Molecular mapping of tyrosine-phosphorylated proteins in focal adhesion using flourescence resonance energy transfer

Journal of Cell Science

Volumn 119, Issue 5, 2006, Pages 866-875

  Ballestrem, Christoph ^a   Erez, Noam ^a   Kirchner, Joachim ^a   Kam, Zvi ^a   Bershadsky, Alexander ^a   Geiger, Benjamin ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

CAS; FAK; Focal adhesions; FRET; Paxillin; Phosphorylation

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; CYAN FLUORESCENT PROTEIN; FOCAL ADHESION KINASE; PAXILLIN; PHOSPHOPROTEIN; PHOSPHOTYROSINE; PROTEIN KINASE P60; PROTEIN SH2; RAC PROTEIN; RHO KINASE INHIBITOR; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN;

ANTIBODY LABELING; ARTICLE; CONTROLLED STUDY; FIBROBLAST CULTURE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOCAL ADHESION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; CRK-ASSOCIATED SUBSTRATE PROTEIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; MICE; NIH 3T3 CELLS; PAXILLIN; PHOSPHORYLATION; PROTEIN INTERACTION MAPPING; SRC HOMOLOGY DOMAINS; TYROSINE;

EID: 33645234372     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02794     Document Type: Article

References (44)

1. Abedi, H., Dawes, K. E. and Zachary, I. (1995). Differential effects of platelet-derived growth factor BB on p125 focal adhesion kinase and paxillin tyrosine phosphorylation and on cell migration in rabbit aortic vascular smooth muscle cells and Swiss 3T3 fibroblasts. J. Biol. Chem. 270, 11367-11376.
2. Ballestrem, C., Hinz, B., Imhof, B. A. and Wehrle-Haller, B. (2001). Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior. J. Cell Biol. 155, 1319-1332.
3. Barry, S. T. and Critchley, D. R. (1994). The RhoA-dependent assembly of focal adhesions in Swiss 3T3 cells is associated with increased tyrosine phosphorylation and the recruitment of both pp125FAK and protein kinase C-delta to focal adhesions. J. Cell Sci. 107, 2033-2045.
4. Bellis, S. L., Miller, J. T. and Turner, C. E. (1995). Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J. Biol. Chem. 270, 17437-17441.
5. Brown, M. C. and Turner, C. E. (2004). Paxillin: adapting to change. Physiol. Rev. 84, 1315-1339.
6. Burridge, K. and Chrzanowska-Wodnicka, M. (1996). Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12, 463-518.
7. Choidas, A., Jungbluth, A., Sechi, A., Murphy, J., Ullrich, A. and Marriott, G. (1998). The suitability and application of a GFP-actin fusion protein for long-term imaging of the organization and dynamics of the cytoskeleton in mammalian cells. Eur. J. Cell Biol. 77, 81-90.
8. Clark, E. A., King, W. G., Brugge, J. S., Symons, M. and Hynes, R. O. (1998). Integrin-mediated signals regulated by members of the rho family of GTPases. J. Cell Biol. 142, 573-586.
9. Erez, N., Bershadsky, A. and Geiger, B. (2005). Signaling from adherens-type junctions. Eur. J. Cell Biol. 84, 235-244.
10. Flinn, H. M. and Ridley, A. J. (1996). Rho stimulates tyrosine phosphorylation of focal adhesion kinase, p130 and paxillin. J. Cell Sci. 109, 1133-1141.
11. Geiger, B., Bershadsky, A., Pankov, R. and Yamada, K. M. (2001). Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell. Biol. 2, 793-805.
12. Harte, M. T., Hildebrand, J. D., Burnham, M. R., Bouton, A. H. and Parsons, J. T. (1996). p130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase. J. Biol. Chem. 271, 13649-13655.
13. Ilic, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M. and Yamamoto, T. (1995). Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544.
14. Jares-Erijman, E. A. and Jovin, T. M. (2003). FRET imaging. Nat. Biotechnol. 21, 1387-1395.
15. Kam, Z., Volberg, T. and Geiger, B. (1995). Mapping of adherens junction components using microscopic resonance energy transfer imaging. J. Cell Sci. 108, 1051-1062.
16. Katz, B. Z., Romer, L., Miyamoto, S., Volberg, T., Matsumoto, K., Cukierman, E., Geiger, B. and Yamada, K. M. (2003). Targeting membrane-localized focal adhesion kinase to focal adhesions: roles of tyrosine phosphorylation and SRC family kinases. J. Biol. Chem. 278, 29115-29120.
17. Kirchner, J., Kam, Z., Tzur, G., Bershadsky, A. D. and Geiger, B. (2003). Live-cell monitoring of tyrosine phosphorylation in focal adhesions following microtubule disruption. J. Cell Sci. 116, 975-986.
