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Cell control by membrane–cytoskeleton adhesion

Nature Reviews Molecular Cell Biology volume 2, pages 392–396 (2001)Cite this article

Abstract

The rates of mechanochemical processes, such as endocytosis, membrane extension and membrane resealing after cell wounding, are known to be controlled biochemically, through interaction with regulatory proteins. Here, I propose that these rates are also controlled physically, through an apparently continuous adhesion between plasma membrane lipids and cytoskeletal proteins.

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Figure 1: The energetics of endocytic vesicle formation are similar to those of tether formation.
Figure 2: Blebs lack cytoskeleton support.
Figure 3: Lipid-based cytoskeleton–membrane adhesion.
Figure 4: Competition for membrane-binding sites.

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References

  1. Sheetz, M. P. & Dai, J. Modulation of membrane dynamics and cell motility by membrane tension. Trends Cell Biol. 6, 85–89 (1996).

    Article  CAS  Google Scholar 

  2. Raucher, D. & Sheetz, M. P. Membrane expansion increases endocytosis rate during mitosis. J. Cell Biol. 144, 497–506 (1999).

    Article  CAS  Google Scholar 

  3. Dai, J., Ting-Beall, H. P. & Sheetz, M. P. The secretion-coupled endocytosis correlates with membrane tension changes in RBL 2H3 cells. J. Gen. Physiol. 110, 1–10 (1997).

    Article  CAS  Google Scholar 

  4. Dai, J., Sheetz, M. P. & Morris, C. E. Membrane tension in swelling and shrinking molluscan neurons. J. Neurosci. 18, 6681– 6692 (1998).

    Article  CAS  Google Scholar 

  5. Pypaert, M., Mundy, D., Souter, E., Labbe, J. C. & Warren. G. Mitotic cytosol inhibits invagination of coated pits in broken mitotic cells. J. Cell Biol. 114, 1159–1166 (1991).

    Article  CAS  Google Scholar 

  6. Machesky, L. M. & Insall, R. H. Signaling to actin dynamics. J. Cell Biol. 146, 267– 272 (1999).

    Article  CAS  Google Scholar 

  7. Higgs, H. N. & Pollard, T. D. Activation of Cdc42 and PIP2 of WASP stimulates actin nucleation by Arp2/3 complex. J. Cell. Biol. 150, 1311–1320 ( 2000).

    Article  CAS  Google Scholar 

  8. Rohatgi, R., Ho, L. & Kirschner, M. Mechanism of N-wasp activation by CDC 42 and PIP2. J. Cell Biol. 150, 1299–1310 (2000).

    Article  CAS  Google Scholar 

  9. Cameron, L. A., Giardini, P. A., Soo, F. S. & Theriot, J. A. Secrets of actin-based motility revealed by a bacterial pathogen. Nature Rev. Mol. Cell Biol. 1, 110– 119 (2000).

    Article  CAS  Google Scholar 

  10. Prehoda, K. E., Scott, J. A., Dyche Mullins, R. & Lim, W.A. Integration of multiple signals through cooperative regulation of the N-wasp–Arp 2/3 complex. Science 290, 801– 806 (2000).

    Article  CAS  Google Scholar 

  11. Chen, F. et al. Cdc42 is required for PIP2-induced actin polymerization and early development but not for cell viability. Curr. Biol. 10, 758–765 (2000).

    Article  CAS  Google Scholar 

  12. Sormunen, R. & Lehto, V. P. Spectrin in the leading lamella of cultured chicken fibroblasts. Eur. J. Cell Biol. 68, 387–397 (1995).

    CAS  PubMed  Google Scholar 

  13. Mogilner, A. & Oster, G. Cell motility driven by actin polymerization . Biophys. J. 71, 3030– 3045 (1996).

    Article  CAS  Google Scholar 

  14. Raucher, D. & Sheetz, M. P. Cell spreading is regulated by membrane tension. J. Cell Biol. 148, 127 –136 (2000).

    Article  CAS  Google Scholar 

  15. Steinhardt, R. A., Bi, G.-Q. & Alderton, J. M. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science 263, 390–393 (1994).

    Article  CAS  Google Scholar 

  16. Bi, G. Q., Alderton, J. M. & Steinhardt, R. A. Calcium-regulated exocytosis is required for cell membrane resealing. J. Cell Biol. 131, 1747 –1758 (1995).

    Article  CAS  Google Scholar 

  17. Terasaki, M., Miyake, K. & McNeil, P. L. Large plasma membrane disruptions are rapidly resealed by Ca2+-dependent vesicle–vesicle fusion events. J. Cell Biol. 139, 63–74 (1997).

    Article  CAS  Google Scholar 

  18. Togo, T., Alderton, J. M., Bi, G.-Q. & Steinhardt, R. A. The mechanism of facilitated cell membrane resealing. J. Cell Sci. 112, 719–731 ( 1999).

    CAS  PubMed  Google Scholar 

  19. Togo, T., Krasieva, T. B. & Steinhardt, R. A. A decrease in membrane tension precedes successful cell membrane repair. Mol. Biol. Cell 11, 4339–4346 (2000).

