1932

Abstract

Mechanical stimuli are known to be potent regulators of the form and function of cells and organisms. Although biological regulation has classically been understood in terms of principles from solution biochemistry, advancements in many fields have led to the development of a suite of techniques that are able to reveal the interplay between mechanical loading and changes in the biochemical properties of proteins in systems ranging from single molecules to living organisms. Here, we review these techniques and highlight the emergence of a new molecular-scale understanding of the mechanisms mediating the detection and response of cells to mechanical stimuli, a process termed mechanotransduction. Specifically, we focus on the role of subcellular adhesion structures in sensing the stiffness of the surrounding environment because this process is pertinent to applications in tissue engineering as well the onset of several mechanosensitive disease states, including cancer.

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2015-12-07
2024-06-18
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Literature Cited

  1. DuFort CC, Paszek MJ, Weaver VM. 1.  2011. Balancing forces: architectural control of mechanotransduction. Nat. Rev. Mol. Cell Biol. 12:308–19 [Google Scholar]
  2. Wozniak MA, Chen CS. 2.  2009. Mechanotransduction in development: a growing role for contractility. Nat. Rev. Mol. Cell Biol. 10:34–43 [Google Scholar]
  3. Mammoto T, Ingber DE. 3.  2010. Mechanical control of tissue and organ development. Development 137:1407–20 [Google Scholar]
  4. Hahn C, Schwartz MA. 4.  2009. Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10:53–62 [Google Scholar]
  5. Sun Y, Chen CS, Fu J. 5.  2012. Forcing stem cells to behave: a biophysical perspective of the cellular microenvironment. Annu. Rev. Biophys. 41:519–42 [Google Scholar]
  6. Jaalouk DE, Lammerding J. 6.  2009. Mechanotransduction gone awry. Nat. Rev. Mol. Cell Biol. 10:63–73 [Google Scholar]
  7. Lo CM, Wang HB, Dembo M, Wang YL. 7.  2000. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79:144–52 [Google Scholar]
  8. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. 8.  1997. Geometric control of cell life and death. Science 276:1425–28 [Google Scholar]
  9. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. 9.  2004. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6:483–95 [Google Scholar]
  10. Ruiz SA, Chen CS. 10.  2008. Emergence of patterned stem cell differentiation within multicellular structures. Stem Cells 26:2921–27 [Google Scholar]
  11. Rozario T, DeSimone DW. 11.  2010. The extracellular matrix in development and morphogenesis: a dynamic view. Dev. Biol. 341:126–40 [Google Scholar]
  12. Orr AW, Helmke BP, Blackman BR, Schwartz MA. 12.  2006. Mechanisms of mechanotransduction. Dev. Cell 10:11–20 [Google Scholar]
  13. Guilak F, Butler DL, Goldstein SA, Baaijens FP. 13.  2014. Biomechanics and mechanobiology in functional tissue engineering. J. Biomech. 47:1933–40 [Google Scholar]
  14. Schiele NR, Marturano JE, Kuo CK. 14.  2013. Mechanical factors in embryonic tendon development: potential cues for stem cell tenogenesis. Curr. Opin. Biotechnol. 24:834–40 [Google Scholar]
  15. Lecuit T, Lenne PF. 15.  2007. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 8:633–44 [Google Scholar]
  16. Butcher DT, Alliston T, Weaver VM. 16.  2009. A tense situation: forcing tumour progression. Nat. Rev. Cancer 9:108–22 [Google Scholar]
  17. Engler AJ, Sen S, Sweeney HL, Discher DE. 17.  2006. Matrix elasticity directs stem cell lineage specification. Cell 126:677–89 [Google Scholar]
