From mechanical force to RhoA activation

Biochemistry

Volumn 51, Issue 38, 2012, Pages 7420-7432

  Lessey, Elizabeth C ^a   Guilluy, Christophe ^a   Burridge, Keith ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CYTOSKELETON; CELL ADHESION MOLECULES; CELL MATRIX; CELL-CELL INTERACTION; CYTOSKELETAL; MECHANICAL FORCE; POSITIVE FEEDBACK LOOP; SIGNALING EVENTS; SIGNALING PATHWAYS;

CELLS; CYTOLOGY; GENE EXPRESSION; PROTEINS;

MECHANICAL ENGINEERING;

INTEGRIN; MYOSIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN FILAMENT; ARTICLE; CELL ADHESION; CELL INTERACTION; ENZYME ACTIVATION; FORCE; GENE EXPRESSION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; SHEAR STRESS;

CELL ADHESION MOLECULES; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; GENE EXPRESSION; HUMANS; NEOPLASMS; RHOA GTP-BINDING PROTEIN;

EID: 84866680424     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300758e     Document Type: Article

References (151)

1. Tomasek, J. J., Gabbiani, G., Hinz, B., Chaponnier, C., and Brown, R. A. (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling Nat. Rev. Mol. Cell Biol. 3, 349-363
2. Curtis, A. S. and Seehar, G. M. (1978) The control of cell division by tension or diffusion Nature 274, 52-53
3. Vandenburgh, H. and Kaufman, S. (1979) In vitro model for stretch-induced hypertrophy of skeletal muscle Science 203, 265-268
4. Bray, D. (1979) Mechanical tension produced by nerve cells in tissue culture J. Cell Sci. 37, 391-410
5. Bray, D. (1984) Axonal growth in response to experimentally applied mechanical tension Dev. Biol. 102, 379-389
6. Harris, A. K., Wild, P., and Stopak, D. (1980) Silicone rubber substrata: A new wrinkle in the study of cell locomotion Science 208, 177-179
7. Harris, A. K., Stopak, D., and Wild, P. (1981) Fibroblast traction as a mechanism for collagen morphogenesis Nature 290, 249-251
8. Kolega, J. (1986) Effects of mechanical tension on protrusive activity and microfilament and intermediate filament organization in an epidermal epithelium moving in culture J. Cell Biol. 102, 1400-1411
9. Bershadsky, A., Kozlov, M., and Geiger, B. (2006) Adhesion-mediated mechanosensitivity: A time to experiment, and a time to theorize Curr. Opin. Cell Biol. 18, 472-481
10. Vogel, V. and Sheetz, M. (2006) Local force and geometry sensing regulate cell functions Nat. Rev. Mol. Cell Biol. 7, 265-275
11. Mammoto, A., Mammoto, T., and Ingber, D. E. (2008) Rho signaling and mechanical control of vascular development Curr. Opin. Hematol. 15, 228-234
12. Eyckmans, J., Boudou, T., Yu, X., and Chen, C. S. (2011) A hitchhiker's guide to mechanobiology Dev. Cell 21, 35-47
13. Tzima, E. (2006) Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response Circ. Res. 98, 176-185
14. Hoffman, B. D., Grashoff, C., and Schwartz, M. A. (2011) Dynamic molecular processes mediate cellular mechanotransduction Nature 475, 316-323
15. Hahn, C. and Schwartz, M. A. (2009) Mechanotransduction in vascular physiology and atherogenesis Nat. Rev. Mol. Cell Biol. 10, 53-62
16. Thompson, W. R., Rubin, C. T., and Rubin, J. (2012) Mechanical regulation of signaling pathways in bone Gene 503, 179-193
17. Alberts, B. J., Lewis, J., Raff, M., Roberts, K., and Walter, P. (2007) Molecular Biology of the Cell, 5th ed., Garland Science.
