Persistent, directional motility of cells and cytoplasmic fragments in the absence of microtubules (original) (raw)

Nature volume 310, pages 58–61 (1984)Cite this article

Abstract

Directional cell locomotion is displayed by many cell types both in vivo and _in vitro_1. In many instances, persistency and directionality are imposed by external stimuli such as chemical attractants or substrate properties2–6. Some cell types, such as fibroblasts or leukocytes, are capable of migrating in the absence of known stimuli in a pattern known as persistent random walk7, where the direction of movement is maintained for at least one cell diameter before the cell performs a sudden directional change. In many examples of persistent motility, microtubules are believed to have a key role as elements that stabilize or even determine a cell's direction of movement8–11. If disassembled, persistency is reduced or impaired12–15. Despite some reports to the contrary16–18, these and other observations have led to the widely accepted view that microtubules may be the overall organizers of cell geometry, polarity and motile activity19. Here we report that rapid, directional locomotion of fish epidermal keratocytes is independent of the presence of microtubules. Moreover, small cytoplasmic fragments derived from the anterior lamella of these cells are capable of locomoting in a pattern indistinguishable from that of intact cells. Since these fragments contain no nucleus, microtubules or centrioles, the persistency-determining component must be sought in some other component(s) of the cytoplasm, possibly the motile machinery of the lamella itself.

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References

  1. Trinkaus, J. P. in The Cell Surface in Animal Embryogenesis and Development (eds Poste, G. & Nicholson, G. L.) 225–329 (Eisevier, Amsterdam, 1976).
    Google Scholar
  2. Zigmond, S. H. J. Cell Biol. 77, 269–287 (1978).
    Article CAS Google Scholar
  3. Carter, S. B. Nature 208, 1183–1190 (1965).
    Article ADS CAS Google Scholar
  4. Dunn, G. A. & Heath, J. P. Expl Cell Res. 101, 1–14 (1976).
    Article ADS CAS Google Scholar
  5. Gerisch, G. et al. in Development and Differentiation in the Cellular Slime Molds (eds Cappuccinelli, R. & Ashworth, J. M.) 105–124 (Elsevier, Amsterdam, 1977).
    Book Google Scholar
  6. Bray, D. in Cell Behaviour (eds Bellairs, R., Curtis, A. & Dunn, G.) 299–317 (Cambridge University Press, 1982).
    Google Scholar
  7. Gail, M. H. & Boone, C. Biophys. J. 10, 980–993 (1970).
    Article ADS CAS Google Scholar
  8. Malech, H. L., Root, R. K. & Gallin, J. I. J. Cell Biol. 75, 666–693 (1977).
    Article CAS Google Scholar
  9. Albrecht-Buehler, G. Cell 12, 333–342 (1977).
    Article CAS Google Scholar
  10. Albrecht-Buehler, G. Cell Motility 1, 237–245 (1981).
    Article CAS Google Scholar
  11. Gotlieb, A. I., McBurnie May, L., Subrahmanyan, L. & Kalnins, V. I. J. Cell Biol. 91, 589–594 (1981)..
    Article CAS Google Scholar
  12. Goldman, R. D. J. Cell Biol. 51, 752–767 (1971).
    Article CAS Google Scholar
  13. Vasiliev, J. M. & Gelfand, I. M. in Cell Motility (eds Goldman, R. D., Pollard, T. D. & Rosenbaum, J. L.) 279–304 (Cold Spring Harbor Laboratory, New York, 1976).
    Google Scholar
  14. Zigmond, S. H. J. Cell Biol. 75, 606–616 (1977).
    Article CAS Google Scholar
  15. Gotlieb, A. I., Subrahmanyan, L. & Kalnins, V.I. J. Cell Biol. 96, 1266–1272 (1983).
    Article CAS Google Scholar
  16. Dipasquale, A. Expl Cell Res. 95, 425–439 (1975).
    Article CAS Google Scholar
  17. Dunlap, M. K. & Donaldson, D. J. Expl Cell Res. 116, 15–19 (1978).
    Article CAS Google Scholar
  18. Rich, A. M. & Hoffstein, S. T. J. Cell Sci. 48, 181–191 (1981).
    CAS PubMed Google Scholar
  19. Alberts, B. et al. Molecular Biology of the Cell, 600–601 (Garland, New York, 1983).
    Google Scholar
  20. Henrikson, R. C. & Matoltsy, A. G. J Ultrastruct. Res. 21, 194–205 (1968).
    Article Google Scholar
  21. Schliwa, M. J. Ultrastruct. Res. 52, 377–386 (1975).
    Article CAS Google Scholar
  22. Goodrich, H. B. Biol. Bull. 46, 252–262 (1924).
    Article Google Scholar
  23. Radice, G. P. J. Cell Sci. 44, 201–223 (1980).
    CAS PubMed Google Scholar
  24. Bereiter-Hahn, J., Strohmeier, R., Kunzenbacher, I., Beck, k. & Voth, M. J. Cell Sci. 52, 289–311 (1981).
    CAS PubMed Google Scholar
  25. Kunzenbacher, I., Bereiter-Hahn, J., Osborn, M. & Weber, K. Cell Tissue Res. 222, 445–457 (1982).
    Article CAS Google Scholar
  26. Keller, H. U. & Bessis, M. Nature 258, 723–724 (1975).
    Article ADS CAS Google Scholar
  27. Goldstein, L., Cailleau, R. & Crocker, T.T. Expl Cell Res. 19, 332–342 (1960).
    Article CAS Google Scholar
  28. Kalisz, B. & Korohoda, W. Acta protozool. 15, 345–357 (1976).
    Google Scholar
  29. Shaw, G. & Bray, D. Expl Cell Res. 104, 55–62 (1977).
    Article CAS Google Scholar
  30. Albrecht-Buehler, G. Proc. natn. Acad. Sci. U.S.A. 77, 6639–6643 (1980).
    Article ADS CAS Google Scholar
  31. Swanson, J. A. & Taylor, D. L. Cell 28, 225–232 (1982).
    Article CAS Google Scholar
  32. Schliwa, M. & van Blerkom, J. J. Cell Biol. 90, 222–235 (1981).
    Article CAS Google Scholar
  33. Weber, K., Rathke, P. & Osborn, M. Proc. natn. Acad. Sci. U.S.A. 75, 1820–1824 (1978).
    Article ADS CAS Google Scholar
  34. Wulf, E., Deboben, A., Bautz, F. A., Faustich, H. & Wieland, T. Proc. natn. Acad. Sci U.S.A. 76, 4498–4502 (1979).
    Article ADS CAS Google Scholar

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  1. Department of Zoology, University of California, Berkeley, California, 94720, USA
    Ursula Euteneuer & Manfred Schliwa

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  1. Ursula Euteneuer
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  2. Manfred Schliwa
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Euteneuer, U., Schliwa, M. Persistent, directional motility of cells and cytoplasmic fragments in the absence of microtubules.Nature 310, 58–61 (1984). https://doi.org/10.1038/310058a0

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