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Abstract

Cells actively sense the mechanical properties of the extracellular matrix, such as its rigidity, morphology, and deformation. The cell–matrix interaction influences a range of cellular processes, including cell adhesion, migration, and differentiation, among others. This article aims to review some of the recent progress that has been made in modeling mechanosensing in cell–matrix interactions at different length scales. The issues discussed include specific interactions between proteins, the structure and mechanosensitivity of focal adhesions, the cluster effects of the specific binding, the structure and behavior of stress fibers, cells' sensing of substrate stiffness, and cell reorientation on cyclically stretched substrates. The review concludes by looking toward future opportunities in the field and at the challenges to understanding active cell–matrix interactions.

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2015-06-22
2024-10-06
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Literature Cited

  1. Alexandrova AY, Arnold K, Schaub S, Vasiliev JM, Meister J-J. 1.  et al. 2008. Comparative dynamics of retrograde actin flow and focal adhesions: Formation of nascent adhesions triggers transition from fast to slow flow. PLOS ONE 3e3234 [Google Scholar]
  2. Arampatzis A, Karamanidis K, Albracht K. 2.  2007. Adaptational responses of the human Achilles tendon by modulation of the applied cyclic strain magnitude. J. Exp. Biol. 210:2743–53 [Google Scholar]
  3. Arnold M, Cavalcanti-Adam EA, Glass R, Blummel J, Eck W. 3.  et al. 2004. Activation of integrin function by nanopatterned adhesive interfaces. ChemPhysChem 5:383–88 [Google Scholar]
  4. Arnold M, Hirschfeld-Warneken VC, Lohmuller T, Heil P, Blummel J. 4.  et al. 2008. Induction of cell polarization and migration by a gradient of nanoscale variations in adhesive ligand spacing. Nano Lett. 8:2063–69 [Google Scholar]
  5. Ayala I, Baldassarre M, Caldieri G, Buccione R. 5.  2006. Invadopodia: a guided tour. Eur. J. Cell Biol. 85:159–64 [Google Scholar]
  6. Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G. 6.  et al. 2001. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3:466–72 [Google Scholar]
  7. Bayraktar HH, Keaveny TM. 7.  2004. Mechanisms of uniformity of yield strains for trabecular bone. J. Biomech. 37:1671–78 [Google Scholar]
  8. Bell GI. 8.  1978. Models for the specific adhesion of cells to cells. Science 200:618–27 [Google Scholar]
  9. Bershadsky AD, Balaban NQ, Geiger B. 9.  2003. Adhesion-dependent cell mechanosensitivity. Annu. Rev. Cell Dev. Biol. 19:677–95 [Google Scholar]
  10. Bershadsky AD, Tint IS, Neyfakh AA, Vasiliev JM. 10.  1985. Focal contacts of normal and RSV-transformed quail cells. Hypothesis of the transformation-induced deficient maturation of focal contacts. Exp. Cell Res. 158:433–44 [Google Scholar]
  11. Besser A, Colombelli J, Stelzer EHK, Schwarz US. 11.  2011. Viscoelastic response of contractile filament bundles. Phys. Rev. E 83:051902 [Google Scholar]
  12. Besser A, Schwarz US. 12.  2007. Coupling biochemistry and mechanics in cell adhesion: a model for inhomogeneous stress fiber contraction. New J. Phys. 9:425 [Google Scholar]
  13. Bihr T, Seifert U, Smith A-S. 13.  2012. Nucleation of ligand-receptor domains in membrane adhesion. Phys. Rev. Lett. 109:258101 [Google Scholar]
  14. Boal D. 14.  2002. Mechanics of the Cell Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  15. Brown NH, Gregory SL, Rickoll WL, Fessler LI, Prout M. 15.  et al. 2002. Talin is essential for integrin function in Drosophila. Dev. Cell 3:569–79 [Google Scholar]
