Transmembrane extracellular matrix-cytoskeleton crosstalk

Nature Reviews Molecular Cell Biology

Volumn 2, Issue 11, 2001, Pages 793-805

  Geiger, Benjamin ^a   Bershadsky, Alexander ^a   Pankov, Roumen ^b   Yamada, Kenneth M ^b  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CELL MEMBRANE; CYTOSKELETON; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN BINDING; REVIEW; SIGNAL TRANSDUCTION;

ANIMAL; CELL ADHESION; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; CYTOSKELETON; EXTRACELLULAR MATRIX; HUMAN; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 0035516140     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/35099066     Document Type: Article

References (118)

1. Gumbiner, B. M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357 (1996).
2. Giancotti, F. G. & Ruoslahti, E. Integrin signalling. Science 285, 1028-1032 (1999).
3. Curtis, A. & Wilkinson, C. New depths in cell behaviour: reactions of cells to nanotopography. Biochem. Soc. Symp. 65, 15-26 (1999).
4. Huang, S. & Ingber, D. E. The structural and mechanical complexity of cell-growth control. Nature Cell Biol. 1, E131-138 (1999).
5. Katz, B. Z. et al. Physical state of the extracellular matrix regulates the structure and molecular composition of cell-matrix adhesions. Mol. Biol. Cell 11, 1047-1060 (2000).
6. Lo, C. M., Wang, H. B., Dembo, M. & Wang, Y. L. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152 (2000).
7. Abercrombie, M. & Dunn, G. A. Adhesions of fibroblasts to substratum during contact inhibition observed by interference reflection microscopy. Exp. Cell Res. 92, 57-62 (1975).
8. Izzard, C. S. & Lochner, L. R. Cell-to-substrate contacts in living fibroblasts: an interference reflexion study with an evaluation of the technique. J. Cell. Sci. 21, 129-159 (1976).
9. Sastry, S. K. & Burridge, K. Focal adhesions: A nexus for intracellular signaling and cytoskeletal dynamics. Exp. Cell. Res. 261, 25-36 (2000).
10. Zamir, E. & Geiger, B. Molecular diversity of actin-integrin adhesion complexes. J. Cell Sci. (in the press).
11. Kano, Y., Katoh, K., Masuda, M. & Fujiwara, K. Macromolecular composition of stress fiber-plasma membrane attachment sites in endothelial cells in situ. Circ. Res. 79, 1000-1006 (1996).
12. Turner, C. E., Kramarcy, N., Sealock, R. & Burridge, K. Localization of paxillin, a focal adhesion protein, to smooth muscle dense plaques, and the myotendinous and neuromuscular junctions of skeletal muscle. Exp. Cell Res. 192, 651-655 (1991).
13. Chen, W. T. & Singer, S. J. Immunoelectron microscopic studies of the sites of cell-substratum and cell-cell contacts in cultured fibroblasts. J. Cell Biol. 95, 205-222 (1982).
14. Zamir, E. et al. Molecular diversity of cell-matrix adhesions. J. Cell Sci. 112, 1655-1669 (1999).
15. Zamir, E. et al. Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nature Cell Biol. 2, 191-196 (2000). The dynamics of focal adhesions and fibrillar adhesions and formation of the latter from the former were shown using time-lapse microscopy of GFP-paxillin and GFP-tensin.
16. Bershadsky, A. D., Tint, I. S., Neyfakh, A. A., Jr & Vasiliev, J. M. Focal contacts of normal and RSV-transformed quail cells. Hypothesis of the transformation-induced deficient maturation of focal contacts. Exp. Cell Res. 158, 433-444 (1985).
17. Nobes, C. D. & Hall, A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62 (1995).
18. Rottner, K., Hall, A. & Small, J. V. Interplay between rac and rho in the control of substrate contact dynamics. Curr. Biol. 9, 640-648 (1999). In this study and in reference 17, differential signalling requirements for focal adhesions and focal complexes were established. Focal complex formation depends on Rac activity, whereas focal adhesions require Rho and Rho-kinase activity.
19. Tarone, G., Cirillo, D., Giancotti, F. G., Comoglio, P. M. & Marchisio, P. C. Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes. Exp. Cell Res. 159, 141-157 (1985).
20. Zambonin-Zallone, A. et al. Immunocytochemical distribution of extracellular matrix receptors in human osteoclasts: a β 3 integrin is colocalized with vinculin and talin in the podosomes of osteoclastoma giant cells. Exp. Cell Res. 182, 645-652 (1989).
21. Gaidano, G. et al. Integrin distribution and cytoskeleton organization in normal and malignant monocytes. Leukemia 4, 682-687 (1990).
