Use the force: Membrane tension as an organizer of cell shape and motility

Trends in Cell Biology

Volumn 23, Issue 2, 2013, Pages 47-53

  Diz Muñoz, Alba ^a,b   Fletcher, Daniel A ^a,c   Weiner, Orion D ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Cell shape; Membrane tension; Motility

Indexed keywords

ACTIN; CLATHRIN;

CELL MEMBRANE; CELL MOTILITY; CELL SHAPE; CELL SPREADING; CELL STRUCTURE; CELLULAR PARAMETERS; CYTOSKELETON; ENDOCYTOSIS; EXOCYTOSIS; HUMAN; PLASMA MEMBRANE TENSION; PRIORITY JOURNAL; REVIEW; SENSATION; TENSION;

ACTINS; ANIMALS; BIOMECHANICS; CAVEOLAE; CELL MEMBRANE; CELL MOVEMENT; CELL POLARITY; CELL SHAPE; CYTOSKELETON; ELASTICITY; ENDOCYTOSIS; EXOCYTOSIS; MECHANOTRANSDUCTION, CELLULAR; MYOSINS; STRESS, PHYSIOLOGICAL;

EID: 84872875983     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2012.09.006     Document Type: Review

References (80)

1. Weber G.F., et al. A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev. Cell 2012, 22:104-115.
2. Yonemura S., et al. alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 2010, 12:533-542.
3. Yu H., et al. Forcing form and function: biomechanical regulation of tumor evolution. Trends Cell Biol. 2011, 21:47-56.
4. Apodaca G. Modulation of membrane traffic by mechanical stimuli. Am. J. Physiol. Renal Physiol. 2002, 282:F179-F190.
5. Raucher D., Sheetz M.P. Cell spreading and lamellipodial extension rate is regulated by membrane tension. J. Cell Biol. 2000, 148:127-136.
6. Houk A.R., et al. Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration. Cell 2012, 148:175-188.
7. Singer S., Nicolson G. The fluid mosaic model of the structure of cell membranes. Science 1972, 175:720-731.
8. Hamill O.P., Martinac B. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 2001, 81:685-740.
9. Helms J., Zurzolo C. Lipids as targeting signals: lipid rafts and intracellular trafficking. Traffic 2004, 5:247-254.
10. van Meer G., Sprong H. Membrane lipids and vesicular traffic. Curr. Opin. Cell Biol. 2004, 16:373-378.
11. Cao X., et al. Polarized sorting and trafficking in epithelial cells. Cell Res. 2012, 22:793-805.
12. Evans E. New membrane concept applied to the analysis of fluid shear- and micropipette-deformed red blood cells. Biophys. J. 1973, 13:941-954.
13. Engelhardt H., Sackmann E. On the measurement of shear elastic moduli and viscosities of erythrocyte plasma membranes by transient deformation in high frequency electric fields. Biophys. J. 1988, 54:495-508.
14. Hénon S., et al. A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys. J. 1999, 76:1145-1151.
15. Hochmuth R., et al. Measurement of the elastic modulus for red cell membrane using a fluid mechanical technique. Biophys. J. 1973, 13:747-762.
16. Hochmuth R., Waugh R. Erythrocyte membrane elasticity and viscosity. Annu. Rev. Physiol. 1987, 49:209-219.
17. Hochmuth F.M., et al. Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys. J. 1996, 70:358-369.
18. Bo L., Waugh R.E. Determination of bilayer membrane bending stiffness by tether formation from giant, thin-walled vesicles. Biophys. J. 1989, 55:509-517.
19. Shao J-Y., Xu J. A modified micropipette aspiration technique and its application to tether formation from human neutrophils. J. Biomech. Eng. 2002, 124:388-396.
20. Gauthier N.C., et al. Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:11467-11472.
21. Boulant S., et al. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 2011, 13:1124-1131.
22. Batchelder E.L., et al. Membrane tension regulates motility by controlling lamellipodium organization. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:114429-114434.
23. Keren K., et al. Mechanism of shape determination in motile cells. Nature 2008, 453:475-480.