  16. Brown RA, Prajapati R, McGrouther DA, Yannas IV, Eastwood M. 16.  1998. Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates. J. Cell. Physiol. 175:323–32 [Google Scholar]
  17. Burridge K, Chrzanowska-Wodnicka M. 17.  1996. Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12:463–519 [Google Scholar]
  18. Burton K, Park JH, Taylor DL. 18.  1999. Keratocytes generate traction forces in two phases. Mol. Biol. Cell 10:3745–69 [Google Scholar]
  19. Byron A, Morgan MR, Humphries MJ. 19.  2010. Adhesion signalling complexes. Curr. Biol. 20:R1063–67 [Google Scholar]
  20. Chan CE, Odde DJ. 20.  2008. Traction dynamics of filopodia on compliant substrates. Science 322:1687–91 [Google Scholar]
  21. Chen B. 21.  2013. Self-regulation of motor force through chemomechanical coupling in skeletal muscle contraction. J. Appl. Mech. 80:051013 [Google Scholar]
  22. Chen B, Gao H. 22.  2011. Motor force homeostasis in skeletal muscle contraction. Biophys. J. 101:396–403 [Google Scholar]
  23. Chen B, Gao HJ. 23.  2010. Mechanical principle of enhancing cell-substrate adhesion via pre-tension in the cytoskeleton. Biophys. J. 98:2154–62 [Google Scholar]
  24. Chen B, Kemkemer R, Deibler M, Spatz J, Gao H. 24.  2012. Cyclic stretch induces cell reorientation on substrates by destabilizing catch bonds in focal adhesions. PLOS ONE 7e48346 [Google Scholar]
  25. Choi CK, Vicente-Manzanares M, Zareno J, Whitmore LA, Mogilner A, Horwitz AR. 25.  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]
  26. Clark K, Pankov R, Travis MA, Askari JA, Mould AP. 26.  et al. 2005. A specific α5β1-integrin conformation promotes directional integrin translocation and fibronectin matrix formation. J. Cell Sci. 118:291–300 [Google Scholar]
  27. Colombelli J, Besser A, Kress H, Reynaud EG, Girard P. 27.  et al. 2009. Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J. Cell Sci. 122:1665–79 [Google Scholar]
  28. Cooke R. 28.  1986. The mechanism of muscle contraction. CRC Crit. Rev. Biochem. 21:53–118 [Google Scholar]
  29. Costa KD, Hucker WJ, Yin FCP. 29.  2002. Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry. Cell Motil. Cytoskelet. 52:266–74 [Google Scholar]
  30. Curtis AS. 30.  1964. The mechanism of adhesion of cells to glass. A study by interference reflection microscopy. J. Cell Biol. 20:199–215 [Google Scholar]
  31. De R, Zemel A, Safran SA. 31.  2007. Dynamics of cell orientation. Nat. Phys. 3:655–59 [Google Scholar]
  32. Deguchi S, Ohashi T, Sato M. 32.  2006. Tensile properties of single stress fibers isolated from cultured vascular smooth muscle cells. J. Biomech. 39:2603–10 [Google Scholar]
  33. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. 33.  2009. Stretching single talin rod molecules activates vinculin binding. Science 323:638–41 [Google Scholar]
  34. Dembo M, Torney DC, Saxman K, Hammer D. 34.  1988. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc. R. Soc. Lond. B 234:55–83 [Google Scholar]
  35. Dembo M, Wang Y-L. 35.  1999. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76:2307–16 [Google Scholar]
  36. Endlich N, Otey CA, Kriz W, Endlich K. 36.  2007. Movement of stress fibers away from focal adhesions identifies focal adhesions as sites of stress fiber assembly in stationary cells. Cell Motil. Cytoskelet. 64:966–76 [Google Scholar]
  37. Engler AJ, Sen S, Sweeney HL, Discher DE. 37.  2006. Matrix elasticity directs stem cell lineage specification. Cell 126:677–89 [Google Scholar]
  38. Erdmann T, Schwarz US. 38.  2004. Stability of adhesion clusters under constant force. Phys. Rev. Lett. 92:108102 [Google Scholar]
