Crk associates with a multimolecular Paxillin/GIT2/β-PIX complex and promotes Rac-dependent relocalization of Paxillin to focal contacts

Molecular Biology of the Cell

Volumn 14, Issue 7, 2003, Pages 2818-2831

  Lamorte, Louie ^a   Rodrigues, Sonia ^a   Sangwan, Veena ^b   Turner, Christopher E ^c   Park, Morag ^a,b  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CRK LIKE PROTEIN; GENE PRODUCT; PAXILLIN; PROTEIN BETA PIX; PROTEIN CRK; PROTEIN CRKII; PROTEIN GIT2; PROTEIN TYROSINE KINASE; RAC PROTEIN; SCATTER FACTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL JUNCTION; CELL SPREADING; COMPLEX FORMATION; CONTROLLED STUDY; EPITHELIUM; GENE OVEREXPRESSION; LAMELLIPODIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SRC HOMOLOGY DOMAIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADHERENS JUNCTIONS; ANIMALS; CELL ADHESION; CELL CYCLE PROTEINS; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETAL PROTEINS; DOGS; FOCAL ADHESIONS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEPATOCYTE GROWTH FACTOR; MUTATION; NUCLEAR PROTEINS; PAXILLIN; PHOSPHOPROTEINS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-CRK; PSEUDOPODIA;

ANIMALIA;

EID: 0037769892     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-08-0497     Document Type: Article

References (80)