18. Mertens, A. E., Rygiel, T. P., Olivo, C., van der Kammen, R. and Collard, J. G. (2005). The Rac activator Tiam1 controls tight junction biogenesis in keratinocytes through binding to and activation of the Par polarity complex. J. Cell Biol. 170, 1029-1037.
19. Miyawaki, A. and Tsien, R. Y. (2000). Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol. 327, 472-500.
20. Nakamoto, T., Sakai, R., Honda, H., Ogawa, S., Ueno, H., Suzuki, T., Aizawa, S., Yazaki, Y. and Hirai, H. (1997). Requirements for localization of p130cas to focal adhesions. Mol. Cell. Biol. 17, 3884-3897.
21. Nakamura, K., Yano, H., Uchida, H., Hashimoto, S., Schaefer, E. and Sabe, H. (2000). Tyrosine phosphorylation of paxillin alpha is involved in temporospatial regulation of paxillin-containing focal adhesion formation and F-actin organization in motile cells. J. Biol. Chem. 275, 27155-27164.
22. Narumiya, S., Ishizaki, T. and Uehata, M. (2000). Use and properties of ROCK-specific inhibitor Y-27632. Methods Enzymol. 325, 273-284.
23. Nollau, P. and Mayer, B. J. (2001). Profiling the global tyrosine phosphorylation state by Src homology 2 domain binding. Proc. Natl. Acad. Sci. USA 98, 13531-13536.
24. O'Neill, G. M., Fashena, S. J. and Golemis, E. A. (2000). Integrin signalling: a new Cas(t) of characters enters the stage. Trends Cell Biol. 10, 111-119.
25. Panetti, T. S. (2002). Tyrosine phosphorylation of paxillin, FAK, and p130CAS: effects on cell spreading and migration. Front. Biosci. 7, D143-D150.
26. Parsons, J. T., Martin, K. H., Slack, J. K., Taylor, J. M. and Weed, S. A. (2000). Focal adhesion kinase: a regulator of focal adhesion dynamics and cell movement. Oncogene 19, 5606-5613.
27. Pawson, T., Gish, G. D. and Nash, P. (2001). SH2 domains, interaction modules and cellular wiring. Trends Cell Biol. 11, 504-511.
28. Rankin, S. and Rozengurt, E. (1994). 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.
29. Richardson, A. and Parsons, T. (1996). A mechanism for regulation of the adhesion-associated proteintyrosine kinase pp125FAK. Nature 380, 538-540.
30. Ruest, P. J., Shin, N. Y., Polte, T. R., Zhang, X. and Hanks, S. K. (2001). Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src. Mol. Cell. Biol. 21, 7641-7652.
31. Schaller, M. D. (2001). Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim. Biophys. Acta 1540, 1-21.
32. Schaller, M. D. and Parsons, J. T. (1994). Focal adhesion kinase and associated proteins. Curr. Opin. Cell Biol. 6, 705-710.
33. Schaller, M. D. and Parsons, J. T. (1995). pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15, 2635-2645.
34. Siegel, R. M., Chan, F. K., Zacharias, D. A., Swofford, R., Holmes, K. L., Tsien, R. Y. and Lenardo, M. J. (2000). Measurement of molecular interactions in living cells by fluorescence resonance energy transfer between variants of the green fluorescent protein. Sci. STKE 2000, L1.
35. Turner, C. E. (2000a). Paxillin and focal adhesion signalling. Nat. Cell Biol. 2, E231-E236.
36. Turner, C. E. (20006). Paxillin interactions. J. Cell Sci. 113, 4139-4140.
37. Turner, C. E., Glenney, J. R., Jr and Burridge, K. (1990). Paxillin: a new vinculin-binding protein present in focal adhesions. J. Cell Biol. 111, 1059-1068.
38. Volberg, T., Romer, L., Zamir, E. and Geiger, B. (2001). pp60(c-src) and related tyrosine kinases: a role in the assembly and reorganization of matrix adhesions. J. Cell Sci. 114, 2279-2289.
39. Vuori, K., Hirai, H., Aizawa, S. and Ruoslahti, E. (1996). Introduction of p130cas signaling complex formation upon integrin- mediated cell adhesion: a role for Src family kinases. Mol. Cell. Biol. 16, 2606-2613.
40. Wood, C. K., Turner, C. E., Jackson, P. and Critchley, D. R. (1994). Characterisation of the paxillin-binding site and the C-terminal focal adhesion targeting sequence in vinculin. J. Cell Sci. 107, 709-717.
41. Zaidel-Bar, R., Ballestrem, C., Kam, Z. and Geiger, B. (2003). Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J. Cell Sci. 116, 4605-4613.
42. Zaidel-Bar, R., Kam, Z. and Geiger, B. (2005). Polarized downregulation of the paxillin-p130CAS-Rac1 pathway induced by shear flow. J. Cell Sci. 118, 3997-4007.
43. Zamir, E. and Geiger, B. (2001). Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 114, 3583-3590.
44. Zamir, E., Katz, B. Z., Aota, S., Yamada, K. M., Geiger, B. and Kam, Z. (1999). Molecular diversity of cell-matrix adhesions. J. Cell Sci. 112, 1655-1669.