  39. Erdmann T, Schwarz US. 39.  2004. Stochastic dynamics of adhesion clusters under shared constant force and with rebinding. J. Chem. Phys. 121:8997–9017 [Google Scholar]
  40. Erdmann T, Schwarz US. 40.  2006. Bistability of cell-matrix adhesions resulting from non-linear receptor-ligand dynamics. Biophys. J. 91:L60–62 [Google Scholar]
  41. Erdmann T, Schwarz US. 41.  2007. Impact of receptor-ligand distance on adhesion cluster stability. Eur. Phys. J. E 22:123–37 [Google Scholar]
  42. Evans E. 42.  2001. Probing the relation between force—lifetime—and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30:105–28 [Google Scholar]
  43. Evans E, Leung A, Heinrich V, Zhu C. 43.  2004. Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. PNAS 101:11281–86 [Google Scholar]
  44. Evans E, Ludwig F. 44.  2000. Dynamic strengths of molecular anchoring and material cohesion in fluid biomembranes. J. Phys. Condens. Matter 12A315 [Google Scholar]
  45. Evans E, Ritchie K. 45.  1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541–55 [Google Scholar]
  46. Evans EA, Calderwood DA. 46.  2007. Forces and bond dynamics in cell adhesion. Science 316:1148–53 [Google Scholar]
  47. Fournier MF, Sauser R, Ambrosi D, Meister J-J, Verkhovsky AB. 47.  2010. Force transmission in migrating cells. J. Cell Biol. 188:287–97 [Google Scholar]
  48. Freyman TM, Yannas IV, Yokoo R, Gibson LJ. 48.  2002. Fibroblast contractile force is independent of the stiffness which resists the contraction. Exp. Cell Res. 272:153–62 [Google Scholar]
  49. Fu J, Wang Y-K, Yang MT, Desai RA, Yu X. 49.  et al. 2010. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat. Methods 7:733–36 [Google Scholar]
  50. Gao H, Qian J, Chen B. 50.  2011. Probing mechanical principles of focal contacts in cell-matrix adhesion with a coupled stochastic-elastic modelling framework. J. R. Soc. Interface 8:1217–32 [Google Scholar]
  51. Gardel ML, Sabass B, Ji L, Danuser G, Schwarz US, Waterman CM. 51.  2008. Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. J. Cell Biol. 183:999–1005 [Google Scholar]
  52. Geeves MA, Holmes KC. 52.  1999. Structural mechanism of muscle contraction. Annu. Rev. Biochem. 68:687–728 [Google Scholar]
  53. Geiger B, Bershadsky A. 53.  2001. Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13:584–92 [Google Scholar]
  54. Geiger B, Bershadsky A, Pankov R, Yamada KM. 54.  2001. Transmembrane extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2:793–805 [Google Scholar]
  55. Geiger B, Spatz JP, Bershadsky AD. 55.  2009. Environmental sensing through focal adhesions. Nat. Rev. Microbiol. 10:21–33 [Google Scholar]
  56. Georges PC, Janmey PA. 56.  2005. Cell type-specific response to growth on soft materials. J. Appl. Physiol. 98:1547–53 [Google Scholar]
  57. Ghibaudo M, Saez A, Trichet L, Xayaphoummine A, Browaeys J. 57.  et al. 2008. Traction forces and rigidity sensing regulate cell functions. Soft Matter 4:1836–43 [Google Scholar]
  58. Gilmore AP, Burridge K. 58.  1996. Molecular mechanisms for focal adhesion assembly through regulation of protein–protein interactions. Structure 4:647–51 [Google Scholar]
  59. Gimona M, Buccione R. 59.  2006. Adhesions that mediate invasion. Int. J. Biochem. Cell Biol. 38:1875–92 [Google Scholar]
  60. Gingras AR, Ziegler WH, Frank R, Barsukov IL, Roberts GCK. 60.  et al. 2005. Mapping and consensus sequence identification for multiple vinculin binding sites within the talin rod. J. Biol. Chem. 280:37217–24 [Google Scholar]
  61. Goldyn AM, Rioja BA, Spatz JP, Ballestrem C, Kemkemer R. 61.  2009. Force-induced cell polarisation is linked to RhoA-driven microtubule-independent focal-adhesion sliding. J. Cell Sci. 122:3644–51 [Google Scholar]