1. Bagrodia, S., Taylor, S.J., Jordon, K.A., Van Aelst, L., and Cerione, R.A. (1998). A novel regulator of p21-activated kinases. J. Biol. Chem. 273, 23633-23636.
2. Barry, S., and Critchley, D. (1994). The RhoA-dependent assembly of focal adhesions in Swiss 3T3 cells is associated with increased tyrosine phosphorylafion and the recruitment of both pp125FAK and protein kinase C-delta to focal adhesions. J. Cell Sci. 107, 2033-2045.
3. Birchmeier, C., and Gherardi, E. (1998). Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 8, 404-410.
4. Birge, R.B., Fajardo, J.E., Reichman, C., Shoelson, S.E., Songyang, Z., Cantley, L.C., and Hanafusa, H. (1993). Identification and characterization of a high-affinity interaction between v-Crk and tyrosine-mephosphorylated Paxillin in CT10-transformed fibroblasts. Mol. Cell. Biol. 13, 4648-4656.
5. Boshans, R.L., Szanto, S., van Aelst, L., and D'Souza-Schorey, C. (2000). ADP-ribosylafion factor 6 regulates actin cytoskeleton remodeling in coordination with Rac1 and RhoA. Mol. Cell. Biol. 20, 3685-3694.
6. Boyer, B., Valles, A.M., and Edme, N. (2000). Induction and regulation of epithelial-mesenchymal transitions. Biochem. Pharmacol. 60, 1091-1099.
7. Brown, M.C., Perrotta, J.A., and Turner, C.E. (1996). Identification of LIM3 as the principal determinant of Paxillin focal adhesion localization and characterization of a novel motif on Paxillin directing vinculin and focal adhesion kinase binding. J. Cell Biol. 135, 1109-1123.
8. Brown, M.C., West, K,A., and Turner, C.E. (2002). Paxillin-dependent Paxillin kinase linker and p21-activated kinase localization to focal adhesions involves a multistep activation pathway. Mol. Biol. Cell 13, 1550-1565.
9. Brugnera, E., Haney, L., Grimsley, C., Lu, M., Walk, S.F., Tosello-Trampont, A.C., Macara, I.G., Madhani, H., Fink, G.R., and Ravichandran, K.S. (2002). Unconventional Rac-GEF activity is mediated through the Dock180 ELMO complex. Nat. Cell Biol. 4, 574-582.
10. Burridge, K., Turner, C.E., and Romer, L.H. (1992). Tyrosine phosphorylation of Paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119, 893-903.
11. Chavrier, P., and Goud, B. (1999). The role of ARF and Rab GTPases in membrane transport. Curr. Opin. Cell Biol. 11, 466-475.
12. Cho, S.Y., and Klemke, R.L. (2000). Extracellular-regulated kinase activation and CAS/Crk coupling regulate cell migration and suppress apoptosis during invasion of the extracellular matrix. J. Cell Biol. 149, 223-236.
13. 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.
14. de Curtis, I. (2001). Cell migration: GAPs between membrane traffic and the cytoskeleton. EMBO Rep. 2, 277-281.
15. Di Cesare, A., Paris, S., Albertinazzi, C., Dariozzi, S., Andersen, J., Mann, M., Longhi, R., and de Curtis, I. (2000). p95-APP1 links membrane transport to Rac-mediated reorganization of actin. Nat. Cell Biol. 2, 521-530.
16. Feller, S.M. (2001). Crk family adaptors-signalling complex formation and biological roles. Oncogene 20, 6348-6371.
17. Feller, S.M., Knudsen, B., and Hanafusa, H. (1994). c-Abl kinase regulates the protein binding activity of c-Crk. EMBO J. 13, 2341-2351.
18. Fixman, E.D., Fournier, T.M., Kamikura, D.M., Naujokas, M.A., and Park, M. (1996). Pathways downstream of Shc and Grb2 are required for cell transformation by the tpr-Met oncoprotein. J. Biol. Chem. 271, 13116-13122.
19. Franco, M., Peters, P.J., Boretto, J., van Donselaar, E., Neri, A., D'Souza-Schorey, C., and Chavrier, P. (1999). EFA6, a sec7 domain-containing exchange factor for ARF6, coordinates membrane recycling and actin cytoskeleton organization. EMBO J. 18, 1480-1491.
20. 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.
21. Gotoh, T., Hattori, S., Nakamura, S., Kitayama, H., Noda, M., Takai, Y., Kaibuchi, K., Matsui, H., Hatase, O., Takahashi, H., and et al. (1995). Identification of Rap1 as a target for the Crk SH3 domain-binding guanine nucleotide-releasing factor C3G. Mol. Cell. Biol. 15, 6746-6753.
22. Hagel, M., George, E.L., Kim, A., Tamimi, R., Opitz, S.L., Turner, C.E., Imamoto, A., and Thomas, S.M. (2002). The adaptor protein Paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol. Cell. Biol. 22, 901-915.
23. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
24. Harden, N., Lee, J., Loh, H.Y., Ong, Y.M., Tan, I., Leung, T., Manser, E., and Lim, L. (1996). A Drosophila homolog of the Rac- and Cdc42-activated serine/threonine kinase PAK is a potential focal adhesion and focal complex protein that colocalizes with dynamic actin structures. Mol. Cell. Biol. 16, 1896-1908.
25. Hemmeryckx, B., van Wijk, A., Reichert, A., Kaartinen, V., de Jong, R., Pattengale, P.K., Gonzalez-Gomez, I., Groffen, J., and Heisterkamp, N. (2001). Crk1 enhances leukemogenesis in BCR/ABL P190 transgenic mice. Cancer Res 61, 1398-1405.
26. Jackson, T,R., Brown, F.D., Nie, Z., Miura, K., Foroni, L., Sun, J., Hsu, V.W., Donaldson, J.G., and Randazzo, P.A. (2000). ACAPs are arf6 GTPase-activating proteins that function in the cell periphery. J. Cell Biol. 151, 627-638.