18. Ridley, A. J. and Hall, A. (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors Cell 70, 389-399
19. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D., and Hall, A. (1992) The small GTP-binding protein rac regulates growth factor-induced membrane ruffling Cell 70, 401-410
20. Chrzanowska-Wodnicka, M. and Burridge, K. (1996) Rho-stimulated contractility drives the formation of stress fibers and focal adhesions J. Cell Biol. 133, 1403-1415
21. Jaffe, A. B. and Hall, A. (2005) Rho GTPases: Biochemistry and biology Annu. Rev. Cell Dev. Biol. 21, 247-269
22. Rossman, K. L., Der, C. J., and Sondek, J. (2005) GEF means go: Turning on RHO GTPases with guanine nucleotide-exchange factors Nat. Rev. Mol. Cell Biol. 6, 167-180
23. Bos, J. L., Rehmann, H., and Wittinghofer, A. (2007) GEFs and GAPs: Critical elements in the control of small G proteins Cell 129, 865-877
24. Garcia-Mata, R., Boulter, E., and Burridge, K. (2011) The 'invisible hand': Regulation of RHO GTPases by RHOGDIs Nat. Rev. Mol. Cell Biol. 12, 493-504
25. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., and Kaibuchi, K. (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase) J. Biol. Chem. 271, 20246-20249
26. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J. H., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase) Science 273, 245-248
27. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K., and Narumiya, S. (1999) Signaling from rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase Science 285, 895-898
28. Watanabe, N., Kato, T., Fujita, A., Ishizaki, T., and Narumiya, S. (1999) Cooperation between mDia1 and ROCK in Rho-induced actin reorganization Nat. Cell Biol. 1, 136-143
29. Burridge, K. (1981) Are stress fibres contractile? Nature 294, 691-692
30. Chen, C. S. (2008) Mechanotransduction: A field pulling together? J. Cell Sci. 121, 3285-3292
31. Geiger, B., Spatz, J. P., and Bershadsky, A. D. (2009) Environmental sensing through focal adhesions Nat. Rev. Mol. Cell Biol. 10, 21-33
32. Peng, F., Zhang, B., Ingram, A. J., Gao, B., Zhang, Y., and Krepinsky, J. C. (2010) Mechanical stretch-induced RhoA activation is mediated by the RhoGEF Vav2 in mesangial cells Cell. Signalling 22, 34-40
33. Guilluy, C., Swaminathan, V., Garcia-Mata, R., Timothy O'Brien, E., Superfine, R., and Burridge, K. (2011) The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins Nat. Cell Biol. 13, 724-729
34. Kuo, J. C., Han, X., Hsiao, C. T., Yates Iii, J. R., and Waterman, C. M. (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, 383-393
35. Heck, J. N., Ponik, S. M., Garcia-Mendoza, M. G., Pelhke, C. A., Inman, D. R., Eliceiri, K. W., and Keely, P. J. (2012) Microtubules Regulate GEF-H1 in Response to Extracellular Matrix Stiffness Mol. Biol. Cell 23, 2583-2592
36. Goldyn, A. M., Rioja, B. A., Spatz, J. P., Ballestrem, C., and Kemkemer, R. (2009) Force-induced cell polarisation is linked to RhoA-driven microtubule-independent focal-adhesion sliding J. Cell Sci. 122, 3644-3651
37. Birukova, A. A., Fu, P., Xing, J., Yakubov, B., Cokic, I., and Birukov, K. G. (2010) Mechanotransduction by GEF-H1 as a novel mechanism of ventilator-induced vascular endothelial permeability Am. J. Physiol. 298, L837-L848
38. Liu, Z., Tan, J. L., Cohen, D. M., Yang, M. T., Sniadecki, N. J., Ruiz, S. A., Nelson, C. M., and Chen, C. S. (2010) Mechanical tugging force regulates the size of cell-cell junctions Proc. Natl. Acad. Sci. U.S.A. 107, 9944-9949
