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Actin-dependent organelle movement in squid axoplasm

Abstract

STUDIES of organelle movement in axoplasm extruded from the squid giant axon have led to the basic discoveries of microtubule-dependent organelle motility1–3 and the characterization of the microtubule-based motor proteins kinesin and cytoplasmic dynein4,5. Rapid organelle movement in higher animal cells, especially in ,neurons, is considered to be microtubule-based. The role of actin filaments, which are also abundant in axonal cytoplasm6,7, has remained unclear. The inhibition of organelle movement in axoplasm by actin-binding proteins8–11 such as DNase I, gelsolin and synapsin I has been attributed to their ability to disorganize the microtubule domains where most of the actin-fi laments are located7. Here we provide evidence of a new type of organelle movement in squid axoplasm which is independent of both microtubules and microtubule-based motors. This movement is ATP-dependent, unidirectional, actin-dependent, and probably generated by a myosin-like motor. These results demonstrate that an actomyosin-like mechanism can be directly involved in the generation of rapid organelle transport in nerve cells.

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References

  1. Allen, R. D., Metuzals, J., Tasaki, I., Brady, S. T. & Gilbert, S. P. Science 218, 1127–1128 (1982).

    Article  CAS  Google Scholar 

  2. Allen, R. D. et al. J. Cell Biol. 100, 1736–1752 (1985).

    Article  CAS  Google Scholar 

  3. Weiss, D. G., Langford, G. M., Seitz-Tutter, D. & Keller, F. Cell. Motil. Cytoskel. 10, 285–295 (1988).

    Article  CAS  Google Scholar 

  4. Vale, R. D., Reese, T. S. & Sheetz, M. P. Cell 42, 39–50 (1985).

    Article  CAS  Google Scholar 

  5. Gilbert, S. P. & Sloboda, R. D. J. Cell Biol. 109, 2379–2394 (1989).

    Article  CAS  Google Scholar 

  6. Morris, J. R. & Lasek, R. J. J. Cell Biol. 98, 2064–2076 (1984).

    Article  CAS  Google Scholar 

  7. Fath, K. R. & Lasek, R. J. J. Cell Biol. 107, 613–621 (1988).

    Article  CAS  Google Scholar 

  8. Goldberg, D. J., Harris, D. A., Lubit, B. W. & Schwartz, J. H. Proc. natn. Acad. Sci. U.S.A. 77, 7448–7452 (1980).

    Article  ADS  CAS  Google Scholar 

  9. Isenberg, G., Schubert, P. & Kreutzberg, G. W. Brain Res. 194, 588–593 (1980).

    Article  CAS  Google Scholar 

  10. Brady, S. T., Lasek, R. J., Allen, R. D., Yin, H. L. & Stossel, T. P. Nature 310, 56–58 (1984).

    Article  ADS  CAS  Google Scholar 

  11. McGuinness, T. L. et al. J. Neurosci. 9, 4138–4149 (1989).

    Article  CAS  Google Scholar 

  12. Wulf, E., Deboben, A., Bautz, F. A., Faulstich, H. & Wieland, T. Proc. natn. Acad. Sci. U.S.A. 76, 4498–4502 (1979).

    Article  ADS  CAS  Google Scholar 

  13. Weiss, D. G. J. Cell Sci. S5, 1–15 (1986).

    Article  MathSciNet  Google Scholar 

  14. Estes, J. E., Selden, L. A. & Gershman, L. C. Biochemistry 20, 708–712 (1981).

    Article  CAS  Google Scholar 

  15. Maclean-Fletcher, S. & Pollard, T. D. Cell 20, 329–341 (1980).

    Article  CAS  Google Scholar 

  16. West, J. J., Nagy, B. & Gergely, J. J. biol. Chem. 242, 1140–1145 (1967).

    CAS  PubMed  Google Scholar 

  17. West, J. J., Nagy, B. & Gergely, J. Biochem. biophys. Res. Commun. 29, 611–616 (1967)

    Article  CAS  Google Scholar 

  18. Caldwell, P. C. J. Physiol. 152, 561–590 (1960).

    Article  CAS  Google Scholar 

  19. Kron, S. J. & Spudich, J. A. Proc. natn. Acad. Sci. U.S.A. 83, 6272–6276 (1986).

    Article  ADS  CAS  Google Scholar 

  20. Schnapp, B. J., Vale, R. D., Sheetz, M. P. & Reese, T. S., Cell 40, 455–462 (1985).

    Article  CAS  Google Scholar 

  21. Hoebeke, J., Van Nijen, G. & De Brabander, M. Biochem. biophys. Res. Commun. 69, 319–324 (1976).

    Article  CAS  Google Scholar 

  22. Cohn, S. A., Ingold, A. L. & Scholey, J. M. Nature 328, 160–163 (1987).

    Article  ADS  CAS  Google Scholar 

  23. Gibbons, I. R. et al. Proc. natn. Acad. Sci. U.S.A. 75, 2220–2224 (1978).

    Article  ADS  CAS  Google Scholar 

  24. Paschal, B. M. & Vallee, R. B. Nature 330, 181–183 (1987).

    Article  ADS  CAS  Google Scholar 

  25. Sheetz, M. P. & Spudich, J. A. Nature 303, 31–35 (1983).

    Article  ADS  CAS  Google Scholar 

  26. Greene, L. E., Sellers, J. R., Eisenberg, E. & Adelstein, R. S. Biochemistry 22, 530–535 (1983).

    Article  CAS  Google Scholar 

  27. Smith, S. J. & Eisenberg, E. Eur. J. Biochem. 193, 69–73 (1990).

    Article  CAS  Google Scholar 

  28. Brady, S. T., Lasek, R. J. & Allen, R. D. Cell Motil. 5, 81–101 (1985).

    Article  CAS  Google Scholar 

  29. Weiss, D. G., Maile, W. & Wick, R. A. in Light Microscopy in Biology—A Practical Approach (ed. Lacey, A. J.) 221–278 (IRL, Oxford, 1989).

    Google Scholar 

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Kuznetsov, S., Langford, G. & Weiss, D. Actin-dependent organelle movement in squid axoplasm. Nature 356, 722–725 (1992). https://doi.org/10.1038/356722a0

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