Force-dependent integrin-cytoskeleton linkage formation requires downregulation of focal complex dynamics by Shp2

EMBO Journal

Volumn 22, Issue 19, 2003, Pages 5023-5035

  Von Wichert, Götz ^a   Haimovich, Beatrice ^b   Feng, Gen Sheng ^c   Sheetz, Michael P ^a  

^a Columbia University ^*  (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^c BURNHAM INSTITUTE   (United States)

Author keywords

Focal adhesion kinase; Focal complex; Force; FRAP; Shp2

Indexed keywords

ALPHA ACTININ; FOCAL ADHESION KINASE; GREEN FLUORESCENT PROTEIN; INTEGRIN; PAXILLIN; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE 2; UNCLASSIFIED DRUG; VINCULIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; BLEACHING; CELL ADHESION; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; ENZYME INHIBITION; FIBROBLAST; FLUORESCENCE; FORCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION;

ACTININ; ANIMALS; CYTOSKELETON; DOWN-REGULATION; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; INTEGRINS; PROTEIN-TYROSINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; SRC HOMOLOGY DOMAINS;

ANIMALIA;

EID: 0141865507     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg492     Document Type: Article

References (53)

1. Balaban, N.Q. et al. (2001) Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol., 3, 466-472.
2. Ballestrem, C., Hinz, B., Imhof, B.A. and Wehrle-Haller, B. (2001) Marching at the front and dragging behind: differential αVP3-integrin turnover regulates focal adhesion behavior. J. Cell Biol., 155, 1319-1332.
3. 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.
4. Choquet, D., Felsenfeld, D.P. and Sheetz, M.P. (1997) Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell, 88, 39-48.
5. Critchley, D.R. (2000) Focal adhesions-the cytoskeletal connection. Curr. Opin. Cell Biol., 12, 133-139.
6. Edlund, M., Lotano, M.A. and Otey, C.A. (2001) Dynamics of α-actinin in focal adhesions and stress fibers visualized with α-actinin-green fluorescent protein. Cell Motil. Cytoskeleton, 48, 190-200.
7. Felsenfeld, D.P., Choquet, D. and Sheetz, M.P. (1996) Ligand binding regulates the directed movement of β1 integrins on fibroblasts. Nature, 383, 438-440.
8. Felsenfeld, D.P., Schwartzberg, P.L., Venegas, A., Tse, R. and Sheetz, M.P. (1999) Selective regulation of integrin-cytoskeleton interactions by the tyrosine kinase Src. Nat. Cell Biol., 1, 200-206.
9. Feng, G.S. (1999) Shp-2 tyrosine phosphatase: signaling one cell or many. Exp. Cell Res., 253, 47-54.
10. Fincham, V.J. and Frame, M.C. (1998) 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, 81-92.
11. Galbraith, C.G., Yamada, K.M. and Sheetz, M.P. (2002) The relationship between force and focal complex development. J. Cell Biol., 159, 695-705.
12. Geiger, B. and Bershadsky, A. (2002) Exploring the neighborhood: adhesion-coupled cell mechanosensors. Cell, 110, 139-142.
13. 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.
14. Giancotti, F.G. and Ruoslahti, E. (1999) Integrin signaling. Science, 285, 1028-1032.
15. Hughes, P.E. and Pfaff, M. (1998) Integrin affinity modulation. Trends Cell Biol., 8, 359-364.
16. Ilic, D. et al. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature, 377, 539-544.
17. Inagaki, K., Yamao, T., Noguchi, T., Matozaki, T., Fukunaga, K., Takada, T., Hosooka, T., Akira, S. and Kasuga, M. (2000) SHPS-1 regulates integrin-mediated cytoskeletal reorganization and cell motility. EMBO J., 19, 6721-6731.
18. Izaguirre, G., Aguirre, L., Hu, Y.P., Lee, H.Y., Schlaepfer, D.D., Aneskievich, B.J. and Haimovich, B. (2001) The cytoskeletal/non-muscle isoform of α-actinin is phosphorylated on its actin-binding domain by the focal adhesion kinase. J. Biol. Chem., 276, 28676-28685.
19. Kodama, A., Matozaki, T., Fukuhara, A., Kikyo, M., Ichihashi, M. and Takai, Y. (2000) Involvement of an SHP-2-Rho small G protein pathway in hepatocyte growth factor/scatter factor-induced cell scattering. Mol. Biol. Cell, 11, 2565-2575.
20. Lacalle, R.A., Mira, E., Gomez-Mouton, C., Jimenez-Baranda, S., Martinez, A.C. and Manes, S. (2002) Specific SHP-2 partitioning in raft domains triggers integrin-mediated signaling via Rho activation. J. Cell Biol., 157, 277-289.
21. Lauffenburger, D.A. and Horwitz, A.F. (1996) Cell migration: a physically integrated molecular process. Cell, 84, 359-369.
22. Laukaitis, C.M., Webb, D.J., Donais, K. and Horwitz, A.F. (2001) Differential dynamics of α5 integrin, paxillin and α-actinin during formation and disassembly of adhesions in migrating cells. J. Cell Biol., 153, 1427-1440.
23. Manes, S., Mira, E., Gomez-Mouton, C., Zhao, Z.J., Lacalle, R.A. and Martinez, A.C. (1999) Concerted activity of tyrosine phosphatase SHP-2 and focal adhesion kinase in regulation of cell motility. Mol. Cell. Biol., 19, 3125-3135.