39. Brevier, J., Montero, D., Svitkina, T., and Riveline, D. (2008) The asymmetric self-assembly mechanism of adherens junctions: A cellular push-pull unit Phys. Biol. 5, 016005
40. le Duc, Q., Shi, Q., Blonk, I., Sonnenberg, A., Wang, N., Leckband, D., and de Rooij, J. (2010) Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner J. Cell Biol. 189, 1107-1115
41. Aijaz, S., D'Atri, F., Citi, S., Balda, M. S., and Matter, K. (2005) Binding of GEF-H1 to the tight junction-associated adaptor cingulin results in inhibition of Rho signaling and G1/S phase transition Dev. Cell 8, 777-786
42. Benais-Pont, G., Punn, A., Flores-Maldonado, C., Eckert, J., Raposo, G., Fleming, T. P., Cereijido, M., Balda, M. S., and Matter, K. (2003) Identification of a tight junction-associated guanine nucleotide exchange factor that activates Rho and regulates paracellular permeability J. Cell Biol. 160, 729-740
43. Terry, S. J., Zihni, C., Elbediwy, A., Vitiello, E., Leefa Chong San, I. V., Balda, M. S., and Matter, K. (2011) Spatially restricted activation of RhoA signalling at epithelial junctions by p114RhoGEF drives junction formation and morphogenesis Nat. Cell Biol. 13, 159-166
44. Li, G., Du, X., Vass, W. C., Papageorge, A. G., Lowy, D. R., and Qian, X. (2011) Full activity of the deleted in liver cancer 1 (DLC1) tumor suppressor depends on an LD-like motif that binds talin and focal adhesion kinase (FAK) Proc. Natl. Acad. Sci. U.S.A. 108, 17129-17134
45. Liao, Y. C., Shih, Y. P., and Lo, S. H. (2008) Mutations in the focal adhesion targeting region of deleted in liver cancer-1 attenuate their expression and function Cancer Res. 68, 7718-7722
46. Clark, K., Howe, J. D., Pullar, C. E., Green, J. A., Artym, V. V., Yamada, K. M., and Critchley, D. R. (2010) Tensin 2 modulates cell contractility in 3D collagen gels through the RhoGAP DLC1 J. Cell. Biochem. 109, 808-817
47. Kawai, K., Iwamae, Y., Yamaga, M., Kiyota, M., Ishii, H., Hirata, H., Homma, Y., and Yagisawa, H. (2009) Focal adhesion-localization of START-GAP1/DLC1 is essential for cell motility and morphology Genes Cells 14, 227-241
48. Tomar, A., Lim, S. T., Lim, Y., and Schlaepfer, D. D. (2009) A FAK-p120RasGAP-p190RhoGAP complex regulates polarity in migrating cells J. Cell Sci. 122, 1852-1862
49. Arthur, W. T., Petch, L. A., and Burridge, K. (2000) Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism Curr. Biol. 10, 719-722
50. Noren, N. K., Arthur, W. T., and Burridge, K. (2003) Cadherin engagement inhibits RhoA via p190RhoGAP J. Biol. Chem. 278, 13615-13618
51. Arthur, W. T. and Burridge, K. (2001) RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity Mol. Biol. Cell 12, 2711-2720
52. Yang, B., Radel, C., Hughes, D., Kelemen, S., and Rizzo, V. (2011) p190 RhoGTPase-activating protein links the β1 integrin/caveolin-1 mechanosignaling complex to RhoA and actin remodeling Arterioscler., Thromb., Vasc. Biol. 31, 376-383
53. Mammoto, A., Connor, K. M., Mammoto, T., Yung, C. W., Huh, D., Aderman, C. M., Mostoslavsky, G., Smith, L. E., and Ingber, D. E. (2009) A mechanosensitive transcriptional mechanism that controls angiogenesis Nature 457, 1103-1108
54. Omelchenko, T. and Hall, A. (2012) Myosin-IXA Regulates Collective Epithelial Cell Migration by Targeting RhoGAP Activity to Cell-Cell Junctions Curr. Biol. 22, 278-288
55. Guilluy, C., Garcia-Mata, R., and Burridge, K. (2011) Rho protein crosstalk: Another social network? Trends Cell Biol. 21, 718-726