27. Kiyokawa, E., Hashimoto, Y., Kobayashi, S., Sugimura, H., Kurata, T., and Matsuda, M. (1998a). Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev. 12, 3331-3336.
28. Kiyokawa, E., Hashimoto, Y., Kurata, T., Sugimura, H., and Matsuda, M. (1998b). Evidence that DOCK180 up-regulates signals from the CrkII-p130(Cas) complex. J. Biol. Chem. 273, 24479-24484.
29. Klemke, R.L., Leng, J., Molander, R., Brooks, P.C., Vuori, K., and Cheresh, D.A. (1998). CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J. Cell Biol. 140, 961-972.
30. Kondo, A., Hashimoto, S., Yano, H., Nagayama, K., Mazaki, Y., and Sabe, H. (2000). A new Paxillin-binding protein, PAG3/Papalpha/KIAA0400, bearing an ADP-ribosylation factor GTPase-activating protein activity, is involved in Paxillin recruitment to focal adhesions and cell migration. Mol. Biol. Cell 11, 1315-1327.
31. Lamorte, L., Rodrigues, S., Naujokas, M., and Park, M. (2002a). Crk synergizes with epidermal growth factor for epithelial invasion and morphogenesis and is required for the met morphogenic program. J. Biol. Chem. 277, 37904-37911.
32. Lamorte, L., Royal, I., Naujokas, M., and Park, M. (2002b). Crk adapter proteins promote an epithelial-mesenchymal-like transition and are required for HGF-mediated cell spreading and breakdown of epithelial adherens junctions. Mol. Biol. Cell 13, 1449-1461.
33. Lauffenburger, D.A., and Horwitz, A.F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
34. Laukaitis, C.M., Webb, D.J., Donais, K., and Horwitz, A.F. (2001). Differential dynamics of alpha 5 integrin, Paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells. J. Cell Biol. 153, 1427-1440.
35. Liu, Y., Loijens, J.C., Martin, K.H., Karginov, A.V., and Parsons, J.T. (2002a). The association of ASAP1, an ADP ribosylation factor-GTPase activating protein, with focal adhesion kinase contributes to the process of focal adhesion assembly. Mol. Biol. Cell 13, 2147-2156.
36. Liu, Z.X., Yu, C.F., Nickel, C., Thomas, S., and Cantley, L.G. (2002b). Hepatocyte growth factor (HGF) induces ERK-dependent Paxillin phosphorylation and regulates Paxillin/FAK association. J. Biol. Chem. 9, 9
37. Manabe Ri, R., Kovalenko, M., Webb, D.J., and Horwitz, A.R. (2002). GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J. Cell Sci. 115, 1497-1510.
38. Manser, E., Huang, H.Y., Loo, T.H., Chen, X.Q., Dong, J.M., Leung, T., and Lim, L. (1997). Expression of constitutively active alpha-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17, 1129-1143.
39. Manser, E., Loo, T.H., Koh, C.G., Zhao, Z.S., Chen, X.Q., Tan, L., Tan, I., Leung, T., and Lim, L. (1998). PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell 1, 183-192.
40. Maroun, C.R., Holgado-Madruga, M., Royal, I., Naujokas, M.A., Fournier, T.M., Wong, A.J., and Park, M. (1999). The Gab1 PH domain is required for localization of Gab1 at sites of cell-cell contact and epithelial morphogenesis downstream from the met receptor tyrosine kinase. Mol. Cell. Biol. 19, 1784-1799.
41. Matafora, V., Paris, S., Dariozzi, S., and de Curtis, I. (2001). Molecular mechanisms regulating the subcellular localization of p95-APP1 between the endosomal recycling compartment and sites of actin organization at the cell surface. J. Cell Sci. 114, 4509-4520.
42. Matsuda, M., Tanaka, S., Nagata, S., Kojima, A., Kurata, T., and Shibuya, M. (1992). Two species of human CRK cDNA encode proteins with distinct biological activities. Mol. Cell. Biol. 12, 3482-3489.
43. Mazaki, Y., et al. (2001). An ADP-ribosylation factor GTPase-activating protein Git2-short/KIAA0148 is involved in subcellular localization of Paxillin and actin cytoskeletal organization. Mol. Biol. Cell 12, 645-662.
44. 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.
45. 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.
46. Nolan, K.M., Barrett, K., Lu, Y., Hu, K.Q., Vincent, S., and Settleman, J. (1998). Myoblast city, the Drosophila homolog of DOCK180/CED-5, is required in a Rac signaling pathway utilized for multiple developmental processes. Genes Dev. 12, 3337-3342.
47. Norman, J.C., Jones, D., Barry, S.T., Holt, M.R., Cockcroft, S., and Critchley, D.R. (1998). ARF1 mediates Paxillin recruitment to focal adhesions and potentiates Rho-stimulated stress fiber formation in intact and permeabilized Swiss 3T3 fibroblasts. J. Cell Biol. 143, 1981-1995.
48. Obermeier, A., Ahmed, S., Manser, E., Yen, S.C., Hall, C., and Lim, L. (1998). PAK promotes morphological changes by acting upstream of Rac. EMBO J. 17, 4328-4339.
49. Palacios, F., Price, L., Schweitzer, J., Collard, J.G., and D'Souza-Schorey, C. (2001). An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J. 20, 4973-4986.
50. Petit, V., Boyer, B., Lentz, D., Turner, C.E., Thiery, J.P., and Valles, A.M. (2000). Phosphorylation of tyrosine residues 31 and 118 on Paxillin regulates cell migration through an association with CRK in NBT-II cells. J. Cell Biol. 148, 957-970.
51. Potempa, S., and Ridley, A.J. (1998). Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/scatter factor-induced adherens junction disassembly. Mol. Biol. Cell 9, 2185-2200.
