The detection and role of molecular tension in focal adhesion dynamics

Progress in Molecular Biology and Translational Science

Volumn 126, Issue , 2014, Pages 3-24

  Hoffman, Brenton D ^a  

^a Duke University   (United States)

Author keywords

Cell migration, Focal adhesions; Forster Resonance Energy Transfer; Mechanobiology; Mechanotransduction; Tension sensor; Vinculin

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ACTININ; ADAPTOR PROTEIN; BIOPOLYMER; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBRONECTIN; FILAMIN; FOCAL ADHESION KINASE; GREEN FLUORESCENT PROTEIN; INTEGRIN; MEMBRANE PROTEIN; MYOSIN; PAXILLIN; SINGLE STRANDED DNA; SPECTRIN; TALIN; TRANSCRIPTION FACTOR; UVOMORULIN; VINCULIN;

ACTIN FILAMENT; ARTICLE; BIOSENSOR; CONFORMATION SENSOR; CYTOSKELETON; ENERGY TRANSFER; EXTRACELLULAR MATRIX; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOCAL ADHESION; FORSTER RESONANCE ENERGY TRANSFER; GENE EXPRESSION; HUMAN; MEASUREMENT; MECHANOTRANSDUCTION; MICROSCOPY; MOLECULAR DYNAMICS; MOLECULE; NONHUMAN; OPTICS; PRIORITY JOURNAL; PROTEIN STRUCTURE; STRESS FIBER; TENSION SENSOR; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; GENETIC PROCEDURES; LIGHT RELATED PHENOMENA; METABOLISM;

ANIMALS; BIOMECHANICAL PHENOMENA; BIOSENSING TECHNIQUES; FOCAL ADHESIONS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; OPTICAL PHENOMENA;

EID: 84905169079     PISSN: 18771173     EISSN: 18780814     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394624-9.00001-4     Document Type: Chapter

References (102)