56. Houk, A. R., Jilkine, A., Mejean, C. O., Boltyanskiy, R., Dufresne, E. R., Angenent, S. B., Altschuler, S. J., Wu, L. F., and Weiner, O. D. (2012) Membrane Tension Maintains Cell Polarity by Confining Signals to the Leading Edge during Neutrophil Migration Cell 148, 175-188
57. Worthylake, R. A. and Burridge, K. (2003) RhoA and ROCK promote migration by limiting membrane protrusions J. Biol. Chem. 278, 13578-13584
58. Ohta, Y., Hartwig, J. H., and Stossel, T. P. (2006) FilGAP, a Rho and ROCK-regulated GAP for Rac binds filamin A to control actin remodeling Nat. Cell Biol. 8, 803-814
59. Ehrlicher, A. J., Nakamura, F., Hartwig, J. H., Weitz, D. A., and Stossel, T. P. (2011) Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A Nature 478, 260-263
60. Sanz-Moreno, V., Gadea, G., Ahn, J., Paterson, H., Marra, P., Pinner, S., Sahai, E., and Marshall, C. J. (2008) Rac activation and inactivation control plasticity of tumor cell movement Cell 135, 510-523
61. Boulter, E., Garcia-Mata, R., Guilluy, C., Dubash, A., Rossi, G., Brennwald, P. J., and Burridge, K. (2010) Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1 Nat. Cell Biol. 12, 477-483
62. Ishijima, A., Doi, T., Sakurada, K., and Yanagida, T. (1991) Sub-piconewton force fluctuations of actomyosin in vitro Nature 352, 301-306
63. Molloy, J. E., Burns, J. E., Kendrick-Jones, J., Tregear, R. T., and White, D. C. (1995) Movement and force produced by a single myosin head Nature 378, 209-212
64. Finer, J. T., Simmons, R. M., and Spudich, J. A. (1994) Single myosin molecule mechanics: Piconewton forces and nanometre steps Nature 368, 113-119
65. Tonomura, Y. and Oosawa, F. (1972) Molecular mechanism of contraction Annu. Rev. Biophys. Bioeng. 1, 159-190
66. Lee, J., Leonard, M., Oliver, T., Ishihara, A., and Jacobson, K. (1994) Traction forces generated by locomoting keratocytes J. Cell Biol. 127, 1957-1964
67. Galbraith, C. G. and Sheetz, M. P. (1997) A micromachined device provides a new bend on fibroblast traction forces Proc. Natl. Acad. Sci. U.S.A. 94, 9114-9118
68. Balaban, N. Q., Schwarz, U. S., Riveline, D., Goichberg, P., Tzur, G., Sabanay, I., Mahalu, D., Safran, S., Bershadsky, A., Addadi, L., and Geiger, B. (2001) Force and focal adhesion assembly: A close relationship studied using elastic micropatterned substrates Nat. Cell Biol. 3, 466-472
69. Schwarz, U. S., Balaban, N. Q., Riveline, D., Bershadsky, A., Geiger, B., and Safran, S. A. (2002) Calculation of forces at focal adhesions from elastic substrate data: The effect of localized force and the need for regularization Biophys. J. 83, 1380-1394
70. Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V., and Wang, Y. L. (2001) Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts J. Cell Biol. 153, 881-888
71. Tan, J. L., Tien, J., Pirone, D. M., Gray, D. S., Bhadriraju, K., and Chen, C. S. (2003) Cells lying on a bed of microneedles: An approach to isolate mechanical force Proc. Natl. Acad. Sci. U.S.A. 100, 1484-1489
72. Provenzano, P. P. and Keely, P. J. (2011) Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling J. Cell Sci. 124, 1195-1205
73. Banes, A. J., Gilbert, J., Taylor, D., and Monbureau, O. (1985) A new vacuum-operated stress-providing instrument that applies static or variable duration cyclic tension or compression to cells in vitro J. Cell Sci. 75, 35-42
74. Sumpio, B. E., Banes, A. J., Levin, L. G., and Johnson, G., Jr. (1987) Mechanical stress stimulates aortic endothelial cells to proliferate Journal of Vascular Surgery 6, 252-256
