Cell spreading and lamellipodial extension rate is regulated by membrane tension

Journal of Cell Biology

Volumn 148, Issue 1, 2000, Pages 127-136

  Raucher, Drazen ^a   Sheetz, Michael P ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cell spreading; Laser optical tweezers; Membrane expansion; Membrane tether; Membrane cytoskeleton adhesion

Indexed keywords

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MOTILITY; CELL SPREADING; CELL SWELLING; CONTROLLED STUDY; CYTOSKELETON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION;

3T3 CELLS; ANIMALS; CELL MEMBRANE; CELL MOVEMENT; DEOXYCHOLIC ACID; DETERGENTS; FLUORESCENT DYES; MICE; ORGANELLES; PHOSPHOLIPIDS; PLATELET-DERIVED GROWTH FACTOR; PSEUDOPODIA;

ANIMALIA;

EID: 0034627878     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.148.1.127     Document Type: Article

References (43)

1. Abercrombie, M., J.E. Heaysman, and S.M. Pegrum. 1970. The locomotion of fibroblasts in culture. 3. Movements of particles on the dorsal surface of the leading lamella. Exp. Cell Res. 62:384-398.
2. Bergman, J.E., A. Kupfer, and S.J. Singer. 1983. Membrane insertion and at the leading edge of motile fibroblasts. Proc. Natl. Acad. Sci. USA. 80:1367-1371.
3. Bershadsky, A.D., and A.H. Futerman. 1994. Disruption of the Golgi apparatus by brefeldin A blocks cell polarization and inhibits directed cell migration. Proc. Natl. Acad. Sci. USA. 91:5686-5689.
4. Chen, W.T. 1981. Mechanism of retraction of the trailing edge during fibroblast movement, J. Cell Biol. 90:187-200.
5. Condeelis, J. 1993. Life at the leading edge: the formation of cell protrusions. Annu. Rev. Cell Biol. 9:411-444.
6. Choquet, D., D.P. Felsenfeld, and M.P. Sheetz, 1997. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88:39-48.
7. Dai, J., and M.P. Sheetz. 1995a. Axon membrane flows from the growth cone to the cell body. Cell. 83:693-701.
8. Dai. J., and M.P. Sheetz. 1995b. Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers. Biophys. J. 68:988-996.
9. Dai, J., and M.P. Sheetz. 1999. Membrane tethers formation from blebbing cells. Biophys. J. 77:3363-3370.
10. Dai, J., H.P. Ting-Beall, and M.P. Sheetz. 1997. The secretion-coupled endocytosis correlates with membrane tension changes in RBL 2H3 cells. Gen. Physiol. 110:1-10.
11. Dai, J., M.P. Sheetz, X. Wan, and C.E. Morris, 1998. Membrane tension in swelling and shrinking molluscan neurons. J. Neurosci. 18:6681-6692.
12. Felder, S., and E.L. Elson. 1990. Mechanics of fibroblast locomotion: quantitative analysis of forces and motions at the leading lamellas of fibroblasts. J. Cell Biol. 111:2513-2526.
13. Felsenfeld, D.P., P.L. Schwartzberg, A. Venegas, R. Tse, and M.P. Sheetz. 1999. Selective regulation of integrin - cytoskeleton interactions by the tyrosine kinase Src. Nat. Cell. Biol. 1:200-206.
14. Hartwig, J.H., S. Kung, T. Kovacsovics, P.A. Janmey, L.C. Cantley, T.P. Stossel, and A. Toker. 1996. D3 phosphoinositides and outside-in integrin signaling by glycoprotein IIb-IIIa mediate platelet actin assembly and filopodial extension induced by phorbol 12-myristate 13-acetate. J. Biol. Chem. 271:32986-32993.
15. Heidemann, S.R., and R.E. Buxhaum. 1998. Cell crawling: first the motor, now the transmission. J. Cell Biol. 141:1-4.
16. Heldin, C.H. 1997. Simultaneous induction of stimulatory and inhibitory signals by PDGF. FEBS (Fed. Eur. Biochem. Soc.) Lett. 410:17-21.
17. Hochmuth, F.M., J.Y. Shao, J. Dai, and M.P. Sheetz. 1996. Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys. J. 70:358-369.
18. Khan, S., and M.P. Sheetz. 1997. Force effects on biochemical kinetics. Annu. Rev. Biochem. 66:785-805.
19. Klausner, R.D., J.G. Donaldson, and J. Lippincott-Schwartz. 1992. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:1071-1080.