  62. Guo B, Guilford WH. 62.  2006. Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. PNAS 103:9844–49 [Google Scholar]
  63. Guo X, Lu X, Kassab GS. 63.  2005. Transmural strain distribution in the blood vessel wall. Am. J. Physiol. Heart Circ. Physiol. 288:H881–86 [Google Scholar]
  64. Guthardt Torres P, Bischofs IB, Schwarz US. 64.  2012. Contractile network models for adherent cells. Phys. Rev. E 85:011913 [Google Scholar]
  65. Hanein D, Horwitz AR. 65.  2012. The structure of cell-matrix adhesions: the new frontier. Curr. Opin. Cell Biol. 24:134–40 [Google Scholar]
  66. He S, Su Y, Ji B, Gao H. 66.  2014. Some basic questions on mechanosensing in cell–substrate interaction. J. Mech. Phys. Solids 70:116–35 [Google Scholar]
  67. Heath JP, Dunn GA. 67.  1978. Cell to substratum contacts of chick fibroblasts and their relation to the microfilament system. A correlated interference-reflexion and high-voltage electron-microscope study. J. Cell Sci. 29:197–212 [Google Scholar]
  68. Hill TL. 68.  1987. Linear Aggregation Theory in Cell Biology New York: Springer-Verlag [Google Scholar]
  69. Hotulainen P, Lappalainen P. 69.  2006. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol. 173:383–94 [Google Scholar]
  70. Huang B, Babcock H, Zhuang X. 70.  2010. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143:1047–58 [Google Scholar]
  71. Hytönen VP, Vogel V. 70a.  2008. How force might activate talin's vinculin binding sites: SMD reveals a structural mechanism. PLOS Comput. Biol. 4e24 [Google Scholar]
  72. Ji B, Bao G. 71.  2011. Cell and molecular biomechanics: perspectives and challenges. Acta Mech. Solida Sin. 24:27–51 [Google Scholar]
  73. Jiang G, Giannone G, Critchley DR, Fukumoto E, Sheetz MP. 72.  2003. Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424:334–37 [Google Scholar]
  74. Jungbauer S, Gao H, Spatz JP, Kemkemer R. 73.  2008. Two characteristic regimes in frequency-dependent dynamic reorientation of fibroblasts on cyclically stretched substrates. Biophys. J. 95:3470–78 [Google Scholar]
  75. Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW. 74.  et al. 2010. Nanoscale architecture of integrin-based cell adhesions. Nature 468:580–84 [Google Scholar]
  76. Kaunas R, Hsu H-J, Deguchi S. 75.  2011. Sarcomeric model of stretch-induced stress fiber reorganization. Cell Health Cytoskelet. 3:13–22 [Google Scholar]
  77. Kaverina I, Krylyshkina O, Beningo K, Anderson K, Wang Y-L, Small JV. 76.  2002. Tensile stress stimulates microtubule outgrowth in living cells. J. Cell Sci. 115:2283–91 [Google Scholar]
  78. Kobayashi T, Sokabe M. 77.  2010. Sensing substrate rigidity by mechanosensitive ion channels with stress fibers and focal adhesions. Curr. Opin. Cell Biol. 22:669–76 [Google Scholar]
  79. Kong D, Ji B, Dai L. 78.  2008. Stability of adhesion clusters and cell reorientation under lateral cyclic tension. Biophys. J. 95:4034–44 [Google Scholar]
  80. Kong D, Ji B, Dai L. 79.  2010. Stabilizing to disruptive transition of focal adhesion response to mechanical forces. J. Biomech. 43:2524–29 [Google Scholar]
  81. Kong F, García AJ, Mould AP, Humphries MJ, Zhu C. 80.  2009. Demonstration of catch bonds between an integrin and its ligand. J. Cell Biol. 185:1275–84 [Google Scholar]
  82. Kozlov MM, Mogilner A. 81.  2007. Model of polarization and bistability of cell fragments. Biophys. J. 93:3811–19 [Google Scholar]
  83. Kumar S, Maxwell IZ, Heisterkamp A, Polte TR, Lele TP. 82.  et al. 2006. Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys. J. 90:3762–73 [Google Scholar]
  84. Lecuit T, Lenne P-F. 83.  2007. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Microbiol. 8:633–44 [Google Scholar]