  18. Leight JL, Wozniak MA, Chen S, Lynch ML, Chen CS. 18.  2012. Matrix rigidity regulates a switch between TGF-β1-induced apoptosis and epithelial-mesenchymal transition. Mol. Biol. Cell 23:781–91 [Google Scholar]
  19. Bilodeau K, Mantovani D. 19.  2006. Bioreactors for tissue engineering: focus on mechanical constraints. A comparative review. Tissue Eng. 12:2367–83 [Google Scholar]
  20. Martinac B. 20.  2004. Mechanosensitive ion channels: molecules of mechanotransduction. J. Cell Sci. 117:2449–60 [Google Scholar]
  21. Leckband DE, le Duc Q, Wang N, de Rooij J. 21.  2011. Mechanotransduction at cadherin-mediated adhesions. Curr. Opin. Cell Biol. 23:523–30 [Google Scholar]
  22. Wang N, Tytell JD, Ingber DE. 22.  2009. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10:75–82 [Google Scholar]
  23. Geiger B, Spatz JP, Bershadsky AD. 23.  2009. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10:21–33 [Google Scholar]
  24. Pelham RJ Jr, Wang Y. 24.  1997. Cell locomotion and focal adhesions are regulated by substrate flexibility. PNAS 94:13661–65 [Google Scholar]
  25. Zaidel-Bar R, Itzkovitz S, Ma'ayan A, Iyengar R, Geiger B. 25.  2007. Functional atlas of the integrin adhesome. Nat. Cell Biol. 9:858–67 [Google Scholar]
  26. Winograd-Katz SE, Fassler R, Geiger B, Legate KR. 26.  2014. The integrin adhesome: from genes and proteins to human disease. Nat. Rev. Mol. Cell Biol. 15:273–88 [Google Scholar]
  27. Schwarz US, Gardel ML. 27.  2012. United we stand—integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction. J. Cell Sci. 125:3051–60 [Google Scholar]
  28. Kiosses WB, Shattil SJ, Pampori N, Schwartz MA. 28.  2001. Rac recruits high-affinity integrin αvβ3 to lamellipodia in endothelial cell migration. Nat. Cell Biol. 3:316–20 [Google Scholar]
  29. Choi CK, Vicente-Manzanares M, Zareno J, Whitmore LA, Mogilner A, Horwitz AR. 29.  2008. Actin and α-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat. Cell Biol. 10:1039–50 [Google Scholar]
  30. Schiller HB, Friedel CC, Boulegue C, Fassler R. 30.  2011. Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins. EMBO Rep. 12:259–66 [Google Scholar]
  31. Kaverina I, Krylyshkina O, Small JV. 31.  2002. Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 34:746–61 [Google Scholar]
  32. Thievessen I, Thompson PM, Berlemont S, Plevock KM, Plotnikov SV. 32.  et al. 2013. Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth. J. Cell Biol. 202:163–77 [Google Scholar]
  33. Stricker J, Beckham Y, Davidson MW, Gardel ML. 33.  2013. Myosin II-mediated focal adhesion maturation is tension insensitive. PLOS ONE 8:e70652 [Google Scholar]
  34. Plotnikov SV, Pasapera AM, Sabass B, Waterman CM. 34.  2012. Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 151:1513–27 [Google Scholar]
  35. Burridge K, Wennerberg K. 35.  2004. Rho and Rac take center stage. Cell 116:167–79 [Google Scholar]
  36. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O. 36.  et al. 2009. Coordination of Rho GTPase activities during cell protrusion. Nature 461:99–103 [Google Scholar]
  37. Lawson CD, Burridge K. 37.  2014. The on-off relationship of Rho and Rac during integrin-mediated adhesion and cell migration. Small GTPases 5:e27958 [Google Scholar]
  38. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S. 38.  et al. 2011. Role of YAP/TAZ in mechanotransduction. Nature 474:179–83 [Google Scholar]
  39. Connelly JT, Gautrot JE, Trappmann B, Tan DW, Donati G. 39.  et al. 2010. Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat. Cell Biol. 12:711–18 [Google Scholar]