    Article  CAS  Google Scholar 

  20. Dai, J. & Sheetz, M. P. Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers . Biophys. J. 68, 988–996 (1995).

    Article  CAS  Google Scholar 

  21. Evans, E. Microscopic-physical determinants in biological adhesion. Blood Cells 19, 401–419 ( 1993).

    CAS  PubMed  Google Scholar 

  22. Raucher, D. et al. Phosphatidylinositol-4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221–228 ( 2000).

    Article  CAS  Google Scholar 

  23. Berk, D. A. & Hochmuth, R. M. Lateral mobility of integral proteins in red blood cell tethers. Biophys. J. 61, 9–18 (1992).

    Article  CAS  Google Scholar 

  24. Dai, J. & Sheetz, M. P. Membrane tether formation from blebbing cells. Biophys. J. 77, 3363– 3370 (1999).

    Article  CAS  Google Scholar 

  25. Keller, H. & Eggli, P. Protrusive activity, cytoplasmic compartmentalization, and restriction rings in locomoting, blebbing Walker carcinosarcoma cells are related to detachment of cortical ac193. Cell Motil. Cytoskeleton 41, 181–193 ( 1998).

    Article  CAS  Google Scholar 

  26. Cunningham, C. C. Actin polymerization and intracellular solvent flow in cell surface blebbing . J. Cell Biol. 129, 1589– 1599 (1995).

    Article  CAS  Google Scholar 

  27. Edidin, M., Zuniga, M. C. & Sheetz, M. P. Truncation mutants define and locate cytoplasmic barriers to lateral mobility of membrane glycoproteins. Proc. Natl Acad. Sci. USA 91, 3378–3382 (1994).

    Article  CAS  Google Scholar 

  28. Janmey, P.A., Xian, W. & Flanagan, L. A. Controlling cytoskeleton structure by phosphoinositide–protein interactions: phosphoinositide binding protein domains and effects of lipid packing. Chem. Phys. Lipids 101, 93– 107 (1999).

    Article  CAS  Google Scholar 

  29. Wang, J., Arbuzova, A., Hangyas-Mihalyne, G. & McLaughlin, S. The effector domain of myristoylated alanine-rich C kinase substrate (MARCKS) binds strongly to phosphatidylinositol 4,5-bisphosphate (PIP2) . J. Biol. Chem. (in the press).

  30. O'Toole, P. J., Wolfe, C., Ladha, S. & Cherry, R. J. Rapid diffusion of spectrin bound to a lipid surface. Biochim. Biophys. Acta 1419, 64–70 (1999).

    Article  CAS  Google Scholar 

  31. Bouchard, M. et al. Interaction between G-actin and various types of liposomes: A 19F, 31P, and 2H nuclear magnetic resonance study. Biochemistry 37, 3149– 3155 (1998).

    Article  CAS  Google Scholar 

  32. Niebuhr, K. et al. IpgD, a protein secreted by the type III secretion machinery of Shigella flexneri, is chaperoned by IpgE and implicated in entry focus formation. Mol. Microbiol. 38, 8– 19 (2000).

    Article  CAS  Google Scholar 

  33. Lanier, L. M. & Gertler, F. B. Actin cytoskeleton: thinking globally, actin' locally. Curr. Biol. 10, R655–R657 (2000).

    Article  CAS  Google Scholar 

  34. Sheetz, M. P. Glycoprotein motility and dynamic domains in fluid plasma membranes. Annu. Rev. Biophys. Biomol. Struct. 22, 417– 431 (1993).

    Article  CAS  Google Scholar 

  35. Apgar, J. R. Activation of protein kinase C in rat basophilic leukemia cells stimulates increased production of phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate: correlation with actin polymerization. Mol. Biol. Cell 6, 97–108 ( 1995).

    Article  CAS  Google Scholar 

  36. Kell, A. & Glaser, R. W. On the mechanical and dynamic properties of plant cell membranes: their role in growth, direct gene transfer and protoplast fusion. J. Theor. Biol. 160, 41–62 (1993).

    Article  CAS  Google Scholar 

  37. Morris, C. E. & Homann, N. Cell surface area regulation and membrane tension. J. Membr. Biol. 179, 79 –102 (2001).

    Article  CAS  Google Scholar 

  38. Herring, T. L., Cohan, C. S., Welnhofer, E. A., Mills, L. R. & Morris, C. E. F-actin at newly invaginated membrane in neurons: implications for surface area regulation. J. Membr. Biol. 171, 151–169 ( 1999).

    Article  CAS  Google Scholar 

  39. Hochmuth, R. M., Shao, J. Y., Dai, J. & Sheetz, M. P. Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys. J. 70, 358–369 (1996).

    Article  CAS  Google Scholar 

  40. Raucher, D. & Sheetz, M. P. Characteristics of a membrane reservoir buffering membrane tension. Biophys. J. 77 , 1992–2002 (1999).

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biological Sciences, Columbia University, Sherman Fairchild Center, 1212 Amsterdam Avenue, PO Box 2408, New York, 10027, New York, USA

    Michael P. Sheetz

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  1. Michael P. Sheetz
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WASP

filamin

pleckstrin homology domains

phospholipase Cδ

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Sheetz, M. Cell control by membrane–cytoskeleton adhesion . Nat Rev Mol Cell Biol 2, 392–396 (2001). https://doi.org/10.1038/35073095

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