Mechanical cues direct focal adhesion dynamics

Progress in Molecular Biology and Translational Science

Volumn 126, Issue , 2014, Pages 103-134

  Haase, Kristina ^a   Al Rekabi, Zeinab ^a,b   Pelling, Andrew E ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b University of Washington   (United States)

Author keywords

Atomic force microscopy; Cytoskeletal strain; Focal adhesions; Mechanosensing; Traction force microscopy

Indexed keywords

ACTIN; ALPHA INTEGRIN; ARGINYLGLYCYLASPARTIC ACID; BETA INTEGRIN; CELL PROTEIN; FOCAL ADHESION KINASE; GOLD NANOPARTICLE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; MYOSIN LIGHT CHAIN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE SHP; QUANTUM DOT; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE; RHO KINASE; SCLEROPROTEIN; VINCULIN; ZYXIN;

ACTIN POLYMERIZATION; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL CYCLE; CELL MIGRATION; CELL SHAPE; CELL SPREADING; CELL STIMULATION; CYTOSKELETON; ELASTICITY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; FOCAL ADHESION; FORCE; HUMAN; HYDROGEL; MACROMOLECULE; MECHANICAL STIMULATION; MICROENVIRONMENT; MICROSCOPY; MUSCLE CONTRACTION; NONHUMAN; PHASE CONTRAST MICROSCOPY; PRIORITY JOURNAL; STIMULUS RESPONSE; STRESS FIBER; STRESS STRAIN RELATIONSHIP; TURNOVER TIME; ANIMAL; ASSOCIATION; METABOLISM;

ANIMALS; CUES; ELASTICITY; FOCAL ADHESIONS; HUMANS; MICROSCOPY, ATOMIC FORCE;

EID: 84905190421     PISSN: 18771173     EISSN: 18780814     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394624-9.00005-1     Document Type: Chapter

References (139)

1. 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)
2. A. Buxboim, I.L. Ivanovska, and D.E. Discher Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells "feel" outside and in? J Cell Sci 123 3 2010 297 308
3. P.A. Janmey, and R.T. Miller Mechanisms of mechanical signaling in development and disease J Cell Sci 124 1 2011 9 18
4. P.A. Janmey, and D.A. Weitz Dealing with mechanics: mechanisms of force transduction in cells Trends Biochem Sci 29 7 2004 364 370 (Pubitemid 38968753)
5. L. Guolla, M. Bertrand, K. Haase, and A.E. Pelling Force transduction and strain dynamics in actin stress fibres in response to nanonewton forces J Cell Sci 125 3 2012 603 613
6. Z. Al-Rekabi, and A.E. Pelling Cross talk between matrix elasticity and mechanical force regulates myoblast traction dynamics Phys Biol 10 6 2013 066003
7. M.L. Gardel, B. Sabass, L. Ji, G. Danuser, U.S. Schwarz, and C.M. Waterman Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed J Cell Biol 183 6 2008 999 1005
8. N. Huebsch, P.R. Arany, and A.S. Mao et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate Nat Mater 9 6 2010 518 526
9. S. Munevar, Y.L. 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)
10. S.K. Mitra, D.A. Hanson, and D.D. Schlaepfer Focal adhesion kinase: in command and control of cell motility Nat Rev Mol Cell Biol 6 1 2005 56 68 (Pubitemid 40064899)
11. B. Geiger, A. Bershadsky, R. Pankov, and K.M. Yamada Transmembrane extracellular matrix-cytoskeleton crosstalk Nat Rev Mol Cell Biol 2 11 2001 793 805 (Pubitemid 33674080)
12. 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 881 887 (Pubitemid 34286117)
13. R. McBeath, D.M. Pirone, C.M. Nelson, K. Bhadriraju, and C.S. Chen Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev Cell 6 4 2004 483 495 (Pubitemid 38456178)
14. A.Y. Alexandrova, K. Arnold, and S. Schaub et al. Comparative dynamics of retrograde actin flow and focal adhesions: formation of nascent adhesions triggers transition from fast to slow flow PLoS ONE 3 9 2008 e3234 10.1371/journal.pone.0003234