1. C.C. DuFort, M.J. Paszek, and V.M. Weaver Balancing forces: architectural control of mechanotransduction Nat Rev Mol Cell Biol 12 5 2011 308 319
2. M.A. Wozniak, and C.S. Chen Mechanotransduction in development: a growing role for contractility Nat Rev Mol Cell Biol 10 1 2009 34 43
3. W.J. Polacheck, R. Li, S.G. Uzel, and R.D. Kamm Microfluidic platforms for mechanobiology Lab Chip 13 12 2013 2252 2267
4. D.E. Jaalouk, and J. Lammerding Mechanotransduction gone awry Nat Rev Mol Cell Biol 10 1 2009 63 73
5. T. Mammoto, A. Mammoto, and D.E. Ingber Mechanobiology and developmental control Annu Rev Cell Dev Biol 29 2013 27 61
6. C. Hahn, and M.A. Schwartz Mechanotransduction in vascular physiology and atherogenesis Nat Rev Mol Cell Biol 10 1 2009 53 62
7. S. Nemir, and J.L. West Synthetic materials in the study of cell response to substrate rigidity Ann Biomed Eng 38 1 2010 2 20
8. Y. Sun, and J. Fu Mechanobiology: a new frontier for human pluripotent stem cells Integr Biol (Camb) 5 3 2013 450 457
9. K. Takahashi, Y. Kakimoto, K. Toda, and K. Naruse Mechanobiology in cardiac physiology and diseases J Cell Mol Med 17 2 2013 225 232
10. I. Schoen, B.L. Pruitt, and V. Vogel The Yin-Yang of rigidity sensing: how forces and mechanical properties regulate the cellular response to materials Annu Rev Mater Res 43 2013 589 618
11. D.E. Conway, and M.A. Schwartz Flow-dependent cellular mechanotransduction in atherosclerosis J Cell Sci 126 Pt 22 2013 5101 5109
12. B.L. Ricca, G. Venugopalan, and D.A. Fletcher To pull or be pulled: parsing the multiple modes of mechanotransduction Curr Opin Cell Biol 25 5 2013 558 564
13. B.D. Hoffman, C. Grashoff, and M.A. Schwartz Dynamic molecular processes mediate cellular mechanotransduction Nature 475 7356 2011 316 323
14. B. Geiger, J.P. Spatz, and A.D. Bershadsky Environmental sensing through focal adhesions Nat Rev Mol Cell Biol 10 1 2009 21 33
15. M.J. Paszek, N. Zahir, and K.R. Johnson et al. Tensional homeostasis and the malignant phenotype Cancer cell 8 3 2005 241 254 (Pubitemid 41317594)
16. C.M. Lo, H.B. Wang, M. Dembo, and Y.L. Wang Cell movement is guided by the rigidity of the substrate Biophys J 79 1 2000 144 152 (Pubitemid 30436733)
17. A.J. Engler, S. Sen, H.L. Sweeney, and D.E. Discher Matrix elasticity directs stem cell lineage specification Cell 126 4 2006 677 689 (Pubitemid 44233625)
18. C.M. Nelson, R.P. Jean, and J.L. Tan et al. Emergent patterns of growth controlled by multicellular form and mechanics Proc Natl Acad Sci USA 102 33 2005 11594 11599 (Pubitemid 41170771)
19. N. Desprat, W. Supatto, P.A. Pouille, E. Beaurepaire, and E. Farge Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos Dev Cell 15 3 2008 470 477
20. R.L. Duncan, and C.H. Turner Mechanotransduction and the functional response of bone to mechanical strain Calcif Tissue Int 57 5 1995 344 358
21. G. Osol Mechanotransduction by vascular smooth muscle J Vasc Res 32 5 1995 275 292
22. D.E. Ingber Mechanobiology and diseases of mechanotransduction Ann Med 35 8 2003 564 577 (Pubitemid 38005314)
23. K.R. Levental, H. Yu, and L. Kass et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling Cell 139 5 2009 891 906
24. A. Bershadsky, M. Kozlov, and B. Geiger Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize Curr Opin Cell Biol 18 5 2006 472 481 (Pubitemid 44332917)
25. H.P. Erickson Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin Proc Natl Acad Sci USA 91 21 1994 10114 10118
26. M. Rief, M. Gautel, F. Oesterhelt, J.M. Fernandez, and H.E. Gaub Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276 5315 1997 1109 1112 (Pubitemid 27218118)
27. A. del Rio, R. Perez-Jimenez, R. Liu, P. Roca-Cusachs, J.M. Fernandez, and M.P. Sheetz Stretching single talin rod molecules activates vinculin binding Science 323 5914 2009 638 641
28. P.F. Davies Flow-mediated endothelial mechanotransduction Physiol Rev 75 3 1995 519 560
