 184, 497518 (1984).Google Scholar
28. Burton, K. and Huxley, A. F. Biophys. J. 68(6), 24292443 (1995).Google Scholar
29. Tameyasu, T., Toyoki, T. and Sugi, H. Biophys. J. 48, 461465 (1985).Google Scholar
30. Toride, M.and Sugi, H. Proc. Japan Acad. 65(B3), 4952 (1989).Google Scholar
31. Tameyasu, T. Japan. J. Physiol. 44, 295318 (1994).Google Scholar
32. Pollack, G.H. Muscles and Molecules: Uncovering the Principles of Biological Motion (Ebner & Sons, Seatttle, 1990).Google Scholar
33. Israelachvili, J., McGuiggan, P., Gee, M., Homola, A., Robbins, M., and Thompson, P.. J. Phys. Condens. Matter 2, SA89–SA98 (1990).Google Scholar
34. Yoshizawa, H. and Israelachvili, J.. J. Phys. Chem. 97, 1130011313 (1993).Google Scholar
35. Bhushan, B., Israelachvili, J., and Landman, U.. Nature 374, 607616 (1995).Google Scholar
36. Gee, M., McGuiggan, P., and Israelachvili, J.N.. J. Chem. Phys. 93(3), 18951906 (1990).Google Scholar
37. Thompson, P. and Robbins, M.. Science 250, 792794 (1990).Google Scholar
38. Diestler, D., Schoen, M., and Cushman, J.. Science 262, 545547 (1993).Google Scholar
39. Ling, G.N. A Revolution in the Physiology of the Living Cell (Krieger Publishing, Florida, 1992).Google Scholar
40. Pollack, G.H. Biophys. Chem. 59, 315328 (1996).Google Scholar
41. Oplatka, A. Critical Rev. Biochem. Mol. Biol. 32, 307360 (1997).Google Scholar
42. Yanagida, T and Ishijima, A. Biophys J. 68, 312s320s(1995).Google Scholar
43. Schutt, C. E. and Lindberg, U. Proc. Nat'l Acad. Sci. 89, 319323 (1992).Google Scholar
44. DeBeer, E.L., Sontrop, A.M.A.T.A., Kellermayer, M.S.Z., and Pollack, G.H. Cell Motil. Cytoskel. (in press).Google Scholar