  85. Legant WR, Choi CK, Miller JS, Shao L, Gao L. 83a.  et al. 2013. Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions. PNAS 110:881–86 [Google Scholar]
  86. Legant WR, Miller JS, Blakely BL, Cohen DM, Genin GM, Chen CS. 84.  2010. Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat. Methods 7:969–71 [Google Scholar]
  87. Li D, Ji B. 85.  2014. Predicted rupture force of a single molecular bond becomes rate independent at ultralow loading rates. Phys. Rev. Lett. 112:078302 [Google Scholar]
  88. Lo C-M, Wang H-B, Dembo M, Wang Y-l. 86.  2000. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79:144–52 [Google Scholar]
  89. Lu L, Feng Y, Hucker WJ, Oswald SJ, Longmore GD, Yin FCP. 87.  2008. Actin stress fiber pre-extension in human aortic endothelial cells. Cell Motil. Cytoskelet. 65:281–94 [Google Scholar]
  90. Luo B-H, Carman CV, Springer TA. 88.  2007. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25:619–47 [Google Scholar]
  91. Lymn RW, Taylor EW. 89.  1971. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10:4617–24 [Google Scholar]
  92. Maloney J, Walton E, Bruce C. Vliet K. 90. , Van 2008. Influence of finite thickness and stiffness on cellular adhesion-induced deformation of compliant substrata. Phys. Rev. E 78:041923 [Google Scholar]
  93. Mao Y, Schwarzbauer JE. 91.  2005. Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol. 24:389–99 [Google Scholar]
  94. Marcq P, Yoshinaga N, Prost J. 92.  2011. Rigidity sensing explained by active matter theory. Biophys. J. 101:L33–35 [Google Scholar]
  95. Marshall BT, Long M, Piper JW, Yago T, McEver RP, Zhu C. 93.  2003. Direct observation of catch bonds involving cell-adhesion molecules. Nature 423:190–93 [Google Scholar]
  96. Maruthamuthu V, Sabass B, Schwarz US, Gardel ML. 94.  2011. Cell-ECM traction force modulates endogenous tension at cell–cell contacts. PNAS 108:4708–13 [Google Scholar]
  97. Maskarinec SA, Franck C, Tirrell DA, Ravichandran G. 94a.  2009. Quantifying cellular traction forces in three dimensions. PNAS 106:22108–13 [Google Scholar]
  98. Merkel R, Kirchgessner N, Cesa CM, Hoffmann B. 95.  2007. Cell force microscopy on elastic layers of finite thickness. Biophys. J. 93:3314–23 [Google Scholar]
  99. Mertz A, Banerjee S, Che Y, German G, Xu Y. 96.  et al. 2012. Scaling of traction forces with the size of cohesive cell colonies. Phys. Rev. Lett. 108:198101 [Google Scholar]
  100. Mizutani T, Haga H, Kawabata K. 97.  2004. Cellular stiffness response to external deformation: tensional homeostasis in a single fibroblast. Cell Motil. Cytoskelet. 59:242–48 [Google Scholar]
  101. Morgan MR, Humphries MJ, Bass MD. 98.  2007. Synergistic control of cell adhesion by integrins and syndecans. Nat. Rev. Microbiol. 8:957–69 [Google Scholar]
  102. Naumanen P, Lappalainen P, Hotulainen P. 99.  2008. Mechanisms of actin stress fibre assembly. J. Microsc. 231:446–54 [Google Scholar]
  103. Neidlinger-Wilke C, Wilke HJ, Claes L. 100.  1994. Cyclic stretching of human osteoblasts affects proliferation and metabolism: a new experimental method and its application. J. Orthop. Res. 12:70–78 [Google Scholar]
  104. Oakes PW, Beckham Y, Stricker J, Gardel ML. 101.  2012. Tension is required but not sufficient for focal adhesion maturation without a stress fiber template. J. Cell Biol. 196:363–74 [Google Scholar]
  105. Pankov R, Cukierman E, Katz BZ, Matsumoto K, Lin DC. 102.  et al. 2000. Integrin dynamics and matrix assembly: tensin-dependent translocation of α5β1 integrins promotes early fibronectin fibrillogenesis. J. Cell Biol. 148:1075–90 [Google Scholar]