  40. Wozniak MA, Cheng CQ, Shen CJ, Gao L, Olarerin-George AO. 40.  et al. 2012. Adhesion regulates MAP kinase/ternary complex factor exchange to control a proliferative transcriptional switch. Curr. Biol. 22:2017–26 [Google Scholar]
  41. Hoffman BD, Grashoff C, Schwartz MA. 41.  2011. Dynamic molecular processes mediate cellular mechanotransduction. Nature 475:316–23 [Google Scholar]
  42. Vogel V. 42.  2006. Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 35:459–88 [Google Scholar]
  43. Schwartz MA, DeSimone DW. 43.  2008. Cell adhesion receptors in mechanotransduction. Curr. Opin. Cell Biol. 20:551–56 [Google Scholar]
  44. Gardel ML, Kasza KE, Brangwynne CP, Liu J, Weitz DA. 44.  2008. Chapter 19: mechanical response of cytoskeletal networks. Methods Cell Biol. 89:487–519 [Google Scholar]
  45. Na S, Collin O, Chowdhury F, Tay B, Ouyang M. 45.  et al. 2008. Rapid signal transduction in living cells is a unique feature of mechanotransduction. PNAS 105:6626–31 [Google Scholar]
  46. Vogel V, Sheetz M. 46.  2006. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7:265–75 [Google Scholar]
  47. Árnadóttir J, Chalfie M. 47.  2010. Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39:111–37 [Google Scholar]
  48. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. 48.  2009. Stretching single talin rod molecules activates vinculin binding. Science 323:638–41 [Google Scholar]
  49. Holle AW, Tang X, Vijayraghavan D, Vincent LG, Fuhrmann A. 49.  et al. 2013. In situ mechanotransduction via vinculin regulates stem cell differentiation. Stem Cells 31:2467–77 [Google Scholar]
  50. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R. 50.  et al. 2006. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127:1015–26 [Google Scholar]
  51. Mallion JM, Baguet JP, Siche JP, Tremel F, De Gaudemaris R. 51.  1997. Left ventricular hypertrophy and arterial hypertrophy. Adv. Exp. Med. Biol. 432:123–33 [Google Scholar]
  52. Yao M, Goult BT, Chen H, Cong P, Sheetz MP, Yan J. 52.  2014. Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation. Sci. Rep. 4:4610 [Google Scholar]
  53. Rognoni L, Stigler J, Pelz B, Ylanne J, Rief M. 53.  2012. Dynamic force sensing of filamin revealed in single-molecule experiments. PNAS 109:19679–84 [Google Scholar]
  54. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE. 54.  1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276:1109–12 [Google Scholar]
  55. Furuike S, Ito T, Yamazaki M. 55.  2001. Mechanical unfolding of single filamin A (ABP-280) molecules detected by atomic force microscopy. FEBS Lett. 498:72–75 [Google Scholar]
  56. Chen H, Chandrasekar S, Sheetz MP, Stossel TP, Nakamura F, Yan J. 56.  2013. Mechanical perturbation of filamin A immunoglobulin repeats 20–21 reveals potential non-equilibrium mechanochemical partner binding function. Sci. Rep. 3:1642 [Google Scholar]
  57. Ortiz V, Nielsen SO, Klein ML, Discher DE. 57.  2005. Unfolding a linker between helical repeats. J. Mol. Biol. 349:638–47 [Google Scholar]
  58. Ferrer JM, Lee H, Chen J, Pelz B, Nakamura F. 58.  et al. 2008. Measuring molecular rupture forces between single actin filaments and actin-binding proteins. PNAS 105:9221–26 [Google Scholar]
  59. Lee H, Pelz B, Ferrer JM, Kim T, Lang MJ, Kamm RD. 59.  2009. Cytoskeletal deformation at high strains and the role of cross-link unfolding or unbinding. Cell. Mol. Bioeng. 2:28–38 [Google Scholar]
  60. Lee CY, Lou J, Wen KK, McKane M, Eskin SG. 60.  et al. 2013. Actin depolymerization under force is governed by lysine 113:glutamic acid 195-mediated catch-slip bonds. PNAS 110:5022–27 [Google Scholar]