15. S.V. Plotnikov, A.M. Pasapera, B. Sabass, and C.M. Waterman Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration Cell 151 7 2012 1513 1527
16. H. Wolfenson, A. Bershadsky, Y.I. Henis, and B. Geiger Actomyosin-generated tension controls the molecular kinetics of focal adhesions J Cell Sci 124 9 2011 1425 1432
17. K.A. Beningo, K. Hamao, M. Dembo, Y.L. Wang, and H. Hosoya Traction forces of fibroblasts are regulated by the Rho-dependent kinase but not by the myosin light chain kinase Arch Biochem Biophys 456 2 2006 224 231 (Pubitemid 44880290)
18. B. Geiger, J.P. Spatz, and A.D. Bershadsky Environmental sensing through focal adhesions Nat Rev Mol Cell Biol 10 1 2009 21 33
19. P.P. Provenzano, and P.J. Keely Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling J Cell Sci 124 8 2011 1195 1205
20. T.A. Ulrich, E.M.D. Pardo, and S. Kumar The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells Cancer Res 69 10 2009 4167 4174
21. G. Maheshwari, G. Brown, D.A. Lauffenburger, A. Wells, and L.G. Griffith Cell adhesion and motility depend on nanoscale RGD clustering J Cell Sci 113 10 2000 1677 1686 (Pubitemid 30333117)
22. J.V. Small, B. Geiger, I. Kaverina, and A. Bershadsky How do microtubules guide migrating cells? Nat Rev Mol Cell Biol 3 12 2002 957 964 (Pubitemid 35477373)
23. E. Hadjipanayi, V. Mudera, and R.A. Brown Guiding cell migration in 3D: a collagen matrix with graded directional stiffness Cell Motil Cytoskeleton 66 3 2009 121 128
24. M. Guvendiren, and J.A. Burdick The control of stem cell morphology and differentiation by hydrogel surface wrinkles Biomaterials 31 25 2010 6511 6518
25. 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)
26. H.B. Wang, and Y.L. Wang Substrate flexibility regulates growth and apoptosis of normal but not h-ras-transformed cells Mol Biol Cell 10 1999 66a
27. H.B. Wang, M. Dembo, and Y.L. Wang Substrate flexibility regulates growth and apoptosis of normal but not transformed cells Am J Physiol Cell Physiol 279 5 2000 C1345 C1350
28. K. Burridge, K. Fath, T. Kelly, G. Nuckolls, and C. Turner Focal adhesions - transmembrane junctions between the extracellular-matrix and the cytoskeleton Annu Rev Cell Biol 4 1988 487 525 (Pubitemid 19139264)
29. 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 858 868
30. R.W. Tilghman, and J.T. Parsons Focal adhesion kinase as a regulator of cell tension in the progression of cancer Semin Cancer Biol 18 1 2008 45 52 (Pubitemid 350266368)
31. G. Giannone, and M.P. Sheetz Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways Trends Cell Biol 16 4 2006 213 223
32. A. Nayal, D.J. Webb, and A.F. Horwitz Talin: an emerging focal point of adhesion dynamics Curr Opin Cell Biol 16 1 2004 94 98 (Pubitemid 38368158)
33. S. Ghassemi, G. Meacci, and S.M. Liu et al. Cells test substrate rigidity by local contractions on submicrometer pillars Proc Natl Acad Sci USA 109 14 2012 5328 5333
34. K.A. Kilian, B. Bugarija, B.T. Lahn, and M. Mrksich Geometric cues for directing the differentiation of mesenchymal stem cells Proc Natl Acad Sci USA 107 11 2010 4872 4877
35. S.A. Ruiz, and C.S. Chen Emergence of patterned stem cell differentiation within multicellular structures Stem Cells 26 11 2008 2921 2927
36. G. Le Saux, A. Magenau, and K. Gunaratnam et al. Spacing of integrin ligands influences signal transduction in endothelial cells Biophys J 101 4 2011 764 773
37. S.P. Massia, and J.A. Hubbell An Rgd spacing of 440 nm is sufficient for integrin alpha-V-beta-3-mediated fibroblast spreading and 140 nm for focal contact and stress fiber formation J Cell Biol 114 5 1991 1089 1100 (Pubitemid 21909870)
