Membrane tension in rapidly moving cells is determined by cytoskeletal forces

Current Biology

Volumn 23, Issue 15, 2013, Pages 1409-1417

  Lieber, Arnon D ^a   Yehudai Resheff, Shlomit ^a   Barnhart, Erin L ^b   Theriot, Julie A ^b   Keren, Kinneret ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84881311569     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2013.05.063     Document Type: Article

References (43)

1. N.C. Gauthier, T.A. Masters, and M.P. Sheetz Mechanical feedback between membrane tension and dynamics Trends Cell Biol. 22 2012 527 535
2. K. Keren Cell motility: the integrating role of the plasma membrane Eur. Biophys. J. 40 2011 1013 1027
3. M.P. Sheetz, and J. Dai Modulation of membrane dynamics and cell motility by membrane tension Trends Cell Biol. 6 1996 85 89
4. C.E. Morris, and U. Homann Cell surface area regulation and membrane tension J. Membr. Biol. 179 2001 79 102
5. D. Raucher, and M.P. Sheetz Cell spreading and lamellipodial extension rate is regulated by membrane tension J. Cell Biol. 148 2000 127 136
6. A.R. Houk, A. Jilkine, C.O. Mejean, R. Boltyanskiy, E.R. Dufresne, S.B. Angenent, S.J. Altschuler, L.F. Wu, and O.D. Weiner Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration Cell 148 2012 175 188
7. K. Keren, Z. Pincus, G.M. Allen, E.L. Barnhart, G. Marriott, A. Mogilner, and J.A. Theriot Mechanism of shape determination in motile cells Nature 453 2008 475 480
8. N. Ofer, A. Mogilner, and K. Keren Actin disassembly clock determines shape and speed of lamellipodial fragments Proc. Natl. Acad. Sci. USA 108 2011 20394 20399
9. Y. Cai, O. Rossier, N.C. Gauthier, N. Biais, M.A. Fardin, X. Zhang, L.W. Miller, B. Ladoux, V.W. Cornish, and M.P. Sheetz Cytoskeletal coherence requires myosin-IIA contractility J. Cell Sci. 123 2010 413 423
10. J. Dai, and M.P. Sheetz Regulation of endocytosis, exocytosis, and shape by membrane tension Cold Spring Harb. Symp. Quant. Biol. 60 1995 567 571
11. M.M. Kozlov, and A. Mogilner Model of polarization and bistability of cell fragments Biophys. J. 93 2007 3811 3819
12. N.C. Gauthier, M.A. Fardin, P. Roca-Cusachs, and M.P. Sheetz Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading Proc. Natl. Acad. Sci. USA 108 2011 14467 14472
13. E. Evans, and W. Rawicz Entropy-driven tension and bending elasticity in condensed-fluid membranes Phys. Rev. Lett. 64 1990 2094 2097
14. J. Dai, and M.P. Sheetz Membrane tether formation from blebbing cells Biophys. J. 77 1999 3363 3370
15. F.M. Hochmuth, J.Y. Shao, J. Dai, and M.P. Sheetz Deformation and flow of membrane into tethers extracted from neuronal growth cones Biophys. J. 70 1996 358 369
16. M.P. Sheetz, J.E. Sable, and H.G. Döbereiner Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics Annu. Rev. Biophys. Biomol. Struct. 35 2006 417 434
17. D. Raucher, T. Stauffer, W. Chen, K. Shen, S. Guo, J.D. York, M.P. Sheetz, and T. Meyer Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion Cell 100 2000 221 228
18. G. Apodaca Modulation of membrane traffic by mechanical stimuli Am. J. Physiol. Renal Physiol. 282 2002 F179 F190
19. B. Sinha, D. Köster, R. Ruez, P. Gonnord, M. Bastiani, D. Abankwa, R.V. Stan, G. Butler-Browne, B. Vedie, and L. Johannes Cells respond to mechanical stress by rapid disassembly of caveolae Cell 144 2011 402 413
20. P. Sens, and M.S. Turner Budded membrane microdomains as tension regulators Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 73 2006 031918
21. D. Raucher, and M.P. Sheetz Characteristics of a membrane reservoir buffering membrane tension Biophys. J. 77 1999 1992 2002