29. S. Chien Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell Am J Physiol Heart Circ Physiol 292 3 2007 H1209 1224
30. F. Meng, T.M. Suchyna, and F. Sachs A fluorescence energy transfer-based mechanical stress sensor for specific proteins in situ FEBS J 275 12 2008 3072 3087 (Pubitemid 351743583)
31. C. Grashoff, B.D. Hoffman, and M.D. Brenner et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics Nature 466 7303 2010 263 266
32. Y. Wang, F. Meng, and F. Sachs Genetically encoded force sensors for measuring mechanical forces in proteins Commun Integr Biol 4 4 2011 385 390
33. D. Riveline, E. Zamir, and N.Q. Balaban et al. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism J Cell Biol 153 6 2001 1175 1186
34. M.A. Schwartz, and D.W. DeSimone Cell adhesion receptors in mechanotransduction Curr Opin Cell Biol 20 5 2008 551 556
35. B. Geiger, and A. Bershadsky Assembly and mechanosensory function of focal contacts Curr Opin Cell Biol 13 5 2001 584 592 (Pubitemid 32817017)
36. R. Zaidel-Bar, S. Itzkovitz, A. Ma'ayan, R. Iyengar, and B. Geiger Functional atlas of the integrin adhesome Nat Cell Biol 9 8 2007 858 867 (Pubitemid 47190436)
37. R. Zaidel-Bar, and B. Geiger The switchable integrin adhesome J Cell Sci 123 Pt 9 2010 1385 1388
38. R.O. Hynes Integrins: bidirectional, allosteric signaling machines Cell 110 6 2002 673 687 (Pubitemid 35283958)
39. P. Kanchanawong, G. Shtengel, and A.M. Pasapera et al. Nanoscale architecture of integrin-based cell adhesions Nature 468 7323 2010 580 584
40. A.W. Orr, B.P. Helmke, B.R. Blackman, and M.A. Schwartz Mechanisms of mechanotransduction Dev Cell 10 1 2006 11 20 (Pubitemid 43025673)
41. R. De, A. Zemel, and S.A. Safran Theoretical concepts and models of cellular mechanosensing Methods Cell Biol 98 2010 143 175
42. G.I. Bell Models for the specific adhesion of cells to cells Science 200 4342 1978 618 627
43. R. Merkel, P. Nassoy, A. Leung, K. Ritchie, and E. Evans Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy Nature 397 6714 1999 50 53 (Pubitemid 29038244)
44. E.A. Evans, and D.A. Calderwood Forces and bond dynamics in cell adhesion Science 316 5828 2007 1148 1153 (Pubitemid 46877469)
45. F. Kong, A.J. Garcia, A.P. Mould, M.J. Humphries, and C. Zhu Demonstration of catch bonds between an integrin and its ligand J Cell Biol 185 7 2009 1275 1284
46. B. Guo, and W.H. Guilford Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction Proc Natl Acad Sci USA 103 26 2006 9844 9849 (Pubitemid 43993585)
47. W.E. Thomas, V. Vogel, and E. Sokurenko Biophysics of catch bonds Annu Rev Biophys 37 2008 399 416
48. K. Hu, L. Ji, K.T. Applegate, G. Danuser, and C.M. Waterman-Storer Differential transmission of actin motion within focal adhesions Science 315 5808 2007 111 115 (Pubitemid 46196992)
49. M.L. Smith, D. Gourdon, and W.C. Little et al. Force-induced unfolding of fibronectin in the extracellular matrix of living cells PLoS Biol 5 10 2007 e268
50. Y. Sawada, M. Tamada, and B.J. Dubin-Thaler et al. Force sensing by mechanical extension of the Src family kinase substrate p130Cas Cell 127 5 2006 1015 1026 (Pubitemid 44803062)
51. D.R. Critchley Biochemical and structural properties of the integrin-associated cytoskeletal protein talin Annu Rev Biophys 38 2009 235 254
52. B.T. Goult, X.P. Xu, and A.R. Gingras et al. Structural studies on full-length talin1 reveal a compact auto-inhibited dimer: implications for talin activation J Struct Biol 184 1 2013 21 32
53. X. Peng, E.S. Nelson, J.L. Maiers, and K.A. DeMali New insights into vinculin function and regulation Int Rev Cell Mol Biol 287 2011 191 231
54. C. Bakolitsa, D.M. Cohen, and L.A. Bankston et al. Structural basis for vinculin activation at sites of cell adhesion Nature 430 6999 2004 583 586 (Pubitemid 38998634)
55. H. Chen, D.M. Cohen, D.M. Choudhury, N. Kioka, and S.W. Craig Spatial distribution and functional significance of activated vinculin in living cells J Cell Biol 169 3 2005 459 470 (Pubitemid 40686696)