  106. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI. 103.  et al. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell 8:241–54 [Google Scholar]
  107. Pelham RJ, Wang YL. 104.  1997. Cell locomotion and focal adhesions are regulated by substrate flexibility. PNAS 94:13661–65 [Google Scholar]
  108. Peng X, Huang J, Xiong C, Fang J. 105.  2012. Cell adhesion nucleation regulated by substrate stiffness: a Monte Carlo study. J. Biomech. 45:116–22 [Google Scholar]
  109. Pereverzev YV, Prezhdo OV, Forero M, Sokurenko EV, Thomas WE. 106.  2005. The two-pathway model for the catch-slip transition in biological adhesion. Biophys. J. 89:1446–54 [Google Scholar]
  110. Peterson LJ, Rajfur Z, Maddox AS, Freel CD, Chen Y. 107.  et al. 2004. Simultaneous stretching and contraction of stress fibers in vivo. Mol. Biol. Cell 15:3497–508 [Google Scholar]
  111. Pourati J, Maniotis A, Spiegel D, Schaffer JL, Butler JP. 108.  et al. 1998. Is cytoskeletal tension a major determinant of cell deformability in adherent endothelial cells?. Am. J. Physiol. Cell Physiol. 274:C1283–89 [Google Scholar]
  112. Puklin-Faucher E, Sheetz MP. 109.  2009. The mechanical integrin cycle. J. Cell Sci. 122:179–86 [Google Scholar]
  113. Qian J, Gao H. 110.  2010. Soft matrices suppress cooperative behaviors among receptor-ligand bonds in cell adhesion. PLOS ONE 5e12342 [Google Scholar]
  114. Qian J, Liu H, Lin Y, Chen W, Gao H. 111.  2013. A mechanochemical model of cell reorientation on substrates under cyclic stretch. PLOS ONE 8e65864 [Google Scholar]
  115. Qian J, Wang J, Gao H. 112.  2008. Lifetime and strength of adhesive molecular bond clusters between elastic media. Langmuir 24:1262–70 [Google Scholar]
  116. Qian J, Wang JZ, Lin Y, Gao HJ. 113.  2009. Lifetime and strength of periodic bond clusters between elastic media under inclined loading. Biophys. J. 97:2438–45 [Google Scholar]
  117. Rape AD, Guo W-h, Wang Y-l. 114.  2011. The regulation of traction force in relation to cell shape and focal adhesions. Biomaterials 32:2043–51 [Google Scholar]
  118. Reinhart-King CA, Dembo M, Hammer DA. 115.  2005. The dynamics and mechanics of endothelial cell spreading. Biophys. J. 89:676–89 [Google Scholar]
  119. Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T. 116.  et al. 2001. 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. 153:1175–86 [Google Scholar]
  120. Roca-Cusachs P, Gauthier NC. Rio A, Sheetz MP. 117. , del 2009. Clustering of α5β1 integrins determines adhesion strength whereas αvβ3 and talin enable mechanotransduction. PNAS 106:16245–50 [Google Scholar]
  121. Rottiers P, Saltel F, Daubon T, Chaigne-Delalande B, Tridon V. 118.  et al. 2009. TGFβ-induced endothelial podosomes mediate basement membrane collagen degradation in arterial vessels. J. Cell Sci. 122:4311–18 [Google Scholar]
  122. Ruimerman R, Hilbers P, van Rietbergen B, Huiskes R. 119.  2005. A theoretical framework for strain-related trabecular bone maintenance and adaptation. J. Biomech. 38:931–41 [Google Scholar]
  123. Russell RJ, Xia S-L, Dickinson RB, Lele TP. 120.  2009. Sarcomere mechanics in capillary endothelial cells. Biophys. J. 97:1578–85 [Google Scholar]
  124. Saez A, Buguin A, Silberzan P, Ladoux B. 121.  2005. Is the mechanical activity of epithelial cells controlled by deformations or forces?. Biophys. J. 89:L52–54 [Google Scholar]
  125. Sarangapani KK, Yago T, Klopocki AG, Lawrence MB, Fieger CB. 122.  et al. 2004. Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J. Biol. Chem. 279:2291–98 [Google Scholar]
  126. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R. 123.  et al. 2006. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127:1015–26 [Google Scholar]
