Abstract
Key features of clathrin-mediated endocytosis have been conserved across evolution. However, endocytosis in Saccharomyces cerevisiae is completely dependent on a functional actin cytoskeleton, whereas actin appears to be less critical in mammalian cell endocytosis. We reveal that the fundamental requirement for actin in the early stages of yeast endocytosis is to provide a strong framework to support the force generation needed to direct the invaginating plasma membrane into the cell against turgor pressure. By providing osmotic support, pressure differences across the plasma membrane were removed and this reduced the requirement for actin-bundling proteins in normal endocytosis. Conversely, increased turgor pressure in specific yeast mutants correlated with a decreased rate of endocytic patch invagination.
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References
Smythe, E. & Ayscough, K. R. J. Cell Sci. 119, 4589–4598 (2006).
Ayscough, K. R. Curr.Biol. 10, 1587–1590 (2000).
Ayscough, K. R. et al. J. Cell Biol. 137, 399–416 (1997).
Kaksonen, M., Sun, Y. & Drubin, D. G. Cell 115, 475–487 (2003).
Merrifield, C. J., Feldman, M. E., Wan, L. & Almers, W. Nature Cell Biol. 4, 691–698 (2002).
Merrifield, C. J., Perrais, D. & Zenisek, D. Cell 121, 593–606 (2005).
Yarar, D., Waterman-Storer, C. M. & Schmid, S. L. Mol. Biol. Cell 16, 964–975 (2005).
Gheorghe, D. M. et al. J. Biol. Chem. 283, 15037–15046 (2008).
Whitacre, J. L., Davis, D. A., Toenjes, K. A., Brower, S. M., Adams, A. E. M. Genetics 157, 533–543 (2001).
Merchan, S., Bernal, D., Serrano, R. & Yenush, L. Euk. Cell 3, 100–107 (2004).
Yenush, L., Mulet, J. M., Arino, J. & Serrano, R. EMBO J. 21, 920–929 (2002).
Kaiser, C., Michaelis, S. & Mitchell, A. Methods in yeast genetics: A Laboratory Course Manual. (Cold Spring Harbor Laboratory Press, 1994).
Doyle & Botstein Proc. Natl. Acad. Sci. USA 93, 3886–91 (1996).
Kayingo et al. Arch. Microbiol. 177, 29–35 (2001).
Dulic, V. et al. Meths Enzymol. 194, 697–710 (1991).
Gheorghe, D. M. et al. J. Biol. Chem. 283, 15037–15046 (2008).
Yenush, L., Mulet, J. M., Arino, J. & Serrano, R. EMBO J. 21, 920–929 (2002).
Acknowledgements
We thank V. Allan, E. Smythe and S. Winder for discussions and critical reading of the manuscript, L.Yenush (Universidad Politecnica de Valencia, Spain) for yeast strains. K.R.A. is a senior non-clinical MRC Fellow (G0601600). S.A. is supported by a BBSRC studentship. The light microscopy-imaging centre at the University of Sheffield was funded by a grant from the Wellcome Trust (GR077544AIA).
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S.A. performed and analysed experiments. K.R.A. designed experiments, analysed data and wrote the manuscript.
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Aghamohammadzadeh, S., Ayscough, K. Differential requirements for actin during yeast and mammalian endocytosis. Nat Cell Biol 11, 1039–1042 (2009). https://doi.org/10.1038/ncb1918
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DOI: https://doi.org/10.1038/ncb1918
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