  61. Guo B, Guilford WH. 61.  2006. Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. PNAS 103:9844–49 [Google Scholar]
  62. Friedland JC, Lee MH, Boettiger D. 62.  2009. Mechanically activated integrin switch controls α5β1 function. Science 323:642–44 [Google Scholar]
  63. Kong F, Garcia AJ, Mould AP, Humphries MJ, Zhu C. 63.  2009. Demonstration of catch bonds between an integrin and its ligand. J. Cell Biol. 185:1275–84 [Google Scholar]
  64. Kong F, Li Z, Parks WM, Dumbauld DW, Garcia AJ. 64.  et al. 2013. Cyclic mechanical reinforcement of integrin-ligand interactions. Mol. Cell 49:1060–68 [Google Scholar]
  65. Risca VI, Wang EB, Chaudhuri O, Chia JJ, Geissler PL, Fletcher DA. 65.  2012. Actin filament curvature biases branching direction. PNAS 109:2913–18 [Google Scholar]
  66. Ehrlicher AJ, Nakamura F, Hartwig JH, Weitz DA, Stossel TP. 66.  2011. Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A. Nature 478:260–63 [Google Scholar]
  67. Ciobanasu C, Faivre B, Le Clainche C. 67.  2014. Actomyosin-dependent formation of the mechanosensitive talin-vinculin complex reinforces actin anchoring. Nat. Commun. 5:3095 [Google Scholar]
  68. Franz CM, Muller DJ. 68.  2005. Analyzing focal adhesion structure by atomic force microscopy. J. Cell Sci. 118:5315–23 [Google Scholar]
  69. Patla I, Volberg T, Elad N, Hirschfeld-Warneken V, Grashoff C. 69.  et al. 2010. Dissecting the molecular architecture of integrin adhesion sites by cryo-electron tomography. Nat. Cell Biol. 12:909–15 [Google Scholar]
  70. Shtengel G, Galbraith JA, Galbraith CG, Lippincott-Schwartz J, Gillette JM. 70.  et al. 2009. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. PNAS 106:3125–30 [Google Scholar]
  71. Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW. 71.  et al. 2010. Nanoscale architecture of integrin-based cell adhesions. Nature 468:580–84 [Google Scholar]
  72. Paszek MJ, DuFort CC, Rubashkin MG, Davidson MW, Thorn KS. 72.  et al. 2012. Scanning angle interference microscopy reveals cell dynamics at the nanoscale. Nat. Methods 9:825–27 [Google Scholar]
  73. Rubashkin MG, Cassereau L, Bainer R, DuFort CC, Yui Y. 73.  et al. 2014. Force engages vinculin and promotes tumor progression by enhancing PI3K activation of phosphatidylinositol (3,4,5)-triphosphate. Cancer Res. 74:4597–611 [Google Scholar]
  74. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF. 74.  et al. 2008. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 5:155–57 [Google Scholar]
  75. Rossier O, Octeau V, Sibarita JB, Leduc C, Tessier B. 75.  et al. 2012. Integrins β1 and β3 exhibit distinct dynamic nanoscale organizations inside focal adhesions. Nat. Cell Biol. 14:1057–67 [Google Scholar]
  76. Schiller HB, Hermann MR, Polleux J, Vignaud T, Zanivan S. 76.  et al. 2013. β1- and αv-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments. Nat. Cell Biol. 15:625–36 [Google Scholar]
  77. Lele TP, Pendse J, Kumar S, Salanga M, Karavitis J, Ingber DE. 77.  2006. Mechanical forces alter zyxin unbinding kinetics within focal adhesions of living cells. J. Cell. Physiol. 207:187–94 [Google Scholar]
  78. Lele T, Oh P, Nickerson JA, Ingber DE. 78.  2004. An improved mathematical approach for determination of molecular kinetics in living cells with FRAP. Mech. Chem. Biosyst. 1:181–90 [Google Scholar]
  79. Pasapera AM, Schneider IC, Rericha E, Schlaepfer DD, Waterman CM. 79.  2010. Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J. Cell Biol. 188:877–90 [Google Scholar]