52. Premont, R.T., Claing, A., Vitale, N., Perry, S.J., and Lefkowitz, R.J. (2000). The GIT family of ADP-ribosylation factor GTPase-activating proteins. Functional diversity of GIT2 through alternative splicing. J. Biol. Chem. 275, 22373-22380.
53. Radhakrishna, H., Al-Awar, O., Khachikian, Z., and Donaldson, J.G. (1999). ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J. Cell Sci. 112, 855-866.
54. Randazzo, P.A., Andrade, J., Miura, K., Brown, M.T., Long, Y.Q., Stauffer, S., Roller, P., and Cooper, J.A. (2000). The Arf GTPase-activating protein ASAP1 regulates the actin cytoskeleton. Proc. Natl. Acad. Sci. USA 97, 4011-4016.
55. Reddien, P.W., and Horvitz, H.R. (2000). CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2, 131-136.
56. Reichman, C.T., Mayer, B.J., Keshav, S., and Hanafusa, H. (1992). The product of the cellular crk gene consists primarily of SH2 and SH3 regions. Cell Growth Differ. 3, 451-460.
57. Ridley, A.J., Comoglio, P.M., and Hall, A. (1995). Regulation of scatter factor/hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol. Cell. Biol. 15, 1110-1122.
58. 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.
59. Royal, I., Lamarche-Vane, N., Lamorte, L., Kaibuchi, K., and Park, M. (2000). Activation of Cdc42, Rac, PAK, and Rho-kinase in response to hepatocyte growth factor differentially regulates epithelial cell colony spreading and dissociation. Mol. Biol. Cell 11, 1709-1725.
60. Royal, I., and Park, M. (1995). Hepatocyte growth factor induced scatter of MDCK cells requires phosphatidylinositol 3-kinase. J. Biol. Chem. 270, 27780-27787.
61. Santy, L.C., and Casanova, J.E. (2001). Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J. Cell Biol. 154, 599-610.
62. Sastry, S.K., and Burridge, K. (2000). Focal adhesions: a nexus for intracellular signaling and cytoskeletal dynamics. Exp. Cell Res. 261, 25-36.
63. Schaller, M.D., and Schaefer, E.M. (2001). Multiple stimuli induce tyrosine phosphorylation of the Crk-binding sites of Paxillin. Biochem. J. 360, 57-66.
64. Spencer, K.S., Graus-Porta, D., Leng, J., Hynes, N.E., and Klemke, R.L. (2000). ErbB2 is necessary for induction of carcinoma cell invasion by ErbB family receptor tyrosine kinases. J. Cell Biol. 148, 385-397.
65. Stoker, M., Gherardi, E., Perryman, M., and Gray, J. (1987). Scatter factor is a fibroblast-derived modulator of epithelial cell mobility. Nature 327, 239-242.
66. ten Hoeve, J., Morris, C., Heisterkamp, N., and Groffen, J. (1993). Isolation and chromosomal localization of CRKL, a human crk-like gene. Oncogene 8, 2469-2474.
67. Turner, C.E. (2000). Paxillin and focal adhesion signalling. Nat. Cell Biol 2, E231-E236.
68. Turner, C.E., Brown, M.C., Perrotta, J.A., Riedy, M.C., Nikolopoulos, S.N., McDonald, A.R., Bagrodia, S., Thomas, S., and Leventhal, P.S. (1999). Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: a role in cytoskeletal remodeling. J. Cell Biol. 145, 851-863.
69. Turner, C.E., West, K.A., and Brown, M.C. (2001). Paxillin-ARF GAP signaling and the cytoskeleton. Curr. Opin. Cell Biol. 13, 593-599.
70. Uchida, H., Kondo, A., Yoshimura, Y., Mazaki, Y., and Sabe, H. (2001). PAG3/Papalpha/KIAA0400, a GTPase-activating protein for ADP-ribosylation factor (ARF), regulates ARF6 in Fcgamma receptor-mediated phagocytosis of macrophages. J. Exp. Med. 193, 955-966.
71. Uehata, M., et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
72. Uemura, N., and Griffin, J.D. (1999). The adapter protein Crk1 links Cb1 to C3G after integrin ligation and enhances cell migration. J. Biol. Chem. 274, 37525-37532.
73. Webb, D.J., Parsons, J.T., and Horwitz, A.F. (2002). Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again. Nat. Cell Biol. 4, E97-E100.
74. Weidner, K.M., Behrens, J., Vandekerckhove, J., and Birchmeier, W. (1990). Scatter Factor: Molecular characteristics and effect on the invasiveness of epithelial cells. J. Cell Biol. 111, 2097-2108.
75. Weidner, K.M., Sachs, M., and Birchmeier, W. (1993). The Met receptor tyrosine kinase transduces motility, proliferation, and morphogenic signals of scatter factor/hepatocyte growth factor in epithelial cells. J. Cell Biol. 121, 145-154.
76. West, K.A., Zhang, H., Brown, M.C., Nikolopoulos, S.N., Riedy, M.C., Horwitz, A.F., and Turner, C.E. (2001). The LD4 motif of Paxillin regulates cell spreading and motility through an interaction with Paxillin kinase linker (PKL). J. Cell Biol. 154, 161-176.
77. Wittmann, T., and Waterman-Storer, C.M. (2001). Cell motility: can Rho GTPases and microtubules point the way? J. Cell Sci. 114, 3795-3803.
78. Zhang, Q., Calafat, J., Janssen, H., and Greenberg, S. (1999). ARF6 is required for growth factor- and rac-mediated membrane ruffling in macrophages at a stage distal to rac membrane targeting. Mol. Cell. Biol. 19, 8158-8168.
79. Zhao, Z.S., Manser, E., Loo, T.H., and Lim, L. (2000). Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol. Cell. Biol. 20, 6354-6363.
80. Zhu, H., Naujokas, M.A., and Park, M. (1994). Receptor chimeras indicate that the Met tyrosine kinase mediates the motility and morphogenic responses of hepatocyte growth/scatter factor. Cell Growth Differ 5, 359-366.