20. Kolega, J. 1986. Effects of mechanical tension on protrusive activity and microfilament and intermediate filament organization in an epidermal epithelium moving in culture. J. Cell Biol. 102:1400-1411.
21. Kucik, D.F., F.L. Elson, and M.P. Sheetz. 1989. Forward transport of glycoproteins on leading lamellipodia in locomoting cells. Nature. 340:315-317.
22. Kuo, S.C., and M.P. Sheetz. 1993. Force of single kinesin molecules measured with optical tweezers. Science. 260:232-234.
23. Lee, J., M. Gustafsson, K.E. Magnusson. and K. Jacobson. 1990. The direction of membrane lipid flow in locomoting polymorphonuclear leukocytes. Science. 247:1229-1233.
24. Lombardi, L., D. Ballinari, I. Bongarzone, M. Migliari, P. Mondellini, C. Traversari, and S. Modina. 1990. Ultrastructural cytoskeleton alterations and modification of actin expression in the NIH/3T3 cell line after transformation with Ha-ras-activated oncogene. Cell Motil. Cytoskeleton 15:220-229.
25. Mogilner, A., and G. Oster. 1996. Cell motility driven by actin polymerization. Biophys. J. 71:3030-3045.
26. Mullins, R.D., J.A. Heuser, and T.D. Pollard. 1998. The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl. Acad. Sci. USA. 95: 6181-6189.
27. Oster, G. 1988. Biophysics of the leading lamella. Cell. Motil. Cytoskeleton 10: 164-171.
28. Pelham, H.R. 1991. Recycling of proteins between the endoplasmic reticulum and Golgi complex. Curr. Opin. Cell Biol. 3:585-591.
29. Peskin, C.S., G.M. Odell, and G.F. Oster. 1993. Cellular motions and thermal functions: the Brownian ratchet. Biophys. J. 65:316-324.
30. Raucher, D., and M.P. Sheetz. 1999. Membrane expansion increases endocytosis rate during mitosis. J. Cell Biol. 144:497-506.
31. Raucher, D., T. Stauffer, W. Chen, K. Shen, S. Guo, Y.D. York, M.P. Sheetz, and T. Meyer. 1999. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeletal-plasma membrane adhesion. Cell. In press.
32. Seeman, P. 1972. The membrane actions of anesthetics and tranquilizers. Pharmacol. Rev. 24:583-655.
33. Sheetz, M.P., and S.J. Singer. 1974. Biological membranes as biluyer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA. 71:4457-4461.
34. Sheetz, M.P., and J. Dai. 1996. Modulation of membrane dynamics and cell motility by membrane tension. Trends Cell Biol. 6:85-89.
35. Sheetz, M.P., D.B. Wayne, and A.L. Pearlman. 1992. Extension of filopodia by motor-dependent actin assembly. Cell. Motil. Cytoskeleton. 22:160-169.
36. Stossel, T.P. 1993. On the crawling animal cells. Science. 260:1086-1094.
37. Symons, M.H., and T.J. Mitchison. 1991. Control of actin polymerization in live and permeabilized fibroblasts. J. Cell Biol. 114:503-513.
38. Theriot, J. A. 1997. Accelerating on a treadmill: ADF/cofilin promotes rapid actin filament turnover in the dynamic cytoskeleton. J. Cell Biol. 136:1165-1168.
39. Vasiliev, J.M. 1991. Polarization of pseudopodial activities: cytoskeletal mechanisms. J. Cell Sci. 98:1-4.
40. Watson, P.A. 1991. Function follows form: generation of intracellular signals by cell deformation. FASEB (Fed. Am. Soc. Exp. Biol.) J. 5:2013-2019.
41. Weber, I., E. Wallraff. R. Albrecht. and G.J. Gerisch. 1995. Motility and substratum adhesion of Dictyostelium wild-type and cytoskeletal mutant cells: a study by RICM/bright-field double-view image analysis. Cell Sci. 108:1519-1530.
42. Welch, M.D., A.H. DePace, S. Verma, A. Iwamatsu, and T.J. Mitchison. 1997. The human Arp2/3 complex is composed of evolutionary conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J. Cell. Biol. 138:375-384.
43. Welch, M.D., J. Rosenblatt, J. Skoble, D.A. Portnoy, and T.J. Mitchison. 1998. Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science. 281:105-108.