  80. Wolfenson H, Bershadsky A, Henis YI, Geiger B. 80.  2011. Actomyosin-generated tension controls the molecular kinetics of focal adhesions. J. Cell Sci. 124:1425–32 [Google Scholar]
  81. Berkovich R, Wolfenson H, Eisenberg S, Ehrlich M, Weiss M. 81.  et al. 2011. Accurate quantification of diffusion and binding kinetics of non-integral membrane proteins by FRAP. Traffic 12:1648–57 [Google Scholar]
  82. Bacia K, Schwille P. 82.  2003. A dynamic view of cellular processes by in vivo fluorescence auto- and cross-correlation spectroscopy. Methods 29:74–85 [Google Scholar]
  83. Haustein E, Schwille P. 83.  2007. Fluorescence correlation spectroscopy: novel variations of an established technique. Annu. Rev. Biophys. Biomol. Struct. 36:151–69 [Google Scholar]
  84. Hodgson L, Shen F, Hahn K. 84.  2010. Biosensors for characterizing the dynamics of Rho family GTPases in living cells. Curr. Protoc. Cell Biol. 46:14.11.1–26 [Google Scholar]
  85. Wiseman PW, Brown CM, Webb DJ, Hebert B, Johnson NL. 85.  et al. 2004. Spatial mapping of integrin interactions and dynamics during cell migration by image correlation microscopy. J. Cell Sci. 117:5521–34 [Google Scholar]
  86. Digman MA, Brown CM, Horwitz AR, Mantulin WW, Gratton E. 86.  2008. Paxillin dynamics measured during adhesion assembly and disassembly by correlation spectroscopy. Biophys. J. 94:2819–31 [Google Scholar]
  87. Bachir AI, Zareno J, Moissoglu K, Plow EF, Gratton E, Horwitz AR. 87.  2014. Integrin-associated complexes form hierarchically with variable stoichiometry in nascent adhesions. Curr. Biol. 24:1845–53 [Google Scholar]
  88. Digman MA, Dalal R, Horwitz AF, Gratton E. 88.  2008. Mapping the number of molecules and brightness in the laser scanning microscope. Biophys. J. 94:2320–32 [Google Scholar]
  89. Hoffmann JE, Fermin Y, Stricker RL, Ickstadt K, Zamir E. 89.  2014. Symmetric exchange of multi-protein building blocks between stationary focal adhesions and the cytosol. eLife 3:e02257 [Google Scholar]
  90. Lakowicz JR. 90.  2006. Principles of Fluorescence Spectroscopy New York: Springer [Google Scholar]
  91. Itoh RE, Kurokawa K, Ohba Y, Yoshizaki H, Mochizuki N, Matsuda M. 91.  2002. Activation of Rac and Cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol. Cell. Biol. 22:6582–91 [Google Scholar]
  92. Yoshizaki H, Ohba Y, Kurokawa K, Itoh RE, Nakamura T. 92.  et al. 2003. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J. Cell Biol. 162:223–32 [Google Scholar]
  93. Pertz O, Hodgson L, Klemke RL, Hahn KM. 93.  2006. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440:1069–72 [Google Scholar]
  94. Cai X, Lietha D, Ceccarelli DF, Karginov AV, Rajfur Z. 94.  et al. 2008. Spatial and temporal regulation of focal adhesion kinase activity in living cells. Mol. Cell. Biol. 28:201–14 [Google Scholar]
  95. Wang Y, Botvinick EL, Zhao Y, Berns MW, Usami S. 95.  et al. 2005. Visualizing the mechanical activation of Src. Nature 434:1040–45 [Google Scholar]
  96. Sabouri-Ghomi M, Wu Y, Hahn K, Danuser G. 96.  2008. Visualizing and quantifying adhesive signals. Curr. Opin. Cell Biol. 20:541–50 [Google Scholar]
  97. Kemp-O'Brien K, Parsons M. 97.  2013. Using FRET to analyse signals controlling cell adhesion and migration. J. Microsc. 251:270–78 [Google Scholar]
  98. Smith ML, Gourdon D, Little WC, Kubow KE, Eguiluz RA. 98.  et al. 2007. Force-induced unfolding of fibronectin in the extracellular matrix of living cells. PLOS Biol. 5:e268 [Google Scholar]
  99. Klotzsch E, Smith ML, Kubow KE, Muntwyler S, Little WC. 99.  et al. 2009. Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites. PNAS 106:18267–72 [Google Scholar]