38. 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)
39. D.S.W. Benoit, and K.S. Anseth The effect on osteoblast function of colocalized RGD and PHSRN epitopes on PEG surfaces Biomaterials 26 25 2005 5209 5220 (Pubitemid 40387843)
40. P. Kim, D.H. Kim, and B. Kim et al. Fabrication of nanostructures of polyethylene glycol for applications to protein adsorption and cell adhesion Nanotechnology 16 10 2005 2420 2426 (Pubitemid 41376190)
41. U. Hersel, C. Dahmen, and H. Kessler RGD modified polymers: biomaterials for stimulated cell adhesion and beyond Biomaterials 24 24 2003 4385 4415 (Pubitemid 36960136)
42. E.J. Tocce, A.H. Broderick, and K.C. Murphy et al. Functionalization of reactive polymer multilayers with RGD and an antifouling motif: RGD density provides control over human corneal epithelial cell-substrate interactions J Biomed Mater Res A 100A 1 2012 84 93
43. X.Z. Shu, K. Ghosh, and Y.C. Liu et al. Attachment and spreading of fibroblasts on an RGD peptide-modified injectable hyaluronan hydrogel J Biomed Mater Res A 68A 2 2004 365 375 (Pubitemid 38524731)
44. B. Ananthanarayanan, L. Little, D.V. Schaffer, K.E. Healy, and M. Tirrell Neural stem cell adhesion and proliferation on phospholipid bilayers functionalized with RGD peptides Biomaterials 31 33 2010 8706 8715
45. C.H. Yu, J.B.K. Law, M. Suryana, H.Y. Low, and M.P. Sheetz Early integrin binding to Arg-Gly-Asp peptide activates actin polymerization and contractile movement that stimulates outward translocation Proc Natl Acad Sci USA 108 51 2011 20585 20590
46. C.S. Chen, M. Mrksich, S. Huang, G.M. Whitesides, and D.E. Ingber Geometric control of cell life and death Science 276 5317 1997 1425 1428 (Pubitemid 27235413)
47. M. Arnold, E.A. Cavalcanti-Adam, and R. Glass et al. Activation of integrin function by nanopatterned adhesive interfaces Chemphyschem 5 3 2004 383 388
48. F.Z. Jiang, H. Horber, J. Howard, and D.J. Muller Assembly of collagen into microribbons: effects of pH and electrolytes J Struct Biol 148 3 2004 268 278 (Pubitemid 39441364)
49. C. Deng, X.S. Chen, H.J. Yu, J. Sun, T.C. Lu, and X.B. Jing A biodegradable triblock copolymer poly(ethylene glycol)-b-poly(l-lactide)-b- poly(l-lysine): synthesis, self-assembly and RGD peptide modification Polymer 48 1 2007 139 149 (Pubitemid 44918032)
50. Y.L. Huang, and N.T. Nguyen A polymeric cell stretching device for real-time imaging with optical microscopy Biomed Microdevices 15 6 2013 1043 1054
51. D. Tremblay, S. Chagnon-Lessard, M. Mirzaei, A.E. Pelling, and M. Godin A microscale anisotropic biaxial cell stretching device for applications in mechanobiology Biotechnol Lett 16 2013 16
52. D. Wang, Y.Y. Xie, B. Yuan, J. Xu, P.Y. Gong, and X.Y. Jiang A stretching device for imaging real-time molecular dynamics of live cells adhering to elastic membranes on inverted microscopes during the entire process of the stretch Integr Biol (UK) 2 5-6 2010 288 293
53. S. Khetan, M. Guvendiren, W.R. Legant, D.M. Cohen, C.S. Chen, and J.A. Burdick Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels Nat Mater 12 5 2013 458 465
54. G.P. Giannone, G. Jiang, D. Critchley, and M.P. Sheetz Talin-1 is a critical component in early force-dependent reinforcement of integrin-cytoskeleton connections Mol Biol Cell 13 2002 350a
55. E. Montanez, S. Ussar, and M. Schifferer et al. Kindlin-2 controls bidirectional signaling of integrins Gene Dev 22 10 2008 1325 1330 (Pubitemid 351717522)