22. Chellaiah, M. et al. Gelsolin deficiency blocks podosome assembly and produces increased bone mass and strength. J. Cell Biol. 148, 665-678 (2000).
23. Ochoa, G. C. et al. A functional link between dynamin and the actin cytoskeleton at podosomes. J. Cell Biol. 150, 377-389 (2000). An Interesting discovery of dynamin localization at the tubular invaginations of the plasma membrane In podosomes and characterization of its involvement in podosome formation.
24. Xu, W., Baribault, H. & Adamson, E. D. Vinculin knockout results in heart and brain defects during embryonic development. Development 125, 327-337 (1998).
25. Sheppard, D. In vivo functions of integrins: lessons from null mutations in mice. Matrix Biol. 19, 203-209 (2000).
26. Liu, S., Calderwood, D. A. & Ginsberg, M. H. Integrin cytoplasmic domain-binding proteins. J. Cell Sci. 113, 3563-3571 (2000).
27. Echtermeyer, F., Baciu, P. C., Saoncella, S., Ge, Y. & Goetinck, P. F. Syndecan-4 core protein is sufficient for the assembly of focal adhesions and actin stress fibers. J. Cell Sci. 112, 3433-3441 (1999).
28. Bono, P., Rubin, K., Higgins, J. M. & Hynes, R. O. Layilin, a novel integral membrane protein, is a hyaluronan receptor. Mol. Biol. Cell 12, 891-900 (2001).
29. Wei, Y., Yang, X., Liu, Q., Wilkins, J. A. & Chapman, H. A. A role for caveolin and the urokinase receptor in integrin-mediated adhesion and signaling. J. Cell Biol. 144, 1285-1294 (1999).
30. Prehoda, K. E., Scott, J. A., Mullins, R. D. & Lim, W. A. Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex. Science 290, 801-806 (2000).
31. 2-mediated control of plasma membrane interaction with the underlying cytoskeleton.
32. Fukami, K., Endo, T., Imamura, M. & Takenawa, T. α-actinin and vinculin are PIP2-binding proteins involved in signaling by tyrosine kinase. J. Biol. Chem. 269. 1518-1522 (1994).
33. Tall, E. G., Spector, I., Pentyala, S. N., Bitter, I. & Rebecchi, M. J. Dynamics of phosphatidylinositol 4,5-bisphosphate in actin-rich structures. Curr. Biol. 10, 743-746 (2000).
34. Serra-Pages, C. et al. The LAR transmembrane protein tyrosine phosphatase and a coiled-coil LAR-interacting protein co-localize at focal adhesions. EMBO J. 14, 2827-2838 (1995).
35. Inagaki, K. et al. SHPS-1 regulates integrin-mediated cytoskeletal reorganization and cell motility. EMBO J. 19, 6721-6731 (2000).
36. Lin, S. & Lin, D. Mapping of actin, vinculin, and integrin binding domains suggests a direct role of tensin in actin-membrane association. Mol. Biol. Cell 7, (suppl.) 389a (1996).
37. 1 and 14-3-3β. Oncogene 20, 346-357 (2001).
38. Liu, S. & Ginsberg, M. H. Paxillin binding to a conserved sequence motif in the α4 integrin cytoplasmic domain. J. Biol. Chem. 275, 22736-22742 (2000).
39. Liu, S., Slepak, M. & Ginsberg, M. H. Direct binding of paxillin to the α9 integrin cytoplasmic domain inhibits cell spreading. J. Biol. Chem. 27, 37086-37092 (2001).
40. Prasad, N., Topping, R. S. & Decker, S. J. SH2-containing inositol 5′-phosphatase SHIP2 associates with the p130(Cas) adapter protein and regulates cellular adhesion and spreading. Mol. Cell. Biol. 21, 1416-1428 (2001).
41. Miyamoto, S. et al. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol. 131, 791-805 (1995).
42. Miyamoto, S., Akiyama, S. K. & Yamada, K. M. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 267, 883-885 (1995). The local reaction that is induced by interactions of integrins with matrix proteins was analysed by application of micron-sized beads that were covered with a protein of interest to the cell surface. Both the clustering of Integrin molecules and their direct interaction with matrix proteins through the RGD motif (occupancy) were shown to be necessary for inducing recruitment of the appropriate cytoplasmic proteins to the adhesion site.
43. Laukaitis, C. M., Webb, D. J., Donais, K. & Horwitz, A. F. Differential dynamics of α 5 integrin, paxillin, and α-actinin during formation and disassembly of adhesions in migrating cells. J. Cell Biol. 153, 1427-1440 (2001).