  100. Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M. 100.  et al. 2010. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466:263–66 [Google Scholar]
  101. Meng F, Suchyna TM, Sachs F. 101.  2008. A fluorescence energy transfer-based mechanical stress sensor for specific proteins in situ. FEBS J. 275:3072–87 [Google Scholar]
  102. Nakamura F, Song M, Hartwig JH, Stossel TP. 102.  2014. Documentation and localization of force-mediated filamin A domain perturbations in moving cells. Nat. Commun. 5:4656 [Google Scholar]
  103. Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G. 103.  et al. 2001. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3:466–72 [Google Scholar]
  104. Tan JL, Tien J, Pirone DM, Gray DS, Bhadriraju K, Chen CS. 104.  2003. Cells lying on a bed of microneedles: an approach to isolate mechanical force. PNAS 100:1484–89 [Google Scholar]
  105. Trichet L, Le Digabel J, Hawkins RJ, Vedula SR, Gupta M. 105.  et al. 2012. Evidence of a large-scale mechanosensing mechanism for cellular adaptation to substrate stiffness. PNAS 109:6933–38 [Google Scholar]
  106. Maskarinec SA, Franck C, Tirrell DA, Ravichandran G. 106.  2009. Quantifying cellular traction forces in three dimensions. PNAS 106:22108–13 [Google Scholar]
  107. Legant WR, Choi CK, Miller JS, Shao L, Gao L. 107.  et al. 2013. Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions. PNAS 110:881–86 [Google Scholar]
  108. Mitchison T, Kirschner M. 108.  1988. Cytoskeletal dynamics and nerve growth. Neuron 1:761–72 [Google Scholar]
  109. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G. 109.  2004. Two distinct actin networks drive the protrusion of migrating cells. Science 305:1782–86 [Google Scholar]
  110. Bershadsky A, Kozlov M, Geiger B. 110.  2006. Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize. Curr. Opin. Cell Biol. 18:472–81 [Google Scholar]
  111. Shemesh T, Geiger B, Bershadsky AD, Kozlov MM. 111.  2005. Focal adhesions as mechanosensors: a physical mechanism. PNAS 102:12383–88 [Google Scholar]
  112. Nicolas A, Geiger B, Safran SA. 112.  2004. Cell mechanosensitivity controls the anisotropy of focal adhesions. PNAS 101:12520–25 [Google Scholar]
  113. Besser A, Safran SA. 113.  2006. Force-induced adsorption and anisotropic growth of focal adhesions. Biophys. J. 90:3469–84 [Google Scholar]
  114. Olberding JE, Thouless MD, Arruda EM, Garikipati K. 114.  2010. The non-equilibrium thermodynamics and kinetics of focal adhesion dynamics. PLOS ONE 5:e12043 [Google Scholar]
  115. Nicolas A, Besser A, Safran SA. 115.  2008. Dynamics of cellular focal adhesions on deformable substrates: consequences for cell force microscopy. Biophys. J. 95:527–39 [Google Scholar]
  116. Humphries JD, Wang P, Streuli C, Geiger B, Humphries MJ, Ballestrem C. 116.  2007. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 179:1043–57 [Google Scholar]
  117. Carisey A, Tsang R, Greiner AM, Nijenhuis N, Heath N. 117.  et al. 2013. Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner. Curr. Biol. 23:271–81 [Google Scholar]
  118. Dumbauld DW, Lee TT, Singh A, Scrimgeour J, Gersbach CA. 118.  et al. 2013. How vinculin regulates force transmission. PNAS 110:9788–93 [Google Scholar]
  119. Mohl C, Kirchgessner N, Schafer C, Hoffmann B, Merkel R. 119.  2012. Quantitative mapping of averaged focal adhesion dynamics in migrating cells by shape normalization. J. Cell Sci. 125:155–65 [Google Scholar]
  120. Kolega J. 120.  2003. Asymmetric distribution of myosin IIB in migrating endothelial cells is regulated by a Rho-dependent kinase and contributes to tail retraction. Mol. Biol. Cell 14:4745–57 [Google Scholar]