56. M. Moser, B. Nieswandt, S. Ussar, M. Pozgajova, and R. Fassler Kindlin-3 is essential for integrin activation and platelet aggregation Nat Med 14 3 2008 325 330 (Pubitemid 351347914)
57. Y.Q. Ma, J. Qin, C.Y. Wu, and E.F. Plow Kindlin-2 (Mig-2): a co-activator of beta(3) integrins J Cell Biol 181 3 2008 439 446 (Pubitemid 351645034)
58. F. Ye, B.G. Petrich, and P. Anekal et al. The mechanism of kindlin-mediated activation of integrin alpha IIb beta 3 Curr Biol 23 22 2013 2288 2295
59. J.D. Humphries, P. Wang, C. Streuli, B. Geiger, M.J. Humphries, and C. Ballestrem Vinculin controls focal adhesion formation by direct interactions with talin and actin J Cell Biol 179 5 2007 1043 1057 (Pubitemid 350223497)
60. J.V. Small, T. Stradal, E. Vignal, and K. Rottner The lamellipodium: where motility begins Trends Cell Biol 12 3 2002 112 120 (Pubitemid 34164650)
61. H. Shroff, C.G. Galbraith, J.A. Galbraith, and E. Betzig Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics Nat Methods 5 5 2008 417 423 (Pubitemid 351619100)
62. H. Shroff, C.G. Galbraith, and J.A. Galbraith et al. Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes (vol 104, pg 20308, 2007) Proc Natl Acad Sci USA 105 39 2008 15220
63. A. Ponti, M. Machacek, S.L. Gupton, C.M. Waterman-Storer, and G. Danuser Two distinct actin networks drive the protrusion of migrating cells Science 305 5691 2004 1782 1786 (Pubitemid 39249647)
64. P. Vallotton, G. Danuser, S. Bohnet, J.J. Meister, and A.B. Verkhovsky Tracking retrograde flow in keratocytes: news from the front Mol Biol Cell 16 3 2005 1223 1231 (Pubitemid 40349559)
65. W.H. Guo, and Y.L. Wang Retrograde fluxes of focal adhesion proteins in response to cell migration and mechanical signals Mol Biol Cell 18 11 2007 4519 4527
66. G. Giannone, B.J. Dubin-Thaler, and O. Rossier et al. Lamellipodial actin mechanically links myosin activity with adhesion-site formation Cell 128 3 2007 561 575 (Pubitemid 46198897)
67. B. Geiger A role for p130Cas in mechanotransduction Cell 127 5 2006 879 881 (Pubitemid 44792262)
68. 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)
69. J.T. Parsons Focal adhesion kinase: the first ten years J Cell Sci 116 8 2003 1409 1416 (Pubitemid 36527488)
70. G. von Wichert, B. Haimovich, G.S. Feng, and M.P. Sheetz Force-dependent integrin-cytoskeleton linkage formation requires downregulation of focal complex dynamics by Shp2 EMBO J 22 19 2003 5023 5035 (Pubitemid 37222023)
71. A.W. Stoker Protein tyrosine phosphatases and signalling J Endocrinol 185 1 2005 19 33 (Pubitemid 40585064)
72. V.J. Fincham, and M.C. Frame The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility EMBO J 17 1 1998 81 92 (Pubitemid 28041050)
73. M. Schober, S. Raghavan, and M. Nikolova et al. Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics J Cell Biol 176 5 2007 667 680 (Pubitemid 46333981)
74. D.A. Hsia, S.K. Mitra, and C.R. Hauck et al. Differential regulation of cell motility and invasion by FAK J Cell Biol 160 5 2003 753 767 (Pubitemid 36298270)
75. D.J. Webb, K. Donais, and L.A. Whitmore et al. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly Nat Cell Biol 6 2 2004 154
76. 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
77. J.A. Broussard, D.J. Webb, and I. Kaverina Asymmetric focal adhesion disassembly in motile cells Curr Opin Cell Biol 20 1 2008 85 90
78. D.J. Webb, J.T. Parsons, and A.F. Horwitz Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again Nat Cell Biol 4 4 2002 E97 E100
79. A. Huttenlocher, and A.R. Horwitz Integrins in cell migration Cold Spring Harb Perspect Biol 3 9 2011 10.1101/cshperspect.a005074 a005074.