44. Chrzanowska-Wodnicka, M. & Burridge, K. Rhostimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415 (1996). This study first showed the role of myosin II downstream of Rho in the formation of focal adhesions.
45. Bershadsky, A., Chausovsky, A., Becker, E., Lyubimova, A. & Geiger, B. Involvement of microtubules in the control of adhesion-dependent signal transduction. Curr. Biol. 6, 1279-1289 (1996). This study showed that microtubule disruption induces formation of focal adhesions through the activation of myosin II-driven contractility.
46. Riveline, D. et al. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153, 1175-1186 (2001). This study showed the induction of focal-adhesion growth by locally applied tension force. Application of external force bypasses the requirements for Rho kinase (ROCK) and myosin II-dependent cell contractility for the formation of focal adhesions, provided that another target of Rho, mDia1, is active.
47. Volberg, T., Geiger, B., Citi, S. & Bershadsky, A. D. Effect of protein kinase inhibitor H-7 on the contractility, integrity, and membrane anchorage of the microf lament system. Cell Motil. Cytoskel. 29, 321-338 (1994).
48. Uehata, M. et al. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994 (1997).
49. Helfman, D. M. et al. Caldesmon inhibits nonmuscle cell contractility and interferes with the formation of focal adhesions. Mol. Biol. Cell 10, 3097-3112 (1999).
50. Geiger, B. & Bershadsky, A. Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13, 584-592 (2001).
51. Watanabe, N., Kato, T., Fujita, A., Ishizaki, T. & Narumiya, S. Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nature Cell Biol. 1, 136-143 (1999).
52. Choquet, D., Felsenfeld, D. P. & Sheetz, M. P. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88, 39-48 (1997). The simulation of ECM rigidity by trapping ECM-coated beads by laser tweezers leads to a local increase in actomyosin-mediated force applied to the trapped bead by the cell. This Indicates that isometric force applied to an integrin-mediated adhesion site Induces local reinforcement of association of this site with the actin cytoskeleton.
53. Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V. & Wang, Y. L. Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153, 831-888 (2001). This study showed that locomoting cells apply the strongest forces to small zyxin-containing focal complexes at the leading edge.
54. Harris, A K., Wild, P. & Stopak, D. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208, 177-179 (1980). This study showed for the first time that the cell applies mechanical force to the substrate to which it adheres.
55. Burton, K., Park, J. H. & Taylor, D. L. Keratocytes generate traction forces in two phases. Mol. Biol. Cell 10, 3745-3769 (1999).
56. Galbraith, C. G. & Sheetz, M. P. A micromachined device provides a new bend on fibroblast traction forces. Proc. Natl Acad. Sci. USA 94, 9114-9118 (1997).
57. Dembo, M. & Wang, Y. L. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76, 2307-2316 (1999).
58. Munevar, S., Wang, Y. & Dembo, M. Traction force microscopy of migrating normal and h-ras transformed 3t3 fibroblasts. Biophys. J. 80, 1744-1757 (2001).
59. Balaban, N. Q. et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nature Cell Biol. 3, 466-472 (2001). This study used micropatterned elastomer substrate and fluorescence imaging of focal adhesions in live cells, which showed a strong correlation between focal-adhesion size and local forces that are applied by the cell at these sites. The size of the focal contacts decreased rapidly in proportion to a decrease of these forces that were induced by BDM treatment.
60. Kornberg, L., Earp, H. S., Parsons, J. T., Schaller, M. & Juliano, R. L. Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J. Biol. Chem. 267, 23439-23442 (1992).
61. Burridge, K., Turner, C. E. & Romer, L. H. Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119, 893-903 (1992). This and the previous study initiated a cascade of publications showing that the formation of focal adhesions is accompanied by tyrosine phosphorylation of their main components.
62. Rankin, S. & Rozengurt, E. Platelet-derived growth factor modulation of focal adhesion kinase (p125FAK) and paxillin tyrosine phosphorylation in Swiss 3T3 cells. Bell-shaped dose response and cross-talk with bombesin. J. Biol. Chem. 269, 704-710 (1994).
63. Casamassima, A. & Rozengurt, E. Insulin-like growth factor I stimulates tyrosine phosphorylation of p130(Cas), focal adhesion kinase, and paxillin. Role of phosphatidylinositol 3′-kinase and formation of a p130(Cas). Crk complex. J. Biol. Chem. 273, 26149-26156 (1998).
64. Li, S. et al. Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases. J. Biol. Chem. 272, 30455-30462 (1997).
65. Yano, Y., Geibel, J. & Sumpio, B. E. Tyrosine phosphorylation of pp125FAK and paxillin in aortic endothelial cells induced by mechanical strain. Am. J. Physiol. 271, C635-C649 (1996).
