Abstract
KINESIN, a two-headed motor enzyme molecule, hydrolyses ATP to direct organelle transport along microtubules. As it moves along a microtubule, kinesin remains associated with, or 'tracks', micro-tubule protofilaments1,2. We have prepared truncated kinesin derivatives that contain either two mechanochemical head domains3 or only a single head. Unlike intact kinesin and the two-headed derivatives, the one-headed enzyme frequently fails to track protofilaments, suggesting that it detaches from microtubules during movement. In this way, the one-headed kinesin derivative is similar to the motor enzyme myosin, which frequently detaches from the actin filament during movement4. For myosin (which has two heads), the consequence of this detachment is that single molecules do not appear to drive continuous movement along the filament5. Our observations suggest that the ability of single two-headed kinesin molecules to drive continuous movement6,7 results from a 'hand-over-hand' mechanism6–8 in which one head remains bound to the microtubule while the other detaches and moves forwards.
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References
Gelles, J., Schnapp, B. J. & Sheetz, M. P. Nature 331, 450–453 (1988).
Ray, S., Meyhofer, E., Milligan, R. A. & Howard, J. J. Cell Biol. 121, 1083–1093 (1993).
Scholey, J. M., Heuser, J., Yang, J. T. & Goldstein, L. S. B. Nature 338, 355–357 (1989).
Uyeda, T. Q. P., Warrick, H. M., Kron, S. J. & Spudich, J. A. Nature 352, 307–311 (1991).
Uyeda, T. Q. P., Kron, S. J. & Spudich, J. A. J. molec. Biol. 214, 699–710 (1990).
Howard, J., Hudspeth, A. J. & Vale, R. D. Nature 342, 154–158 (1989).
Block, S. M., Goldstein, L. S. B. & Schnapp, B. J. Nature 348, 348–352 (1990).
Schnapp, B. J., Crise, B., Sheetz, M. P., Reese, T. S. & Khan, S. Proc. natn. Acad. Sci. U.S.A. 87, 10053–10057 (1990).
Cronan, J. E. Jr J. biol. Chem. 265, 10327–10333 (1990).
Berliner, E. et al. J. biol. Chem. 269, 8610–8615 (1994) (see also erratum, 23382).
Stewart, R. J., Thaler, J. P. & Goldstein, L. S. B. Proc. natn. Acad. Sci. U.S.A. 90, 5209–5213 (1993).
Chrétien, D. & Wade, R. H. Biol. Cell 71, 161–174 (1991).
Gelles, J. et al. Biophys. J. (in the press).
Gelles, J., Steuer, E., Schnapp, B. J. & Sheetz, M. P. J. Cell Biol. 109, 157a (1989).
Qian, H., Sheetz, M. P. & Elson, E.L. Biophys. J. 60, 910–921 (1991).
Svoboda, K., Schmidt, C. F., Schnapp, B. J. & Block, S. M. Nature 365, 721–727 (1993).
Hackney, D. D. J. biol. Chem. 269, 16508–16511 (1994).
Huang, T. G. & Hackney, D. D. J. biol. Chem. 269, 16493–16501 (1994).
Stein, L., Schwarz, R. Jr, Chock, P. & Eisenberg, E. Biochemistry 18, 3895–3909 (1979).
Young, E. C., Berliner, E., Mahtani, H. K., Perez-Ramirez, B. & Gelles, J. J. biol. Chem. (in the press).
Summers, M. D. & Smith, G. E. A Manual of Methods for Bacutovirus Vectors and Insect Cell Culture Procedures (Texas Agricultural Experiment Station, College Station, 1987).
Cohn, E.J. & Edsall, J. T. Proteins, Amino Acids and Peptides as Ions and Dipolar Ions 370–381 (Reinhold, New York, 1943).
Hirokawa, N. et al. Cell 56, 867–878 (1989).
Weber, P. C., Ohlendorf, D. H., Wendoloski, J. J. & Salemme, F. R. Science 243, 85–88 (1989).
Staros, J. V., Wright, R. W. & Swingle, D. M. Analyt. Biochem. 156, 220–222 (1986).
Schnapp, B. J. Meth. Enzym. 134, 561–573 (1986).
Schafer, D. A., Gelles, J., Sheetz, M. P. & Landick, R. Nature 352, 444–448 (1991).
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Berliner, E., Young, E., Anderson, K. et al. Failure of a single-headed kinesin to track parallel to microtubule protofilaments. Nature 373, 718–721 (1995). https://doi.org/10.1038/373718a0
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DOI: https://doi.org/10.1038/373718a0
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