80. M. Vicente-Manzanares, M.A. Koach, L. Whitmore, M.L. Lamers, and A.F. Horwitz Segregation and activation of myosin IIB creates a rear in migrating cells J Cell Biol 183 3 2008 543 554
81. M. Vicente-Manzanares, X.F. Ma, R.S. Adelstein, and A.R. Horwitz Non-muscle myosin II takes centre stage in cell adhesion and migration Nat Rev Mol Cell Biol 10 11 2009 778 790
82. C.T. Mierke The role of vinculin in the regulation of the mechanical properties of cells Cell Biochem Biophys 53 3 2009 115 126
83. M.A. Wozniak, K. Modzelewska, L. Kwong, and P.J. Keely Focal adhesion regulation of cell behavior BBA Mol Cell Res 1692 2-3 2004 103 119 (Pubitemid 38891769)
84. N. Endlich, C.A. Otey, W. Kriz, and K. Endlich Movement of stress fibers away from focal adhesions identifies focal adhesions as sites of stress fiber assembly in stationary cells Cell Motil Cytoskeleton 64 12 2007 966 976 (Pubitemid 350197283)
85. S. Pellegrin, and H. Mellor Actin stress fibres J Cell Sci 120 20 2007 3491 3499
86. P. Hotulainen, and P. Lappalainen Stress fibers are generated by two distinct actin assembly mechanisms in motile cells J Cell Biol 173 3 2006 383 394
87. M. Thery, A. Pepin, E. Dressaire, Y. Chen, and M. Bornens Cell distribution of stress fibres in response to the geometry of the adhesive environment Cell Motil Cytoskeleton 63 6 2006 341 355 (Pubitemid 43787719)
88. N. Tapon, and A. Hall Rho, Rac and Cdc42 GTPases regulate the organization of the actin cytoskeleton Curr Opin Cell Biol 9 1 1997 86 92 (Pubitemid 27065113)
89. N. Iwaki, K. Karatsu, and M. Miyamoto Role of guanine nucleotide exchange factors for Rho family GTPases in the regulation of cell morphology and actin cytoskeleton in fission yeast Biochem Biophys Res Commun 312 2 2003 414 420 (Pubitemid 37445188)
90. R. Begum, M.S.A. Nur-E-Kamal, and M.A. Zaman The role of Rho GTPases in the regulation of the rearrangement of actin cytoskeleton and cell movement Exp Mol Med 36 4 2004 358 366 (Pubitemid 39279532)
91. S.T. Sit, and E. Manser Rho GTPases and their role in organizing the actin cytoskeleton J Cell Sci 124 5 2011 679 683
92. S. Lee, A. Zeiger, J.M. Maloney, M. Kotecki, K.J. Van Vliet, and I.M. Herman Pericyte actomyosin-mediated contraction at the cell-material interface can modulate the microvascular niche J Phys-Condens Matter 22 19 2010 11 10.1088/0953-8984/22/19/194115
93. E.J. Ezratty, M.A. Partridge, and G.G. Gundersen Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase Nat Cell Biol 7 6 2005 U515 U581
94. P. Kunda, A.E. Pelling, T. Liu, and B. Baum Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis Curr Biol 18 2 2008 91 101
95. L. Chartier, L.L. Rankin, and R.E. Allen et al. Calyculin-a Increases the Level of Protein-Phosphorylation and Changes the Shape of 3t3 Fibroblasts Cell Motil Cytoskeleton 18 1 1991 26 40
96. A. Rape, W.H. Guo, and Y.L. Wang Microtubule depolymerization induces traction force increase through two distinct pathways J Cell Sci 124 24 2011 4233 4240
97. Z. Al-Rekabi, K. Haase, and A.E. Pelling Microtubules mediate changes in membrane cortical elasticity during contractile activation Exp Cell Res 322 1 10 March 2014 21 29
98. R.M. Hochmuth Micropipette aspiration of living cells J Biomech 33 1 2000 15 22
99. N. Wang, and D.E. Ingber Probing transmembrane mechanical coupling and cytomechanics using magnetic twisting cytometry Biochem Cell Biol 73 7-8 1995 327 335
100. J. Guck, R. Ananthakrishnan, H. Mahmood, T.J. Moon, C.C. Cunningham, and J. Kas The optical stretcher: a novel laser tool to micromanipulate cells Biophys J 81 2 2001 767 784 (Pubitemid 32721451)