66. Sai, X., Naruse, K. & Sokabe, M. Activation of pp60(src) is critical for stretch-induced orienting response in fibroblasts. J. Cell Sci. 112, 1365-1373 (1999).
67. Parsons, J. T., Martin, K. H., Slack, J. K., Taylor, J. M. & Weed, S. A. Focal adhesion kinase: a regulator of focal adhesion dynamics and cell movement. Oncogene 19, 5606-5613 (2000).
68. Kaplan, K. B. et al. Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527. EMBO J. 13, 4745-4756 (1994).
69. c-src in the regulation of cell-matrix adhesion.
70. Felsenfeld, D. P., Schwartzberg, P. L., Venegas, A., Tse, R. & Sheetz, M. P. Selective regulation of integrin-cytoskeleton interactions by the tyrosine kinase Src. Nature Cell Biol. 1, 200-206 (1999).
71. Volberg, T., Romer, L., Zamir, E. & Geiger, B. pp60(c-src) and related tyrosine kinases: a role in the assembly and reorganization of matrix adhesions. J. Cell Sci. 114, 2279-2289 (2001).
72. Ilic, D. et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 533-544 (1995).
73. -/- mutant mice. Genes Dev. 11, 2835-2844 (1997).
74. Arthur, W. T., Petch, L. A. & Burridge, K. Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr. Biol. 10, 719-722 (2000).
75. Ren, X. D. et al. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci. 113, 3673-3678 (2000).
76. 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev. 9, 1883-1895 (1995).
77. Henry, M. D. & Campbell, K. P. A role for dystroglycan in basement membrane assembly. Cell 95, 859-870 (1998).
78. Colognato, H., Winkelmann, D. A. & Yurchenco, P. D. Laminin polymerization induces a receptor-cytoskeleton network. J. Cell Biol. 145, 619-631 (1999).
79. Avnur, Z. & Geiger, B. The removal of extracellular fibronectin from areas of cell-substrate contact. Cell 25, 121-132 (1981).
80. 1 integrin from focal adhesions to, and along, fibrillar adhesions that drive the formation of fibronectin matrix.
81. McDonald, J. A., Kelley, D. G. & Broekelmann, T. J. Role of fibronectin in collagen deposition: Fab' to the gelatin-binding domain of fibronectin inhibits both fibronectin and collagen organization in fibroblast extracellular matrix. J. Cell Biol. 92, 485-492 (1982).
82. Akiyama, S. K., Yamada, S. S., Chen, W. T. & Yamada, K. M. Analysis of fibronectin receptor function with monoclonal antibodies: roles in cell adhesion, migration, matrix assembly, and cytoskeletal organization. J. Cell Biol. 109, 863-875 (1989).
83. Harris, A. K., Stopak, D. & Wild, P. Fibroblast traction as a mechanism for collagen morphogenesis. Nature 290, 249-251 (1981).
84. Mosher, D. F. (ed.) in Fibronectin. (Academic, San Diego, 1989).
85. Hynes, R. O. in Fibronectins. (Springer, New York, 1990).
86. Yamada, K. M. & Clark, R. A. F. in The Molecular and Cellular Biology of Wound Repair (ed. Clark, R. A. F.) 51-93 (Plenum, New York, 1996).
87. 1 integrin-dependent and independent polymerization of fibronectin. J. Cell Biol. 132, 227-238 (1996).
88. v integrins. Mol. Biol. Cell 7, 1737-1748 (1996).
89. 1 integrin binding to the alternatively spliced V region. J. Cell Sci. 113, 1491-1498 (2000).
90. 2-terminal region of fibronectin to molecules of large apparent molecular mass. Characterization of fibronectin assembly sites induced by the treatment of fibroblasts with lysophosphatidic acid. J. Biol. Chem. 271, 33284-33292 (1996).
91. Schwarzbauer, J. E. & Sechler, J. L. Fibronectin fibrillogenesis: a paradigm for extracellular matrix assembly. Curr. Opin. Cell Biol. 11, 622-627 (1999).
92. Erickson, H. P. Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin. Proc. Natl Acad. Sci. USA 91, 10114-10118 (1994).
93. Hocking, D. C., Smith, R. K. & McKeown-Longo, P. J. A novel role for the integrin-binding III-10 module in fibronectin matrix assembly. J. Cell Biol. 133, 431-444 (1996).
94. Wu, C., Keivens, V. M., O'Toole, T. E., McDonald, J. A. & Ginsberg, M. H. Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix. Cell 83, 715-724 (1995).