22. E.L. Batchelder, G. Hollopeter, C. Campillo, X. Mezanges, E.M. Jorgensen, P. Nassoy, P. Sens, and J. Plastino Membrane tension regulates motility by controlling lamellipodium organization Proc. Natl. Acad. Sci. USA 108 2011 11429 11434
23. J. Lee, A. Ishihara, J.A. Theriot, and K. Jacobson Principles of locomotion for simple-shaped cells Nature 362 1993 167 171
24. J. Dai, and M.P. Sheetz Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers Biophys. J. 68 1995 988 996
25. E.A. Evans Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests Biophys. J. 43 1983 27 30
26. M. Sun, J.S. Graham, B. Hegedüs, F. Marga, Y. Zhang, G. Forgacs, and M. Grandbois Multiple membrane tethers probed by atomic force microscopy Biophys. J. 89 2005 4320 4329
27. T.D. Pollard, and G.G. Borisy Cellular motility driven by assembly and disassembly of actin filaments Cell 112 2003 453 465
28. C.A. Wilson, M.A. Tsuchida, G.M. Allen, E.L. Barnhart, K.T. Applegate, P.T. Yam, L. Ji, K. Keren, G. Danuser, and J.A. Theriot Myosin II contributes to cell-scale actin network treadmilling through network disassembly Nature 465 2010 373 377
29. J.A. Cooper Effects of cytochalasin and phalloidin on actin J. Cell Biol. 105 1987 1473 1478
30. B.J. Nolen, N. Tomasevic, A. Russell, D.W. Pierce, Z. Jia, C.D. McCormick, J. Hartman, R. Sakowicz, and T.D. Pollard Characterization of two classes of small molecule inhibitors of Arp2/3 complex Nature 460 2009 1031 1034
31. G.T. Charras, C.K. Hu, M. Coughlin, and T.J. Mitchison Reassembly of contractile actin cortex in cell blebs J. Cell Biol. 175 2006 477 490
32. E.L. Barnhart, K.C. Lee, K. Keren, A. Mogilner, and J.A. Theriot An adhesion-dependent switch between mechanisms that determine motile cell shape PLoS Biol. 9 2011 e1001059
33. A. Hategan, R. Law, S. Kahn, and D.E. Discher Adhesively-tensed cell membranes: lysis kinetics and atomic force microscopy probing Biophys. J. 85 2003 2746 2759
34. S.L. Gupton, and C.M. Waterman-Storer Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration Cell 125 2006 1361 1374
35. G.I. Bell Models for the specific adhesion of cells to cells Science 200 1978 618 627
36. A.F. Straight, A. Cheung, J. Limouze, I. Chen, N.J. Westwood, J.R. Sellers, and T.J. Mitchison Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor Science 299 2003 1743 1747
37. H. Ishihara, B.L. Martin, D.L. Brautigan, H. Karaki, H. Ozaki, Y. Kato, N. Fusetani, S. Watabe, K. Hashimoto, and D. Uemura Calyculin A and okadaic acid: inhibitors of protein phosphatase activity Biochem. Biophys. Res. Commun. 159 1989 871 877
38. S.A. Koestler, K. Rottner, F. Lai, J. Block, M. Vinzenz, and J.V. Small F- and G-actin concentrations in lamellipodia of moving cells PLoS ONE 4 2009 e4810
39. A. Diz-Muñoz, M. Krieg, M. Bergert, I. Ibarlucea-Benitez, D.J. Muller, E. Paluch, and C.P. Heisenberg Control of directed cell migration in vivo by membrane-to-cortex attachment PLoS Biol. 8 2010 e1000544
40. V.C. Abraham, V. Krishnamurthi, D.L. Taylor, and F. Lanni The actin-based nanomachine at the leading edge of migrating cells Biophys. J. 77 1999 1721 1732
41. F. Heinemann, H. Doschke, and M. Radmacher Keratocyte lamellipodial protrusion is characterized by a concave force-velocity relation Biophys. J. 100 2011 1420 1427
42. M.N. Teruel, T.A. Blanpied, K. Shen, G.J. Augustine, and T. Meyer A versatile microporation technique for the transfection of cultured CNS neurons J. Neurosci. Methods 93 1999 37 48
43. Z. Pincus, and J.A. Theriot Comparison of quantitative methods for cell-shape analysis J. Microsc. 227 2007 140 156