101. V.M. Laurent, S. Henon, and E. Planus et al. Assessment of mechanical properties of adherent living cells by bead micromanipulation: comparison of magnetic twisting cytometry vs optical tweezers J Biomech Eng T ASME 124 4 2002 408 421
102. T.D. Brown Techniques for mechanical stimulation of cells in vitro: a review J Biomech 33 1 2000 3 14
103. A. Ashkin, J.M. Dziedzic, and T. Yamane Optical trapping and manipulation of single cells using infrared-laser beams Nature 330 6150 1987 769 771
104. B.J. Haupt, A.E. Pelling, and M.A. Horton Integrated confocal and scanning probe microscopy for biomedical research Sci World J 6 2006 1609 1618 (Pubitemid 46045430)
105. K. Haase, and A.E. Pelling Resiliency of the plasma membrane and actin cortex to large-scale deformation Cytoskeleton 70 9 2013 494 514
106. M. Radmacher, M. Fritz, C.M. Kacher, J.P. Cleveland, and P.K. Hansma Measuring the viscoelastic properties of human platelets with the atomic force microscope Biophys J 70 1 1996 556 567 (Pubitemid 26021495)
107. M. Radmacher Measuring the elastic properties of biological samples with the AFM IEEE Eng Med Biol 16 2 1997 47 57 (Pubitemid 27133548)
108. H. Haga, S. Sasaki, K. Kawabata, E. Ito, T. Ushiki, and T. Sambongi Elasticity mapping of living fibroblasts by AFM and immunofluorescence observation of the cytoskeleton Ultramicroscopy 82 1-4 2000 253 258 (Pubitemid 30070109)
109. A. Trache, and S.M. Lim Integrated microscopy for real-time imaging of mechanotransduction studies in live cells J Biomed Opt 14 3 2009 10.1117/1.3155517 034024-034024-13
110. Y. Ueki, Y. Uda, N. Sakamoto, and M. Sato Measurements of strain on single stress fibers in living endothelial cells induced by fluid shear stress Biochem Biophys Res Commun 395 3 2010 441 446
111. J. Colombelli, A. Besser, and H. Kress et al. Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization J Cell Sci 122 10 2009 1665 1679
112. S. Kumar, I.Z. Maxwell, and A. Heisterkamp et al. Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics Biophys J 90 10 2006 3762 3773
113. C. Chen, R. Krishnan, and E.H. Zhou et al. Fluidization and resolidification of the human bladder smooth muscle cell in response to transient stretch PLoS One 5 8 2010 e12035 10.1371/journal.pone.0012035
114. E. Tzima, M.A. del Pozo, S.J. Shattil, S. Chien, and M.A. Schwartz Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment EMBO J 20 17 2001 4639 4647 (Pubitemid 32848617)
115. V. Vogel, and M. Sheetz Local force and geometry sensing regulate cell functions Nat Rev Mol Cell Biol 7 4 2006 265 275
116. D.E. Discher, P. Janmey, and Y.L. Wang Tissue cells feel and respond to the stiffness of their substrate Science 310 5751 2005 1139 1143 (Pubitemid 41681732)
117. J.P. Winer, P.A. Janmey, M.E. McCormick, and M. Funaki Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli Tissue Eng A 15 1 2009 147 154
118. A.W. Holle, and A.J. Engler More than a feeling: discovering, understanding, and influencing mechanosensing pathways Curr Opin Biotechnol 22 5 2011 648 654
119. U.S. Schwarz, and M.L. Gardel United we stand - integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction J Cell Sci 125 13 2012 3051 3060
120. D.J. Modulevsky, D. Tremblay, C. Gullekson, N.V. Bukoresthliev, and A.E. Pelling The physical interaction of myoblasts with the microenvironment during remodeling of the cytoarchitecture PLoS One 7 9 2012 e45329 10.1371/journal. pone.0045329
121. A.M. Collinsworth, S. Zhang, W.E. Kraus, and G.A. Truskey Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation Am J Physiol Cell Phys 283 4 2002 C1219 C1227
