Abstract
Directional cell locomotion is displayed by many cell types both in vivo and in vitro1. 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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Trinkaus, J. P. in The Cell Surface in Animal Embryogenesis and Development (eds Poste, G. & Nicholson, G. L.) 225–329 (Eisevier, Amsterdam, 1976).
Zigmond, S. H. J. Cell Biol. 77, 269–287 (1978).
Carter, S. B. Nature 208, 1183–1190 (1965).
Dunn, G. A. & Heath, J. P. Expl Cell Res. 101, 1–14 (1976).
Gerisch, G. et al. in Development and Differentiation in the Cellular Slime Molds (eds Cappuccinelli, R. & Ashworth, J. M.) 105–124 (Elsevier, Amsterdam, 1977).
Bray, D. in Cell Behaviour (eds Bellairs, R., Curtis, A. & Dunn, G.) 299–317 (Cambridge University Press, 1982).
Gail, M. H. & Boone, C. Biophys. J. 10, 980–993 (1970).
Malech, H. L., Root, R. K. & Gallin, J. I. J. Cell Biol. 75, 666–693 (1977).
Albrecht-Buehler, G. Cell 12, 333–342 (1977).
Albrecht-Buehler, G. Cell Motility 1, 237–245 (1981).
Gotlieb, A. I., McBurnie May, L., Subrahmanyan, L. & Kalnins, V. I. J. Cell Biol. 91, 589–594 (1981)..
Goldman, R. D. J. Cell Biol. 51, 752–767 (1971).
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).
Zigmond, S. H. J. Cell Biol. 75, 606–616 (1977).
Gotlieb, A. I., Subrahmanyan, L. & Kalnins, V.I. J. Cell Biol. 96, 1266–1272 (1983).
Dipasquale, A. Expl Cell Res. 95, 425–439 (1975).
Dunlap, M. K. & Donaldson, D. J. Expl Cell Res. 116, 15–19 (1978).
Rich, A. M. & Hoffstein, S. T. J. Cell Sci. 48, 181–191 (1981).
Alberts, B. et al. Molecular Biology of the Cell, 600–601 (Garland, New York, 1983).
Henrikson, R. C. & Matoltsy, A. G. J Ultrastruct. Res. 21, 194–205 (1968).
Schliwa, M. J. Ultrastruct. Res. 52, 377–386 (1975).
Goodrich, H. B. Biol. Bull. 46, 252–262 (1924).
Radice, G. P. J. Cell Sci. 44, 201–223 (1980).
Bereiter-Hahn, J., Strohmeier, R., Kunzenbacher, I., Beck, k. & Voth, M. J. Cell Sci. 52, 289–311 (1981).
Kunzenbacher, I., Bereiter-Hahn, J., Osborn, M. & Weber, K. Cell Tissue Res. 222, 445–457 (1982).
Keller, H. U. & Bessis, M. Nature 258, 723–724 (1975).
Goldstein, L., Cailleau, R. & Crocker, T.T. Expl Cell Res. 19, 332–342 (1960).
Kalisz, B. & Korohoda, W. Acta protozool. 15, 345–357 (1976).
Shaw, G. & Bray, D. Expl Cell Res. 104, 55–62 (1977).
Albrecht-Buehler, G. Proc. natn. Acad. Sci. U.S.A. 77, 6639–6643 (1980).
Swanson, J. A. & Taylor, D. L. Cell 28, 225–232 (1982).
Schliwa, M. & van Blerkom, J. J. Cell Biol. 90, 222–235 (1981).
Weber, K., Rathke, P. & Osborn, M. Proc. natn. Acad. Sci. U.S.A. 75, 1820–1824 (1978).
Wulf, E., Deboben, A., Bautz, F. A., Faustich, H. & Wieland, T. Proc. natn. Acad. Sci U.S.A. 76, 4498–4502 (1979).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/310058a0
This article is cited by
-
The crucial role of adhesion in the transmigration of active droplets through interstitial orifices
Nature Communications (2023)
-
Phase-Field Modeling of Individual and Collective Cell Migration
Archives of Computational Methods in Engineering (2021)
-
Dual role of the nucleus in cell migration on planar substrates
Biomechanics and Modeling in Mechanobiology (2020)
-
Defining the role of cytoskeletal components in the formation of apoptopodia and apoptotic bodies during apoptosis
Apoptosis (2019)
-
Non-model model organisms
BMC Biology (2017)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.