24. Dai J., Sheetz M.P. Regulation of endocytosis, exocytosis, and shape by membrane tension. Cold Spring Harb. Symp. Quant. Biol. 1995, 60:567-571.
25. Gauthier N.C., et al. Plasma membrane area increases with spread area by exocytosis of a GPI-anchored protein compartment. Mol. Biol. Cell 2009, 20:3261-3272.
26. Sheetz M.P. Glycoprotein motility and dynamic domains in fluid plasma membranes. Annu. Rev. Biophys. Biomol. Struct. 1993, 22:417-431.
27. Gauthier N.C., et al. Mechanical feedback between membrane tension and dynamics. Trends Cell Biol. 2012, 22:527-535.
28. Sheetz M. Cell control by membrane-cytoskeleton adhesion. Nat. Rev. Mol. Cell Biol. 2001, 2:392-396.
29. Dai J., Sheetz M.P. Membrane tether formation from blebbing cells. Biophys. J. 1999, 77:3363-3370.
30. Sinha B., et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 2011, 144:402-413.
31. Gervásio O.L., et al. Caveolae respond to cell stretch and contribute to stretch-induced signaling. J. Cell Sci. 2011, 124:3581-3590.
32. Ofer N., et al. Actin disassembly clock determines shape and speed of lamellipodial fragments. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:20394-20399.
33. Tinevez J-Y., et al. Role of cortical tension in bleb growth. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18581-18586.
34. Mayer M., et al. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 2010, 467:617-621.
35. Cai Y., et al. Cytoskeletal coherence requires myosin-IIA contractility. J. Cell Sci. 2010, 123:413-423.
36. Pasternak C., et al. Capping of surface receptors and concomitant cortical tension are generated by conventional myosin. Nature 1989, 341:549-551.
37. Wessels D., et al. Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Dev. Biol. 1988, 128:164-177.
38. Lee S., et al. Involvement of the cytoskeleton in controlling leading-edge function during chemotaxis. Mol. Biol. Cell 2010, 21:1810-1824.
39. Katsumi A., et al. Effects of cell tension on the small GTPase Rac. J. Cell Biol. 2002, 158:153-164.
40. Kozlov M.M., Mogilner A. Model of polarization and bistability of cell fragments. Biophys. J. 2007, 93:3811-3819.
41. Sukharev S. Mechanosensitive channels in bacteria as membrane tension reporters. FASEB J. 1999, 13:55-61.
42. Charras G.T., et al. Estimating the sensitivity of mechanosensitive ion channels to membrane strain and tension. Biophys. J. 2004, 87:2870-2884.
43. Denk W., Webb W.W. Forward and reverse transduction at the limit of sensitivity studied by correlating electrical and mechanical fluctuations in frog saccular hair cells. Hear. Res. 1992, 60:89-102.
44. Zimmerberg J., Kozlov M.M. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 2006, 7:9-19.
45. Zhao H., et al. I-BAR domain proteins: linking actin and plasma membrane dynamics. Curr. Opin. Cell Biol. 2011, 23:14-21.
46. de Kreuk B.J., et al. The F-BAR domain protein PACSIN2 associates with Rac1 and regulates cell spreading and migration. J. Cell Sci. 2011, 124:2375-2388.
47. Bigay J., et al. Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature. Nature 2003, 426:563-566.
48. Ambroggio E., et al. ArfGAP1 generates an Arf1 gradient on continuous lipid membranes displaying flat and curved regions. EMBO J. 2010, 29:292-303.
49. Sorre B., et al. Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:173-178.
50. Takano K., et al. EFC/F-BAR proteins and the N-WASP-WIP complex induce membrane curvature-dependent actin polymerization. EMBO J. 2008, 27:2817-2828.
51. Peleg B., et al. Propagating cell-membrane waves driven by curved activators of actin polymerization. PLoS ONE 2011, 6:e18635.