56. D.M. Cohen, B. Kutscher, H. Chen, D.B. Murphy, and S.W. Craig A conformational switch in vinculin drives formation and dynamics of a talin-vinculin complex at focal adhesions J Biol Chem 281 23 2006 16006 16015 (Pubitemid 43848494)
57. X. Zhang, G. Jiang, Y. Cai, S.J. Monkley, D.R. Critchley, and M.P. Sheetz Talin depletion reveals independence of initial cell spreading from integrin activation and traction Nat Cell Biol 10 9 2008 1062 1068
58. C.T. Mierke, P. Kollmannsberger, D.P. Zitterbart, J. Smith, B. Fabry, and W.H. Goldmann Mechano-coupling and regulation of contractility by the vinculin tail domain Biophys J 94 2 2008 661 670
59. W. Xu, H. Baribault, and E.D. Adamson Vinculin knockout results in heart and brain defects during embryonic development Development 125 2 1998 327 337 (Pubitemid 28064445)
60. F. Margadant, L.L. Chew, and X. Hu et al. Mechanotransduction in vivo by repeated talin stretch-relaxation events depends upon vinculin PLoS Biol 9 12 2011 e1001223
61. A. Carisey, R. Tsang, and A.M. Greiner et al. Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner Curr Biol 23 4 2013 271 281
62. L.B. Oddershede Force probing of individual molecules inside the living cell is now a reality Nat Chem Biol 8 11 2012 879 886
63. J.R. Lakowicz Principles of Fluorescence Spectroscopy 3rd ed. 2006 Springer New York
64. A. Zeug, A. Woehler, E. Neher, and E.G. Ponimaskin Quantitative intensity-based FRET approaches - a comparative snapshot Biophys J 103 9 2012 1821 1827
65. T.H. Evers, E.M. van Dongen, A.C. Faesen, E.W. Meijer, and M. Merkx Quantitative understanding of the energy transfer between fluorescent proteins connected via flexible peptide linkers Biochemistry 45 44 2006 13183 13192 (Pubitemid 44707679)
66. S. Hohng, R. Zhou, and M.K. Nahas et al. Fluorescence-force spectroscopy maps two-dimensional reaction landscape of the holliday junction Science 318 5848 2007 279 283 (Pubitemid 47574856)
67. S. Okumoto, A. Jones, and W.B. Frommer Quantitative imaging with fluorescent biosensors Annu Rev Plant Biol 63 2012 663 706
68. R.N. Day, C.F. Booker, and A. Periasamy Characterization of an improved donor fluorescent protein for Forster resonance energy transfer microscopy J Biomed Opt 13 3 2008 031203
69. D.R. Stabley, C. Jurchenko, S.S. Marshall, and K.S. Salaita Visualizing mechanical tension across membrane receptors with a fluorescent sensor Nat Methods 9 1 2012 64 67
70. Y. Wang, J.Y. Shyy, and S. Chien Fluorescence proteins, live-cell imaging, and mechanobiology: seeing is believing Annu Rev Biomed Eng 10 2008 1 38
71. F. Meng, and F. Sachs Orientation-based FRET sensor for real-time imaging of cellular forces J Cell Sci 125 Pt 3 2012 743 750
72. H. Shroff, B.M. Reinhard, M. Siu, H. Agarwal, A. Spakowitz, and J. Liphardt Biocompatible force sensor with optical readout and dimensions of 6 nm3 Nano Lett 5 7 2005 1509 1514 (Pubitemid 41084444)
73. F. Meng, and F. Sachs Visualizing dynamic cytoplasmic forces with a compliance-matched FRET sensor J Cell Sci 124 Pt 2 2011 261 269
74. M. Morimatsu, A.H. Mekhdjian, A.S. Adhikari, and A.R. Dunn Molecular tension sensors report forces generated by single integrin molecules in living cells Nano Lett 13 9 2013 3985 3989
75. Y. Liu, K. Yehl, Y. Narui, and K. Salaita Tension sensing nanoparticles for mechano-imaging at the living/nonliving interface J Am Chem Soc 135 14 2013 5320 5323
76. X. Wang, and T. Ha Defining single molecular forces required to activate integrin and notch signaling Science 340 6135 2013 991 994
77. N. Borghi, M. Sorokina, and O.G. Shcherbakova et al. E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch Proc Natl Acad Sci USA 109 31 2012 12568 12573
78. D.E. Conway, M.T. Breckenridge, E. Hinde, E. Gratton, C.S. Chen, and M.A. Schwartz Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1 Curr Biol 23 11 2013 1024 1030