75. Riveline, D., Zamir, E., Balaban, N. Q., Schwarz, U. S., Ishizaki, T., Narumiya, S., Kam, Z., Geiger, B., and Bershadsky, A. D. (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, 1175-1186
76. Wang, N., Butler, J. P., and Ingber, D. E. (1993) Mechanotransduction across the cell surface and through the cytoskeleton Science 260, 1124-1127
77. Choquet, D., Felsenfeld, D. P., and Sheetz, M. P. (1997) Extracellular matrix rigidity causes strengthening of integrin- cytoskeleton linkages Cell 88, 39-48
78. Matthews, B. D., Overby, D. R., Alenghat, F. J., Karavitis, J., Numaguchi, Y., Allen, P. G., and Ingber, D. E. (2004) Mechanical properties of individual focal adhesions probed with a magnetic microneedle Biochem. Biophys. Res. Commun. 313, 758-764
79. Matthews, B. D., Overby, D. R., Mannix, R., and Ingber, D. E. (2006) Cellular adaptation to mechanical stress: Role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels J. Cell Sci. 119, 508-518
80. Glogauer, M. and Ferrier, J. (1998) A new method for application of force to cells via ferric oxide beads Pfluegers Arch. 435, 320-327
81. Zhao, X. H., Laschinger, C., Arora, P., Szaszi, K., Kapus, A., and McCulloch, C. A. (2007) Force activates smooth muscle α-actin promoter activity through the Rho signaling pathway J. Cell Sci. 120, 1801-1809
82. Tim O'Brien, E., Cribb, J., Marshburn, D., Taylor, R. M., II, and Superfine, R. (2008) Chapter 16: Magnetic manipulation for force measurements in cell biology Methods Cell Biol. 89, 433-450
83. Davies, P. F. (1995) Flow-mediated endothelial mechanotransduction Physiol. Rev. 75, 519-560
84. Wojciak-Stothard, B. and Ridley, A. J. (2003) Shear stress-induced endothelial cell polarization is mediated by Rho and Rac but not Cdc42 or PI 3-kinases J. Cell Biol. 161, 429-439
85. Davies, P. F. (2009) Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology Nat. Clin. Pract. Cardiovasc. Med. 6, 16-26
86. Malek, A. M. and Izumo, S. (1994) Molecular aspects of signal transduction of shear stress in the endothelial cell J. Hypertens. 12, 989-999
87. Ku, D. N., Giddens, D. P., Zarins, C. K., and Glagov, S. (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress Arteriosclerosis 5, 293-302
88. Bussolari, S. R., Dewey, C. F., Jr., and Gimbrone, M. A., Jr. (1982) Apparatus for subjecting living cells to fluid shear stress Rev. Sci. Instrum. 53, 1851-1854
89. Schnittler, H. J., Franke, R. P., Akbay, U., Mrowietz, C., and Drenckhahn, D. (1993) Improved in vitro rheological system for studying the effect of fluid shear stress on cultured cells Am. J. Physiol. 265, C289-C298
90. Frangos, J. A., Eskin, S. G., McIntire, L. V., and Ives, C. L. (1985) Flow effects on prostacyclin production by cultured human endothelial cells Science 227, 1477-1479
91. Levesque, M. J. and Nerem, R. M. (1985) The elongation and orientation of cultured endothelial cells in response to shear stress J. Biomech. Eng. 107, 341-347
92. + current in vascular endothelial cells Nature 331, 168-170
93. Ziegelstein, R. C., Cheng, L., and Capogrossi, M. C. (1992) Flow-dependent cytosolic acidification of vascular endothelial cells Science 258, 656-659
94. Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R., and Mitchison, T. J. (2003) Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor Science 299, 1743-1747
95. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M., and Narumiya, S. (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension Nature 389, 990-994