122. A.B. Mathur, A.M. Collinsworth, W.M. Reichert, W.E. Kraus, and G.A. Truskey Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy J Biomech 34 12 2001 1545 1553 (Pubitemid 33041370)
123. L.R. Nyland, and D.W. Maughan Morphology and transverse stiffness of Drosophila myofibrils measured by atomic force microscopy Biophys J 78 3 2000 1490 1497 (Pubitemid 30141573)
124. I.V. Ogneva Transversal stiffness of fibers and desmin content in leg muscles of rats under gravitational unloading of various durations J Appl Physiol 109 6 2010 1702 1709
125. A.J. Engler, M.A. Griffin, S. Sen, C.G. Bonnetnann, H.L. Sweeney, and D.E. Discher Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments J Cell Biol 166 6 2004 877 887 (Pubitemid 39249838)
126. T. Akimoto, T. Uchida, S. Miyaki, H. Akaogi, T. Tateishi, and T. Fukubayashi Effect of mechanical stretch on TGF-beta 1 expression of C2C12 myogenic cells Mater Sci Eng C Biol Sci 24 3 2004 387 389 (Pubitemid 38464318)
127. S.H. Kook, H.J. Lee, and W.T. Chung et al. Cyclic mechanical stretch stimulates the proliferation of C2C12 myoblasts and inhibits their differentiation via prolonged activation of p38 MAPK Mol Cells 25 4 2008 479 486
128. J.S. Otis, T.J. Burkholder, and G.K. Pavlath Stretch-induced myoblast proliferation is dependent on the COX2 pathway Exp Cell Res 310 2 2005 417 425 (Pubitemid 41457344)
129. M. Zhan, B.W. Jin, S.E. Chen, J.M. Reecy, and Y.P. Li TACE release of TNF-alpha mediates mechanotransduction-induced activation of p38 MAPK and myogenesis J Cell Sci 120 4 2007 692 701 (Pubitemid 46437903)
130. M.H. Parker, P. Seale, and M.A. Rudnicki Looking back to the embryo: defining transcriptional networks in adult myogenesis Nat Rev Genet 4 7 2003 497 507 (Pubitemid 36781341)
131. J. Fu, Y.K. Wang, and M.T. Yang et al. Mechanical regulation of cell function with geometrically modulated elastomeric substrates Nat Methods 7 9 2010 733 736
132. S.J. Han, K.S. Bielawski, L.H. Ting, M.L. Rodriguez, and N.J. Sniadecki Decoupling substrate stiffness, spread area, and micropost density: a close spatial relationship between traction forces and focal adhesions Biophys J 103 4 2012 640 648
133. A.C. Nag, and J.D. Foster Myogenesis in adult mammalian skeletal-muscle in vitro J Anat 132 Jan 1981 1 18 (Pubitemid 11210849)
134. Y.F. Yang, A. Creeer, B. Jemiolo, and S. Trappe Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle J Appl Physiol 98 5 2005 1745 1752 (Pubitemid 40570785)
135. D.F. Goldspink, J. Easton, S.K. Winterburn, P.E. Williams, and G.E. Goldspink The role of passive stretch and repetitive electrical-stimulation in preventing skeletal-muscle atrophy while reprogramming gene-expression to improve fatigue resistance J Cardiac Surg 6 1 1991 218 224
136. D.F. Goldspink, V.M. Cox, and S.K. Smith et al. Muscle growth in response to mechanical stimuli Am J Physiol Endocrinol Metab 268 2 1995 E288 E297
137. H.H. Vandenburgh, S. Hatfaludy, P. Karlisch, and J. Shansky Skeletal-muscle growth is stimulated by intermittent stretch-relaxation in tissue-culture Am J Physiol 256 3 1989 C674 C682
138. A.M. Collinsworth, C.E. Torgan, S.N. Nagda, R.J. Rajalingam, W.E. Kraus, and G.A. Truskey Orientation and length of mammalian skeletal myocytes in response to a unidirectional stretch Cell Tissue Res 302 2 2000 243 251
139. H.H. Vandenburgh, S. Swasdison, and P. Karlisch Computer-aided mechanogenesis of skeletal-muscle organs from single cells-in vitro FASEB J 5 13 1991 2860 2867 (Pubitemid 21892859)