24. Miao, H., Burnett, E., Kinch, M., Simon, E. and Wang, B. (2000) Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat. Cell Biol., 2, 62-69.
25. Miyamoto, S., Akiyama, S.K. and Yamada, K.M. (1995) Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science, 267, 883-885.
26. Mortier, E., Cornelissen, F., van Hove, C., Dillen, L. and Richardson, A. (2001) The focal adhesion targeting sequence is the major inhibitory moiety of Fak-related non-kinase. Cell Signal, 13, 901-909.
27. Nobes, C.D. and Hall, A. (1995) Rho, rac and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia and filopodia. Cell, 81, 53-62.
28. Otey, C., Vasquez, G.B., Burridge, K. and Erickson, B.W. (1993) Mapping of the α-actinin binding site within the β1 integrin cytoplasmic domain. J. Biol. Chem., 268, 21193-21197.
29. Pavalko, F.M., Otey, C.A., Simon, K.O. and Burridge, K. (1991) α-actinin: a direct link between actin and integrins. Biochem. Soc. Trans., 19, 1065-1069.
30. Petrone, A. and Sap, J. (2000) Emerging issues in receptor protein tyrosine phosphatase function: lifting fog or simply shifting? J. Cell Sci., 113, 2345-2354.
31. Pierschbacher, M.D. and Ruoslahti, E. (1987) Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. J. Biol. Chem., 262, 17294-17298.
32. Ren, X.D., Kiosses, W.B., Sieg, D.J., Otey, C.A., Schlaepfer, D.D. and Schwartz, M.A. (2000) Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci., 113, 3673-3678.
33. Richardson, A. and Parsons, T. (1996) A mechanism for regulation of the adhesion-associated proteintyrosine kinase pp125FAK. Nature, 380, 538-540.
34. 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 mDial-dependent and ROCK-independent mechanism. J. Cell Biol., 153, 1175-1186.
35. Rottner, K., Hall, A. and Small, J.V. (1999) Interplay between Rac and Rho in the control of substrate contact dynamics. Curr. Biol., 9, 640-648.
36. Salmon, E.D. and Wadsworth, P. (1986) Applications of Fluorescence in the Biomedical Sciences. Alan R. Liss, New York, NY.
37. Sawada, Y. and Sheetz, M.P. (2002) Force transduction by Triton cytoskeletons. J. Cell Biol., 156, 609-615.
38. Saxton, T.M., Henkemeyer, M., Gasca, S., Shen, R., Rossi, D.J., Shalaby, F., Feng, G.S. and Pawson, T. (1997) Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2. EMBO J., 16, 2352-2364.
39. Schaller, M.D. (2001) Paxillin: a focal adhesion-associated adaptor protein. Oncogene, 20, 6459-6472.
40. Schoenwaelder, S.M., Petch, L.A., Williamson, D., Shen, R., Feng, G.S. and Burridge, K. (2000) The protein tyrosine phosphatase Shp-2 regulates RhoA activity. Curr. Biol., 10, 1523-1526.
41. Sheetz, M.P., Felsenfeld, D.P. and Galbraith, C.G. (1998) Cell migration: regulation of force on extracellular-matrix-integrin complexes. Trends Cell Biol., 8, 51-54.
42. Sheetz, M.P., Felsenfeld, D., Galbraith, C.G. and Choquet, D. (1999) Cell migration as a five-step cycle. Biochem. Soc. Symp., 65, 233-243.
43. Sieg, D.J., Hauck, C.R. and Schlaepfer, D.D. (1999) Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci., 112, 2677-2691.
44. Smilenov, L.B., Mikhailov, A., Pelham, R.J., Marcantonio, E.E. and Gundersen, G.G. (1999) Focal adhesion motility revealed in stationary fibroblasts. Science, 286, 1172-1174.
45. Taylor, J.M., Mack, C.P., Nolan, K., Regan, C.P., Owens, G.K. and Parsons, J.T. (2001) Selective expression of an endogenous inhibitor of FAK regulates proliferation and migration of vascular smooth muscle cells. Mol. Cell. Biol., 21, 1565-1572.
46. Tsuruta, D., Gonzales, M., Hopkinson, S.B., Otey, C., Khuon, S., Goldman, R.D. and Jones, J.C. (2002) Microfilament-dependent movement of the β3 integrin subunit within focal contacts of endothelial cells. FASEB J., 16, 866-868.
47. Turner, C.E. (2000) Paxillin and focal adhesion signalling. Nat. Cell Biol., 2, E231-E236.
48. von Wichert, G., Jiang, G., Kostic, A., De Vos, K., Sap, J., Sheetz, M.P. (2003) RPTP-α acts as a transducer of mechanical force on αv/β3-integrin-cytoskeleton linkages. J. Cell Biol., 161, 143-153.
49. Wachsstock, D.H., Schwarz, W.H. and Pollard, T.D. (1994) Cross-linker dynamics determine the mechanical properties of actin gels. Biophys. J., 66, 801-809.
50. Wehrle-Haller, B. and Imhof, B. (2002) The inner lives of focal adhesions. Trends Cell Biol., 12, 382-389.
51. Xu, J., Wirtz, D. and Pollard, T.D. (1998) Dynamic cross-linking by α-actinin determines the mechanical properties of actin filament networks. J. Biol. Chem., 273, 9570-9576.
52. Yu, D.H., Qu, C.K., Henegariu, O., Lu, X. and Feng, G.S. (1998) Protein-tyrosine phosphatase Shp-2 regulates cell spreading, migration and focal adhesion. J. Biol. Chem., 273, 21125-21131.
53. Zamir, E. et al. (2000) Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nat. Cell Biol., 2, 191-196.