96. Peterson, L. J., Rajfur, Z., Maddox, A. S., Freel, C. D., Chen, Y., Edlund, M., Otey, C., and Burridge, K. (2004) Simultaneous stretching and contraction of stress fibers in vivo Mol. Biol. Cell 15, 3497-3508
97. Vicente-Manzanares, M., Koach, M. A., Whitmore, L., Lamers, M. L., and Horwitz, A. F. (2008) Segregation and activation of myosin IIB creates a rear in migrating cells J. Cell Biol. 183, 543-554
98. Pelham, R. J. and Wang, Y. L. (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility Proc. Natl. Acad. Sci. U.S.A. 94, 13661-13665
99. Discher, D. E., Janmey, P., and Wang, Y. L. (2005) Tissue cells feel and respond to the stiffness of their substrate Science 310, 1139-1143
100. Engler, A. J., Sen, S., Sweeney, H. L., and Discher, D. E. (2006) Matrix elasticity directs stem cell lineage specification Cell 126, 677-689
101. Wong, A. J., Pollard, T. D., and Herman, I. M. (1983) Actin filament stress fibers in vascular endothelial cells in vivo Science 219, 867-869
102. Wozniak, M. A., Desai, R., Solski, P. A., Der, C. J., and Keely, P. J. (2003) ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix J. Cell Biol. 163, 583-595
103. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D., Hammer, D. A., and Weaver, V. M. (2005) Tensional homeostasis and the malignant phenotype Cancer Cell 8, 241-254
104. Pasapera, A. M., Schneider, I. C., Rericha, E., Schlaepfer, D. D., and Waterman, C. M. (2010) Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation J. Cell Biol. 188, 877-890
105. Hotulainen, P. and Lappalainen, P. (2006) Stress fibers are generated by two distinct actin assembly mechanisms in motile cells J. Cell Biol. 173, 383-394
106. Bhadriraju, K., Yang, M., Alom Ruiz, S., Pirone, D., Tan, J., and Chen, C. S. (2007) Activation of ROCK by RhoA is regulated by cell adhesion, shape, and cytoskeletal tension Exp. Cell Res. 313, 3616-3623
107. Ren, X. D., Kiosses, W. B., and Schwartz, M. A. (1999) Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton EMBO J. 18, 578-585
108. Dubash, A. D., Wennerberg, K., Garcia-Mata, R., Menold, M. M., Arthur, W. T., and Burridge, K. (2007) A novel role for Lsc/p115 RhoGEF and LARG in regulating RhoA activity downstream of adhesion to fibronectin J. Cell Sci. 120, 3989-3998
109. Lim, Y., Lim, S. T., Tomar, A., Gardel, M., Bernard-Trifilo, J. A., Chen, X. L., Uryu, S. A., Canete-Soler, R., Zhai, J., Lin, H., Schlaepfer, W. W., Nalbant, P., Bokoch, G., Ilic, D., Waterman-Storer, C., and Schlaepfer, D. D. (2008) PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility J. Cell Biol. 180, 187-203
110. Bissell, M. J., Hall, H. G., and Parry, G. (1982) How does the extracellular matrix direct gene expression? J. Theor. Biol. 99, 31-68
111. Streuli, C. H. and Bissell, M. J. (1990) Expression of extracellular matrix components is regulated by substratum J. Cell Biol. 110, 1405-1415
112. Nie, M., Aijaz, S., Leefa Chong San, I. V., Balda, M. S., and Matter, K. (2009) The Y-box factor ZONAB/DbpA associates with GEF-H1/Lfc and mediates Rho-stimulated transcription EMBO Rep. 10, 1125-1131
113. Hill, C. S., Wynne, J., and Treisman, R. (1995) The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF Cell 81, 1159-1170
114. Sordella, R., Jiang, W., Chen, G. C., Curto, M., and Settleman, J. (2003) Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis Cell 113, 147-158
115. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K., and Chen, C. S. (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev. Cell 6, 483-495