95. Halliday, N. L. & Tomasek, J. J. Mechanical properties of the extracellular matrix influence fibronectin fibril assembly in vitro. Exp. Cell Res. 217, 109-117 (1995).
96. Zhong, C. et al. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141, 539-551 (1998). This paper links cell contractility regulated by Rho and stretch-induced exposure of cryptic assembly sites in fibronectin to provide mechanistic insight into matrix assembly.
97. 2 as particularly important for matrix assembly.
98. Ohashi, T., Kiehart, D. P. & Erickson, H. P. Dynamics and elasticity of the fibronectin matrix in living cell culture visualized by fibronectin-green fluorescent protein. Proc. Natl Acad. Sci. USA 96, 2153-2158 (1999). The first paper to document stretching of fibronectin in living cells using green fluorescent protein (GFP).
99. Finer, J. T., Simmons, R. M. & Spudich, J. A. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368, 113-119 (1994).
100. Smilenov, L. B., Mikhailov, A., Pelham, R. J., Marcantonio, E. E. & Gundersen, G. G. Focal adhesion motility revealed in stationary fibroblasts. Science 286, 1172-1174 (1999).
101. Selve, N. & Wegner, A. Rate of treadmilling of actin filaments in vitro. J. Mol. Biol. 187, 627-631 (1986).
102. Waterman-Storer, C. M., Desai, A., Bulinski, J. C. & Salmon, E. D. Fluorescent speckle microscopy, a method to visualize the dynamics of protein assemblies in living cells. Curr. Biol. 8, 1227-1230 (1998).
103. Small, J. V. Rottner, K., Kaverina, I. & Anderson, K. I. Assembling an actin cytoskeleton for cell attachment and movement. Biochim. Biophys. Acta 1404, 271-281 (1998).
104. Lo, S. H., Janmey, P. A., Hartwig, J. H. & Chen, L. B. Interactions of tensin with actin and identification of its three distinct actin-binding domains. J. Cell Biol. 125, 1067-1075 (1994).
105. Craig, D., Krammer, A., Schulten, K. & Vogel, V. Comparison of the early stages of forced unfolding for fibronectin type III modules. Proc. Natl Acad. Sci. USA 98, 5590-5595 (2001).
106. Krammer, A., Lu, H., Isralewitz, B., Schulten, K. & Vogel, V. Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc. Natl Acad. Sci. USA 96, 1351-1356 (1999).
107. McKeown-Longo, P. J. & Mosher, D. F. Binding of plasma fibronectin to cell layers of human skin fibroblasts. J. Cell Biol. 97, 466-472 (1983).
108. Langenbach, K. J. & Sottile, J. Identification of protein-disulfide isomerase activity in fibronectin. J. Biol. Chem. 274, 7032-7038 (1999).
109. Teti, A., Marchisio, P. C. & Zallone, A. Z. Clear zone in osteoclast function: role of podosomes in regulation of bone-resorbing activity. Am. J. Physiol. 261, C1-C7 (1991).
110. Danen, E. H., Sonneveld, P., Sonnenberg, A. & Yamada, K. M. Dual stimulation of Ras/mitogen-activated protein kinase and RhoA by cell adhesion to fibronectin supports growth factor-stimulated cell cycle progression. J. Cell Biol. 151, 1413-1422 (2000).
111. Davies, P. F., Robotewskyj, A. & Griem, M. L. Quantitative studies of endothelial cell adhesion. Directional remodeling of focal adhesion sites in response to flow forces. J. Clin. Invest. 93, 2031-2038 (1994).
112. Chen, K. D. et al. Mechanotransduction in response to shear stress. Roles of receptor tyrosine kinases, integrins, and Shc. J. Biol. Chem. 274, 18393-18400 (1999).
113. Jalali, S. et al. Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc. Natl Acad. Sci. USA 98, 1042-1046 (2001).
114. Hamill, O. P. & Martinac, B. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81, 685-740 (2001).
115. Muller, U. & Littlewood-Evans, A Mechanisms that regulate mechanosensory hair cell differentiation. Trends Cell Biol. 11, 334-342 (2001).
116. Nicklas, R. B., Campbell, M. S., Ward, S. C. & Gorbsky, G. J. Tension-sensitive kinetochore phosphorylation in vitro. J. Cell Sci. 111, 3189-3196 (1998).
117. Bjorge, J. D., Jakymiw, A. & Fujita, D. J. Selected glimpses into the activation and function of Src kinase. Oncogene 19, 5620-5635 (2000).
118. Ishikawa, H. et al. Structural conversion between open and closed forms of radixin: low-angle shadowing electron microscopy. J. Mol. Biol. 310, 973-978 (2001).