  121. Razinia Z, Mäkelä T, Ylänne J, Calderwood DA. 121.  2012. Filamins in mechanosensing and signaling. Annu. Rev. Biophys. 41:227–46 [Google Scholar]
  122. Glogauer M, Arora P, Chou D, Janmey PA, Downey GP, McCulloch CA. 122.  1998. The role of actin-binding protein 280 in integrin-dependent mechanoprotection. J. Biol. Chem. 273:1689–98 [Google Scholar]
  123. Calderwood DA, Campbell ID, Critchley DR. 123.  2013. Talins and kindlins: partners in integrin-mediated adhesion. Nat. Rev. Mol. Cell Biol. 14:503–17 [Google Scholar]
  124. Rognoni L, Most T, Zoldak G, Rief M. 124.  2014. Force-dependent isomerization kinetics of a highly conserved proline switch modulates the mechanosensing region of filamin. PNAS 111:5568–73 [Google Scholar]
  125. Byfield FJ, Wen Q, Levental I, Nordstrom K, Arratia PE. 125.  et al. 2009. Absence of filamin A prevents cells from responding to stiffness gradients on gels coated with collagen but not fibronectin. Biophys. J. 96:5095–102 [Google Scholar]
  126. Legate KR, Montanez E, Kudlacek O, Fassler R. 126.  2006. ILK, PINCH and parvin: the tIPP of integrin signalling. Nat. Rev. Mol. Cell Biol. 7:20–31 [Google Scholar]
  127. Stanchi F, Grashoff C, Nguemeni Yonga CF, Grall D. 127.  et al. 2009. Molecular dissection of the ILK-PINCH-parvin triad reveals a fundamental role for the ILK kinase domain in the late stages of focal-adhesion maturation. J. Cell Sci. 122:1800–11 [Google Scholar]
  128. de Beer AG, Cavalcanti-Adam EA, Majer G, Lopez-Garcia M, Kessler H, Spatz JP. 128.  2010. Force-induced destabilization of focal adhesions at defined integrin spacings on nanostructured surfaces. Phys. Rev. E Stat. Nonlinear Soft Matter Phys. 81:051914 [Google Scholar]
  129. Li Y, Bhimalapuram P, Dinner AR. 129.  2010. Model for how retrograde actin flow regulates adhesion traction stresses. J. Phys. Condens. Matter 22:194113 [Google Scholar]
  130. Gardel ML, Sabass B, Ji L, Danuser G, Schwarz US, Waterman CM. 130.  2008. Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. J. Cell Biol. 183:999–1005 [Google Scholar]
  131. Aratyn-Schaus Y, Gardel ML. 131.  2010. Transient frictional slip between integrin and the ECM in focal adhesions under myosin II tension. Curr. Biol. 20:1145–53 [Google Scholar]
  132. Seong J, Tajik A, Sun J, Guan JL, Humphries MJ. 132.  et al. 2013. Distinct biophysical mechanisms of focal adhesion kinase mechanoactivation by different extracellular matrix proteins. PNAS 110:19372–77 [Google Scholar]
  133. Pompe T, Kaufmann M, Kasimir M, Johne S, Glorius S. 133.  et al. 2011. Friction-controlled traction force in cell adhesion. Biophys. J. 101:1863–70 [Google Scholar]
  134. Trappmann B, Gautrot JE, Connelly JT, Strange DG, Li Y. 134.  et al. 2012. Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 11:642–49 [Google Scholar]
  135. Wen JH, Vincent LG, Fuhrmann A, Choi YS, Hribar KC. 135.  et al. 2014. Interplay of matrix stiffness and protein tethering in stem cell differentiation. Nat. Mater. 13:979–87 [Google Scholar]
  136. Sen S, Engler AJ, Discher DE. 136.  2009. Matrix strains induced by cells: computing how far cells can feel. Cell. Mol. Bioeng. 2:39–48 [Google Scholar]
  137. Hu K, Ji L, Applegate KT, Danuser G, Waterman-Storer CM. 137.  2007. Differential transmission of actin motion within focal adhesions. Science 315:111–15 [Google Scholar]
  138. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI. 138.  et al. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell 8:241–54 [Google Scholar]