116. Lee, H. H. and Chang, Z. F. (2008) Regulation of RhoA-dependent ROCKII activation by Shp2 J. Cell Biol. 181, 999-1012
117. Pertz, O., Hodgson, L., Klemke, R. L., and Hahn, K. M. (2006) Spatiotemporal dynamics of RhoA activity in migrating cells Nature 440, 1069-1072
118. Burridge, K., Turner, C. E., and Romer, L. H. (1992) Tyrosine Phosphorylation of Paxillin and Pp125(Fak) Accompanies Cell-Adhesion to Extracellular-Matrix: A Role in Cytoskeletal Assembly J. Cell Biol. 119, 893-903
119. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., Elvassore, N., and Piccolo, S. (2011) Role of YAP/TAZ in mechanotransduction Nature 474, 179-183
120. Moy, A. B., Shasby, S. S., Scott, B. D., and Shasby, D. M. (1993) The effect of histamine and cyclic adenosine monophosphate on myosin light chain phosphorylation in human umbilical vein endothelial cells J. Clin. Invest. 92, 1198-1206
121. Dudek, S. M. and Garcia, J. G. (2001) Cytoskeletal regulation of pulmonary vascular permeability J. Appl. Physiol. 91, 1487-1500
122. Zhong, C. L., Kinch, M. S., and Burridge, K. (1997) Rho-stimulated contractility contributes to the fibroblastic phenotype of ras-transformed epithelial cells Mol. Biol. Cell 8, 2329-2344
123. Braga, V. M., Machesky, L. M., Hall, A., and Hotchin, N. A. (1997) The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts J. Cell Biol. 137, 1421-1431
124. Jou, T. S., Schneeberger, E. E., and Nelson, W. J. (1998) Structural and functional regulation of tight junctions by RhoA and Rac1 small GTPases J. Cell Biol. 142, 101-115
125. Yamada, S. and Nelson, W. J. (2007) Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion J. Cell Biol. 178, 517-527
126. Shewan, A. M., Maddugoda, M., Kraemer, A., Stehbens, S. J., Verma, S., Kovacs, E. M., and Yap, A. S. (2005) Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts Mol. Biol. Cell 16, 4531-4542
127. Miyake, Y., Inoue, N., Nishimura, K., Kinoshita, N., Hosoya, H., and Yonemura, S. (2006) Actomyosin tension is required for correct recruitment of adherens junction components and zonula occludens formation Exp. Cell Res. 312, 1637-1650
128. Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A., and Shibata, M. (2010) α-Catenin as a tension transducer that induces adherens junction development Nat. Cell Biol. 12, 533-542
129. Yamamoto, M., Ramirez, S. H., Sato, S., Kiyota, T., Cerny, R. L., Kaibuchi, K., Persidsky, Y., and Ikezu, T. (2008) Phosphorylation of claudin-5 and occludin by rho kinase in brain endothelial cells Am. J. Pathol. 172, 521-533
130. Noren, N. K., Niessen, C. M., Gumbiner, B. M., and Burridge, K. (2001) Cadherin engagement regulates Rho family GTPases J. Biol. Chem. 276, 33305-33308
131. Lampugnani, M. G., Zanetti, A., Breviario, F., Balconi, G., Orsenigo, F., Corada, M., Spagnuolo, R., Betson, M., Braga, V., and Dejana, E. (2002) VE-cadherin regulates endothelial actin activating Rac and increasing membrane association of Tiam Mol. Biol. Cell 13, 1175-1189
132. Calautti, E., Grossi, M., Mammucari, C., Aoyama, Y., Pirro, M., Ono, Y., Li, J., and Dotto, G. P. (2002) Fyn tyrosine kinase is a downstream mediator of Rho/PRK2 function in keratinocyte cell-cell adhesion J. Cell Biol. 156, 137-148
133. Charrasse, S., Meriane, M., Comunale, F., Blangy, A., and Gauthier-Rouviere, C. (2002) N-cadherin-dependent cell-cell contact regulates Rho GTPases and β-catenin localization in mouse C2C12 myoblasts J. Cell Biol. 158, 953-965
134. Nelson, C. M., Pirone, D. M., Tan, J. L., and Chen, C. S. (2004) Vascular endothelial-cadherin regulates cytoskeletal tension, cell spreading, and focal adhesions by stimulating RhoA Mol. Biol. Cell 15, 2943-2953