79. S. Iwai, and T.Q. Uyeda Visualizing myosin-actin interaction with a genetically-encoded fluorescent strain sensor Proc Natl Acad Sci USA 105 44 2008 16882 16887
80. T. Ichimura, H. Fujita, K. Yoshizawa, and T.M. Watanabe Engineering strain-sensitive yellow fluorescent protein Chem Commun (Camb) 48 63 2012 7871 7873
81. V.E. Galkin, A. Orlova, and E.H. Egelman Actin filaments as tension sensors Curr Biol 22 3 2012 R96 101
82. K. Austen, C. Kluger, A. Freikamp, A. Chrostek-Grashoff, and C. Grashoff Generation and analysis of biosensors to measure mechanical forces within cells Methods Mol Biol 1066 2013 169 184
83. H. Chen, H.L. Puhl 3rd., S.V. Koushik, S.S. Vogel, and S.R. Ikeda Measurement of FRET efficiency and ratio of donor to acceptor concentration in living cells Biophys J 91 5 2006 L39 41
84. S. Na, O. Collin, and F. Chowdhury et al. Rapid signal transduction in living cells is a unique feature of mechanotransduction Proc Natl Acad Sci USA 105 18 2008 6626 6631 (Pubitemid 351754557)
85. J.T. Parsons, A.R. Horwitz, and M.A. Schwartz Cell adhesion: integrating cytoskeletal dynamics and cellular tension Nat Rev Mol Cell Biol 11 9 2010 633 643
86. M. Chrzanowska-Wodnicka, and K. Burridge Rho-stimulated contractility drives the formation of stress fibers and focal adhesions J Cell Biol 133 6 1996 1403 1415 (Pubitemid 26192339)
87. C.G. Galbraith, K.M. Yamada, and M.P. Sheetz The relationship between force and focal complex development J Cell Biol 159 4 2002 695 705
88. D. Choquet, D.P. Felsenfeld, and M.P. Sheetz Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages Cell 88 1 1997 39 48 (Pubitemid 27180329)
89. C.S. Chen Mechanotransduction - a field pulling together? J Cell Sci 121 Pt 20 2008 3285 3292
90. T. Shemesh, B. Geiger, A.D. Bershadsky, and M.M. Kozlov Focal adhesions as mechanosensors: a physical mechanism Proc Natl Acad Sci USA 102 35 2005 12383 12388 (Pubitemid 41266368)
91. A. Nicolas, B. Geiger, and S.A. Safran Cell mechanosensitivity controls the anisotropy of focal adhesions Proc Natl Acad Sci USA 101 34 2004 12520 12525 (Pubitemid 39122056)
92. A. Besser, and S.A. Safran Force-induced adsorption and anisotropic growth of focal adhesions Biophys J 90 10 2006 3469 3484
93. K.A. Beningo, M. Dembo, I. Kaverina, J.V. Small, and Y.L. Wang Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts J Cell Biol 153 4 2001 881 888
94. J.L. Tan, J. Tien, D.M. Pirone, D.S. Gray, K. Bhadriraju, and C.S. Chen Cells lying on a bed of microneedles: an approach to isolate mechanical force Proc Natl Acad Sci USA 100 4 2003 1484 1489 (Pubitemid 36254472)
95. D.A. Lauffenburger, and A.F. Horwitz Cell migration: a physically integrated molecular process Cell 84 3 1996 359 369 (Pubitemid 26058561)
96. C. Ballestrem, B. Hinz, B.A. Imhof, and B. Wehrle-Haller Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior J Cell Biol 155 7 2001 1319 1332 (Pubitemid 34286280)
97. S. Munevar, Y. Wang, and M. Dembo Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts Biophys J 80 4 2001 1744 1757 (Pubitemid 32280990)
98. S. Munevar, Y.L. Wang, and M. Dembo Distinct roles of frontal and rear cell-substrate adhesions in fibroblast migration Mol Biol Cell 12 12 2001 3947 3954 (Pubitemid 34001084)
99. C.W. Chang, and S. Kumar Vinculin tension distributions of individual stress fibers within cell-matrix adhesions J Cell Sci 126 Pt 14 2013 3021 3030
100. A.W. Holle, X. Tang, and D. Vijayraghavan et al. In situ mechanotransduction via vinculin regulates stem cell differentiation Stem Cells 31 11 2013 2467 2477
101. V. Maruthamuthu, B. Sabass, U.S. Schwarz, and M.L. Gardel Cell-ECM traction force modulates endogenous tension at cell-cell contacts Proc Natl Acad Sci USA 108 12 2011 4708 4713
102. Z. Liu, J.L. Tan, and D.M. Cohen et al. Mechanical tugging force regulates the size of cell-cell junctions Proc Natl Acad Sci USA 107 22 2010 9944 9949