  127. Schoen I, Pruitt BL, Vogel V. 123a.  2013. The yin-yang of rigidity sensing: how forces and mechanical properties regulate the cellular response to materials. Annu. Rev. Mater. Res. 43:589–618 [Google Scholar]
  128. Schwartz MA, Chen CS. 124.  2013. Cell biology. Deconstructing dimensionality. Science 339:402–4 [Google Scholar]
  129. Schwartz MA, Ginsberg MH. 125.  2002. Networks and crosstalk: integrin signalling spreads. Nat. Cell Biol. 4:E65–68 [Google Scholar]
  130. Schwarz US, Erdmann T, Bischofs IB. 126.  2006. Focal adhesions as mechanosensors: the two-spring model. BioSystems 83:225–32 [Google Scholar]
  131. Schwarz US, Gardel ML. 127.  2012. United we stand: integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction. J. Cell Sci. 125:3051–60 [Google Scholar]
  132. Seifert U. 128.  2000. Rupture of multiple parallel molecular bonds under dynamic loading. Phys. Rev. Lett. 84:2750 [Google Scholar]
  133. Selhuber-Unkel C, Erdmann T, López-García M, Kessler H, Schwarz US, Spatz JP. 129.  2010. Cell adhesion strength is controlled by intermolecular spacing of adhesion receptors. Biophys. J. 98:543–51 [Google Scholar]
  134. Sen S, Engler AJ, Discher DE. 130.  2009. Matrix strains induced by cells: computing how far cells can feel. Cell. Mol. Bioeng. 2:39–48 [Google Scholar]
  135. Shemesh T, Geiger B, Bershadsky AD, Kozlov MM. 131.  2005. Focal adhesions as mechanosensors: a physical mechanism. PNAS 102:12383–88 [Google Scholar]
  136. Shemesh T, Verkhovsky AB, Svitkina TM, Bershadsky AD, Kozlov MM. 131a.  2009. Role of focal adhesions and mechanical stresses in the formation and progression of the lamellum interface. Biophys. J. 97:1254–64 [Google Scholar]
  137. Small JV, Rottner K, Kaverina I. 132.  1999. Functional design in the actin cytoskeleton. Curr. Opin. Cell Biol. 11:54–60 [Google Scholar]
  138. Smith ML, Gourdon D, Little WC, Kubow KE, Eguiluz RA. 133.  et al. 2007. Force-induced unfolding of fibronectin in the extracellular matrix of living cells. PLOS Biol. 5e268 [Google Scholar]
  139. Stachowiak MR, O'Shaughnessy B. 134.  2008. Kinetics of stress fibers. New J. Phys. 10:025002 [Google Scholar]
  140. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC. 135.  et al. 2003. Talin binding to integrin β tails: a final common step in integrin activation. Science 302:103–6 [Google Scholar]
  141. Tan JL, Tien J, Pirone DM, Gray DS, Bhadriraju K, Chen CS. 136.  2003. Cells lying on a bed of microneedles: an approach to isolate mechanical force. PNAS 100:1484 [Google Scholar]
  142. Tee S-Y, Fu J, Chen CS, Janmey PA. 137.  2011. Cell shape and substrate rigidity both regulate cell stiffness. Biophys. J. 100:L25–27 [Google Scholar]
  143. Thomas W, Forero M, Yakovenko O, Nilsson L, Vicini P. 137a.  et al. 2006. Catch-bond model derived from allostery explains force-activated bacterial adhesion. Biophys. J. 90:753–64 [Google Scholar]
  144. Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV. 138.  2002. Bacterial adhesion to target cells enhanced by shear force. Cell 109:913–23 [Google Scholar]
  145. Tondon A, Hsu H-J, Kaunas R. 139.  2012. Dependence of cyclic stretch-induced stress fiber reorientation on stretch waveform. J. Biomech. 45:728–35 [Google Scholar]
  146. Trappmann B, Gautrot JE, Connelly JT, Strange DGT, Li Y. 139a.  et al. 2012. Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 11:642–49 [Google Scholar]
  147. Vogel V, Sheetz M. 140.  2006. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7:265–75 [Google Scholar]