135. Liu, W. F., Nelson, C. M., Tan, J. L., and Chen, C. S. (2007) Cadherins, RhoA, and Rac1 are differentially required for stretch-mediated proliferation in endothelial versus smooth muscle cells Circ. Res. 101, e44-e52
136. Katsumi, A., Milanini, J., Kiosses, W. B., Del Pozo, M. A., Kaunas, R., Chien, S., Hahn, K. M., and Schwartz, M. A. (2002) Effects of cell tension on the small GTPase Rac J. Cell Biol. 158, 153-164
137. DuFort, C. C., Paszek, M. J., and Weaver, V. M. (2011) Balancing forces: Architectural control of mechanotransduction Nat. Rev. Mol. Cell Biol. 12, 308-319
138. Provenzano, P. P., Inman, D. R., Eliceiri, K. W., and Keely, P. J. (2009) Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage Oncogene 28, 4326-4343
139. Samuel, M. S., Lopez, J. I., McGhee, E. J., Croft, D. R., Strachan, D., Timpson, P., Munro, J., Schroder, E., Zhou, J., Brunton, V. G., Barker, N., Clevers, H., Sansom, O. J., Anderson, K. I., Weaver, V. M., and Olson, M. F. (2011) Actomyosin-mediated cellular tension drives increased tissue stiffness and β-catenin activation to induce epidermal hyperplasia and tumor growth Cancer Cell 19, 776-791
140. Olson, M. F. and Sahai, E. (2009) The actin cytoskeleton in cancer cell motility Clin. Exp. Metastasis 26, 273-287
141. Provenzano, P. P., Eliceiri, K. W., Campbell, J. M., Inman, D. R., White, J. G., and Keely, P. J. (2006) Collagen reorganization at the tumor-stromal interface facilitates local invasion BMC Med. 4, 38
142. Friedl, P. and Wolf, K. (2009) Plasticity of cell migration: A multiscale tuning model J. Cell Biol. 188, 11-19
143. Wolf, K., Mazo, I., Leung, H., Engelke, K., von Andrian, U. H., Deryugina, E. I., Strongin, A. Y., Brocker, E. B., and Friedl, P. (2003) Compensation mechanism in tumor cell migration: Mesenchymal-amoeboid transition after blocking of pericellular proteolysis J. Cell Biol. 160, 267-277
144. Sahai, E. and Marshall, C. J. (2003) Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis Nat. Cell Biol. 5, 711-719
145. Ren, Y., Li, R., Zheng, Y., and Busch, H. (1998) Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases J. Biol. Chem. 273, 34954-34960
146. Hobert, O., Schilling, J. W., Beckerle, M. C., Ullrich, A., and Jallal, B. (1996) SH3 domain-dependent interaction of the proto-oncogene product Vav with the focal contact protein zyxin Oncogene 12, 1577-1581
147. Bellanger, J. M., Astier, C., Sardet, C., Ohta, Y., Stossel, T. P., and Debant, A. (2000) The Rac1- and RhoG-specific GEF domain of Trio targets filamin to remodel cytoskeletal actin Nat. Cell Biol. 2, 888-892
148. Iwanicki, M. P., Vomastek, T., Tilghman, R. W., Martin, K. H., Banerjee, J., Wedegaertner, P. B., and Parsons, J. T. (2008) FAK, PDZ-RhoGEF and ROCKII cooperate to regulate adhesion movement and trailing-edge retraction in fibroblasts J. Cell Sci. 121, 895-905
149. Sharma, S. V. (1998) Rapid recruitment of p120RasGAP and its associated protein, p190RhoGAP, to the cytoskeleton during integrin mediated cell-substrate interaction Oncogene 17, 271-281
150. Tripathi, V., Popescu, N. C., and Zimonjic, D. B. (2012) DLC1 Interaction with α-Catenin Stabilizes Adherens Junctions and Enhances DLC1 Antioncogenic Activity Mol. Cell. Biol. 32, 2145-2159
151. Haudenschild, D. R., Chen, J., Pang, N., Lotz, M. K., and D'Lima, D. D. (2010) Rho kinase-dependent activation of SOX9 in chondrocytes Arthritis Rheum. 62, 191-200