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Endocytic vesicles move at the tips of actin tails in cultured mast cells

Nature Cell Biology volume 1, pages 72–74 (1999)Cite this article

Actin polymerization is thought to provide the motive force for crawling cells by driving the spread of lamellipodia 1. It may also be involved when membrane ruffles engulf external fluid during macropinocytosis 2. Here we show that, in cells transfected with a fusion protein consisting of green fluorescent protein (GFP) and β-actin, pinosomes (vesicles used for fluid uptake) ignite a burst of actin polymerization when they are pinched off from the plasma membrane. Pinosomes then move into the cytosol at the tips of short-lived actin ‘comet tails’ that are similar to those that propel Listeria 3 and other microorganisms 4,5 through infected cells. Like Listeria, pinosomes appear to carry the machinery required for propulsive actin polymerization. The direction of pinosome movement indicates that they may acquire this machinery from the crests of membrane ruffles. We suggest that actin polymerization moves the leading edge of ruffles. Endocytic vesicles may also use actin polymerization to move into the cytosol after being pinched off from the plasma membrane.

The results shown in Fig. 1a were recorded by evanescent field fluorescence microscopy (EFM) 8, a technique that selectively images the bottom of cells where they adhere to a glass coverslip. Some actin tails seemed to originate in the middle of the cell in such recordings; such tails were also seen when the bottom of chemically fixed cells was viewed by laser-scanning confocal microscopy (LSCM). However, three-dimensional images of such tails reconstructed from serial confocal sections showed them to extend to the plasma membrane above (data not shown). In four cells analysed in this way, the appearance of all tails was consistent with the tails having begun at the plasma membrane.

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Figure 1: Tails of F-actin move through live RBL cells.
Figure 2: Actin tails propel pinosomes.

References

  1. Theriot, J. A. & Mitchison, T. J. Nature 352, 126–131 (1991).

    Article  CAS  Google Scholar 

  2. Swanson, J. A. & Watts, C. Trends Cell Biol. 5, 424–428 (1995).

    Article  CAS  Google Scholar 

  3. Theriot, J. A., Mitchison, T. J., Tilney, L. G. & Portnoy, D. A. Nature 357, 257–260 ( 1992).

    Article  CAS  Google Scholar 

  4. Zeile, W. L., Purich, D. L. & Southwick, F. S. J. Cell Biol. 133, 49– 59 (1996).

    Article  CAS  Google Scholar 

  5. Cudmore, S., Cossart, P., Griffiths, G. & Way, M. Nature 378, 636–638 ( 1995).

    Article  CAS  Google Scholar 

  6. Ballestrem, C., Wehrle-Haller, B. & Imhof, B. A. J. Cell Sci. 111, 1649– 1658 (1998).

    CAS  PubMed  Google Scholar 

  7. Parton, R. G., Joggerst, B. & Simons, K. J. Cell Biol. 127, 1199– 1215 (1994).

    Article  CAS  Google Scholar 

  8. Steyer, J. A. & Almers, W. Biophys. J. 76, 2262–2271 (1999).

    Article  CAS  Google Scholar 

  9. Smith, G. A., Theriot, J. A. & Portnoy, D. A. J. Cell Biol. 135, 647– 660 (1996).

    Article  CAS  Google Scholar 

  10. Goldberg, M. B. & Theriot, J. A. Proc. Natl Acad. Sci. USA 92, 6572–6576 (1995).

    Article  CAS  Google Scholar 

  11. Nanavati, D., Ashton, F. T., Sanger, J. M. & Sanger, J. W. Cell Motil. Cytoskeleton 28, 346–358 (1994).

    Article  CAS  Google Scholar 

  12. Heuser, J. E. & Morisaki, J. H. Mol. Biol. Cell Abstr. 3, 172 (1992).

    Google Scholar 

  13. Frischkecht, F. et al. Curr. Biol. 9, 89– 92 (1999).

    Article  Google Scholar 

  14. Welch, M. D., DePace, A. H., Verma, S., Iwamatsu, A. & Mitchison, T. J. J. Cell Biol. 138, 375– 384 (1997).

    Article  CAS  Google Scholar 

  15. Kubler, E. & Riezman, H. EMBO J. 12, 2855–2862 (1993).

    Article  CAS  Google Scholar 

  16. Gottlieb, T. A., Ivanov, I. E., Adesnik, M. & Sabatini, D. D. J. Cell Biol. 120, 695–710 (1993).

    Article  CAS  Google Scholar 

  17. Lamaze, C., Fujimoto, L.M., Yin, H. L. & Schmid, S. L. J. Biol. Chem. 272, 20333–20335 (1997).

    Article  Google Scholar 

  18. Swanson, J. A. J. Cell Sci. 94, 135–142 (1989).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Schweizerische Krebsliga and the Swiss National Science Foundation, by a European Commission grant and by the Max Planck Society. C.J.M. was the recipient of an EMBO short-term fellowship. We thank T. Soldati and T. Lang for comments on the manuscript.

Correspondence and requests for materials should be addressed to W. A.

Supplementary information is available on Nature Cell Biology’s World-Wide Web site (http://www.nature.com/ncb/webfocus/index.html).

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Author notes

  1. Christien J. Merrifield & Wolfhard Almers

    Present address: Vollum Institute, 3181 Sam Jackson Park Road, Portland, Oregon, 97201-3098, USA

Authors and Affiliations

  1. Department of Physiology, University College London, Gower Street, London , WC1E 6BT, UK

    Christien J. Merrifield & Stephen E. Moss

  2. Department of Pathology, Centre Medical Universitaire, Rue Michel-Servet 1, Geneva, CH-1211, Switzerland

    Christoph Ballestrem & Beat A. Imhof

  3. Max Planck Institute für Medizinische Forschung, Jahnstrasse 29, Heidelberg, 69120 , Germany

    Günter Giese, Ilse Wunderlich & Wolfhard Almers

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Correspondence to Wolfhard Almers.

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Merrifield, C., Moss, S., Ballestrem, C. et al. Endocytic vesicles move at the tips of actin tails in cultured mast cells . Nat Cell Biol 1, 72–74 (1999). https://doi.org/10.1038/9048

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