  148. Wang H, Ji B, Liu XS, Guo XE, Huang Y, Hwang K-C. 141.  2012. Analysis of microstructural and mechanical alterations of trabecular bone in a simulated three-dimensional remodeling process. J. Biomech. 45:2417–25 [Google Scholar]
  149. Wang H, Ji B, Liu XS, van Oers RFM, Guo XE. 142.  et al. 2014. Osteocyte-viability-based simulations of trabecular bone loss and recovery in disuse and reloading. Biomech. Model. Mechanobiol. 13:153–66 [Google Scholar]
  150. Wang JH, Goldschmidt-Clermont P, Wille J, Yin FC. 143.  2001. Specificity of endothelial cell reorientation in response to cyclic mechanical stretching. J. Biomech. 34:1563–72 [Google Scholar]
  151. Wang N, Naruse K, Stamenovic D, Fredberg JJ, Mijailovich SM. 144.  et al. 2001. Mechanical behavior in living cells consistent with the tensegrity model. PNAS 98:7765–70 [Google Scholar]
  152. Wang N, Tolić-Nørrelykke IM, Chen J, Mijailovich SM, Butler JP. 145.  et al. 2002. Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Physiol. Cell Physiol. 282:C606–16 [Google Scholar]
  153. Weng S, Fu J. 146.  2011. Synergistic regulation of cell function by matrix rigidity and adhesive pattern. Biomaterials 32:9584–93 [Google Scholar]
  154. Wolfenson H, Henis YI, Geiger B, Bershadsky AD. 147.  2009. The heel and toe of the cell's foot: a multifaceted approach for understanding the structure and dynamics of focal adhesions. Cell Motil. Cytoskelet. 66:1017–29 [Google Scholar]
  155. Wozniak MA, Chen CS. 148.  2009. Mechanotransduction in development: a growing role for contractility. Nat. Rev. Microbiol. 10:34–43 [Google Scholar]
  156. Xiao T, Takagi J, Coller BS, Wang J-H, Springer TA. 149.  2004. Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature 432:59–67 [Google Scholar]
  157. Yu C-H, Law JBK, Suryana M, Low HY, Sheetz MP. 149a.  2011. Early integrin binding to Arg-Gly-Asp peptide activates actin polymerization and contractile movement that stimulates outward translocation. PNAS 108:20585–90 [Google Scholar]
  158. Zaidel-Bar R, Itzkovitz S, Ma'ayan A, Iyengar R, Geiger B. 150.  2007. Functional atlas of the integrin adhesome. Nat. Cell Biol. 9:858–67 [Google Scholar]
  159. Zamir E, Katz BZ, Aota S, Yamada KM, Geiger B, Kam Z. 151.  1999. Molecular diversity of cell-matrix adhesions. J. Cell Sci. 112:1655–69 [Google Scholar]
  160. Zamir E, Katz M, Posen Y, Erez N, Yamada KM. 152.  et al. 2000. Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nat. Cell Biol. 2:191–96 [Google Scholar]
  161. Zhong Y, He S, Dong C, Ji B, Hu G. 153.  2014. Cell polarization energy and its implications for cell migration. C. R. Mec. 342:334–46 [Google Scholar]
  162. Zhong Y, He S, Ji B. 154.  2012. Mechanics in mechanosensitivity of cell adhesion and its roles in cell migration. Int. J. Comput. Mater. Sci. Eng. 1:1250032 [Google Scholar]
  163. Zhong Y, Ji B. 155.  2013. Impact of cell shape on cell migration behavior on elastic substrate. Biofabrication 5:015011 [Google Scholar]
  164. Zhong Y, Ji B. 156.  2014. How do cells produce and regulate the driving force in the process of migration?. Eur. Phys. J. Special Top. 223:1373–90 [Google Scholar]
  165. Zhong Y, Kong D, Dai L, Ji B. 157.  2011. Frequency-dependent focal adhesion instability and cell reorientation under cyclic substrate stretching. Cell. Mol. Bioeng. 4:442–56 [Google Scholar]
  166. Zhu C, Lou J, McEver RP. 158.  2005. Catch bonds: physical models, structural bases, biological function and rheological relevance. Biorheology 42:443–62 [Google Scholar]
  167. Ziegler WH, Gingras AR, Critchley DR, Emsley J. 159.  2008. Integrin connections to the cytoskeleton through talin and vinculin. Biochem. Soc. Trans. 36:235–39 [Google Scholar]
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