  139. Galbraith CG, Yamada KM, Sheetz MP. 139.  2002. The relationship between force and focal complex development. J. Cell Biol. 159:695–705 [Google Scholar]
  140. Wang N, Naruse K, Stamenovic D, Fredberg JJ, Mijailovich SM. 140.  et al. 2001. Mechanical behavior in living cells consistent with the tensegrity model. PNAS 98:7765–70 [Google Scholar]
  141. Chan CE, Odde DJ. 141.  2008. Traction dynamics of filopodia on compliant substrates. Science 322:1687–91 [Google Scholar]
  142. Sabass B, Schwarz US. 142.  2010. Modeling cytoskeletal flow over adhesion sites: competition between stochastic bond dynamics and intracellular relaxation. J. Phys. Condens. Matter 22:194112 [Google Scholar]
  143. Walcott S, Kim DH, Wirtz D, Sun SX. 143.  2011. Nucleation and decay initiation are the stiffness-sensitive phases of focal adhesion maturation. Biophys. J. 101:2919–28 [Google Scholar]
  144. Hirata H, Chiam KH, Lim CT, Sokabe M. 144.  2014. Actin flow and talin dynamics govern rigidity sensing in actin-integrin linkage through talin extension. J. R. Soc. Interface 11:20140734 [Google Scholar]
  145. Yamashita H, Ichikawa T, Matsuyama D, Kimura Y, Ueda K. 145.  et al. 2014. The role of the interaction of the vinculin proline-rich linker region with vinexin α in sensing the stiffness of the extracellular matrix. J. Cell Sci. 127:1875–86 [Google Scholar]
  146. Elosegui-Artola A, Bazellieres E, Allen MD, Andreu I, Oria R. 146.  et al. 2014. Rigidity sensing and adaptation through regulation of integrin types. Nat. Mater. 13:631–37 [Google Scholar]
  147. Giannone G, Sheetz MP. 147.  2006. Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol. 16:213–23 [Google Scholar]
  148. Prager-Khoutorsky M, Lichtenstein A, Krishnan R, Rajendran K, Mayo A. 148.  et al. 2011. Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat. Cell Biol. 13:1457–65 [Google Scholar]
  149. Lavelin I, Wolfenson H, Patla I, Henis YI, Medalia O. 149.  et al. 2013. Differential effect of actomyosin relaxation on the dynamic properties of focal adhesion proteins. PLOS ONE 8:e73549 [Google Scholar]
  150. Yao M, Qiu W, Liu R, Efremov AK, Cong P. 150.  et al. 2014. Force-dependent conformational switch of α-catenin controls vinculin binding. Nat. Commun. 5:4525 [Google Scholar]
  151. Gad AK, Ronnlund D, Spaar A, Savchenko AA, Petranyi G. 151.  et al. 2012. Rho GTPases link cellular contractile force to the density and distribution of nanoscale adhesions. FASEB J. 26:2374–82 [Google Scholar]
  152. Johnsson AK, Dai Y, Nobis M, Baker MJ, McGhee EJ. 152.  et al. 2014. The Rac-FRET mouse reveals tight spatiotemporal control of Rac activity in primary cells and tissues. Cell Rep. 6:1153–64 [Google Scholar]
  153. Krieg M, Dunn AR, Goodman MB. 153.  2014. Mechanical control of the sense of touch by β-spectrin. Nat. Cell Biol. 16:224–33 [Google Scholar]
  154. Pines M, Das R, Ellis SJ, Morin A, Czerniecki S. 154.  et al. 2012. Mechanical force regulates integrin turnover in Drosophila in vivo. Nat. Cell Biol. 14:935–43 [Google Scholar]
  155. Humphries JD, Byron A, Bass MD, Craig SE, Pinney JW. 155.  et al. 2009. Proteomic analysis of integrin-associated complexes identifies RCC2 as a dual regulator of Rac1 and Arf6. Sci. Signal. 2:ra51 [Google Scholar]
  156. Kuo JC, Han X, Hsiao CT, Yates JR 3rd, Waterman CM. 156.  2011. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for β-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 13:383–93 [Google Scholar]
  157. Bell GI. 157.  1978. Models for the specific adhesion of cells to cells. Science 200:618–27 [Google Scholar]
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