52. Tempel M., et al. Insertion of filamin into lipid membranes examined by calorimetry, the film balance technique, and lipid photolabeling. Biochemistry 1994, 33:12565-12572.
53. Nambiar R., et al. Control of cell membrane tension by myosin-I. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:11972-11977.
54. Ehrlicher A.J., et al. Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A. Nature 2011, 478:260-263.
55. Holt J., et al. A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 2002, 108:371-381.
56. Laakso J.M., et al. Myosin I can act as a molecular force sensor. Science 2008, 321:133-136.
57. Wittmann T., Waterman-Storer C.M. Cell motility: can Rho GTPases and microtubules point the way?. J. Cell Sci. 2001, 114:3795-3803.
58. Kusumi A., et al. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 2005, 34:351-378.
59. Tooley A.J., et al. Amoeboid T lymphocytes require the septin cytoskeleton for cortical integrity and persistent motility. Nat. Cell Biol. 2009, 11:17-26.
60. Cole K.S. Surface forces of the Arbacia egg. J. Cell. Comp. Physiol. 1932, 1:1-9.
61. Norris C.H. The tension at the surface, and other physical properties of the nucleated erythrocyte. J. Cell. Comp. Physiol. 1939, 4:117-128.
62. Evans E. Minimum energy analysis of membrane deformation applied to pipet aspiration and surface adhesion of red blood cells. Biophys. J. 1980, 30:265-284.
63. Evans E., Yeung A. Hidden dynamics in rapid changes of bilayer shape. Chem. Phys. Lipids 1994, 73:39-56.
64. Hochmuth R.M., et al. Extensional flow of erythrocyte membrane from cell body to elastic tether. II. Experiment. Biophys. J. 1982, 39:83-89.
65. Dai J., Sheetz M.P. Cell membrane mechanics. Methods Cell Biol. 1998, 55:157-171.
66. Diz-Muñoz A., et al. Control of directed cell migration in vivo by membrane-to-cortex attachment. PLoS Biol. 2010, 8:e1000544.
67. Heinrich V., Waugh R.E. A piconewton force transducer and its application to measurement of the bending stiffness of phospholipid membranes. Ann. Biomed. Eng. 1996, 24:595-605.
68. Grashoff C., et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 2010, 466:263-266.
69. Stewart M.P., et al. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 2011, 469:226-230.
70. Sun M., et al. Multiple membrane tethers probed by atomic force microscopy. Biophys. J. 2005, 89:4320-4329.
71. Waugh R., et al. Local and nonlocal curvature elasticity in bilayer membranes by tether formation from lecithin vesicles. Biophys. J. 1992, 61:974-982.
72. Sheetz M.P., Dai J. Modulation of membrane dynamics and cell motility by membrane tension. Trends Cell Biol. 1996, 6:85-89.
73. Needham D., Evans E. Structure and mechanical properties of giant lipid (DMPC) vesicle bilayers from 20 degrees C below to 10 degrees C above the liquid crystal-crystalline phase transition at 24 degrees C. Biochemistry 1988, 27:8261-8269.
74. Charras G., Paluch E. Blebs lead the way: how to migrate without lamellipodia. Nat. Rev. Mol. Cell Biol. 2008, 9:730-736.
75. Sheetz M., et al. Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:417-434.
76. Brochard-Wyart F., et al. Hydrodynamic narrowing of tubes extruded from cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:7660-7663.
77. Dai J., et al. Membrane tension in swelling and shrinking molluscan neurons. J. Neurosci. 1998, 18:6681-6692.
78. Raucher D., et al. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 2000, 100:221-228.
79. Dai J., Sheetz M.P. Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers. Biophys. J. 1995, 68:988-996.
80. Krieg M., et al. A bond for a lifetime: employing membrane nanotubes from living cells to determine receptor-ligand kinetics. Angew. Chem. Int. Ed. Engl. 2008, 47:9775-9777.