Induction of p130cas signaling complex formation upon integrin-mediated cell adhesion: A role for Src family kinases

Molecular and Cellular Biology

Volumn 16, Issue 6, 1996, Pages 2606-2613

  Vuori, Kristiina ^a   Hirai, Hisamaru ^b   Aizawa, Shinichi ^c   Ruoslahti, Erkki ^a  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; PROTEIN KINASE P60; BCAR1 PROTEIN, MOUSE; BCAR1 PROTEIN, RAT; CELL ADHESION MOLECULE; CRK ASSOCIATED SUBSTRATE PROTEIN; CRK LIKE PROTEIN; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 1; HYBRID PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; PROTEIN; PROTEIN P130; PROTEIN TYROSINE KINASE; PTK2 PROTEIN, MOUSE; PTK2 PROTEIN, RAT; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TYROSINE;

ANIMAL CELL; ARTICLE; CELL ADHESION; ENZYME PHOSPHORYLATION; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; BINDING SITE; CELL CULTURE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MUTATION; PHOSPHORYLATION; PHYSIOLOGY; RAT; SRC HOMOLOGY DOMAIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BINDING SITES; CELL ADHESION; CELL ADHESION MOLECULES; CELLS, CULTURED; CRK-ASSOCIATED SUBSTRATE PROTEIN; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; INTEGRINS; MICE; MUTATION; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTEINS; RATS; RECOMBINANT FUSION PROTEINS; RETINOBLASTOMA-LIKE PROTEIN P130; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; SRC-FAMILY KINASES; TYROSINE;

EID: 0029664531     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.6.2606     Document Type: Article

References (66)

1. Avraham, S., R. London, Y. Fu, S. Ota, D. Hiregowdara, J. Li, S. Jiang, L. M. Pasztor, R. A. White, J. E. Groopman, and H. Avraham. 1995. Identification and characterization of a novel related adhesion focal tyrosine kinase (RAFTK) from megakaryocytes and brain. J. Biol. Chem. 270:27742-27751.
2. Bhattacharya, S., C. Fu, J. Bhattacharya, and S. Greenberg. 1995. Soluble ligands of the αvβ3 integrin mediate enhanced tyrosine phosphorylation of multiple proteins in adherent bovine pulmonary artery endothelial cells. J. Biol. Chem. 270:16781-16787.
3. Birge, R. B., J. E. Fajardo, B. J. Mayer, and H. Hanafusa. 1992. Tyrosine-phosphorylated epidermal growth factor receptor and cellular p130 provide high affinity binding substrates to analyze Crk-phosphotyrosine-dependent interactions in vitro. J. Biol. Chem. 267:10588-10595.
4. Birge, R. B., J. E. Fajardo, C. Reichman, S. E. Shoelson, Z. Songyang, L. C. Cantley, and H. Hanafusa. 1993. Identification and characterization of a high-affinity interaction between v-Crk and tyrosine-phosphorylated paxillin in CT10-transformed fihroblasts. Mol. Cell. Biol. 13:4648-4656.
5. Bockholt, S. M., and K. Burridge. 1993. Cell spreading on extracellular matrix proteins induces tyrosine phosphorylation of tensin. J. Biol. Chem. 468:14565-14567.
6. Bockholt, S. M., and K. Burridge. 1995. An examination of focal adhesion formation and tyrosine phosphorylation in fibroblasts isolated from src, fyn, and yes mice. Cell Adhes. Commun. 3:91-100.
7. FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119:893-903.
8. Calalb, M. B., T. R. Polte, and S. K. Hanks. 1995. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol. Cell. Biol. 15:954-963.
9. FAK. J. Biol. Chem. 269:20567-20574.
10. Chen, H. C., and J.-L. Guan. 1994. Association of focal adhesion kinase with its potential substrate phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 91:10148-10152.
11. Chen, Q., M. S. Kinch, T. H. Lin, K. Burridge, and R. L. Juliano. 1994. Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J. Biol. Chem. 269:26602-26605.
12. Clark, E. A., and J. S. Brugge. 1995. Integrins and signal transduction pathways: the road taken. Science 268:233-239.
13. FAK. Mol. Cell. Biol. 14:147-155.
14. FAK. Mol. Cell. Biol. 15:2819-2827.
15. Feller, S. M., B. Knudsen, and H. Hanafusa. 1994. c-Abl kinase regulates the protein binding activity of c-Crk. EMBO J. 13:2341-2351.
16. Feller, S. M., B. Knudsen, and H. Hanafusa. 1995 Cellular proteins binding to the first Src homology 3 (SH3) domain of the proto-oncogene product c-Crk indicate Crk-specific signaling pathways. Oncogene 10:1465-1473.
17. Feller, S. M., R. Ren, H. Hanafusa, and D. Baltimore. 1994. SH2 and SH3 domains as molecular adhesives: the interactions of Crk and Abl. Trends Biochem. Sci. 19:453-458.
18. Frech, M., J. John, V. Pizon, P. Chardin, A. Tavitian, R. Clark, F. McCormick, and A. Wittinghofer. 1990. Inhibition of GTPase activating protein stimulation of Ras-p21 GTPase by the Krev-1 gene product. Science 249:159-171.
19. 18a.Frisch, S. M., K. Vuori, and E. Ruoslahti. Submitted for publication.
20. Gale, N. W., S. Kaplan, E. J. Lowenstein, J. Schlessinger, and D. Bar-Sagi. 1993. Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature (London) 363:88-92.
21. Gotoh, T., S. Hattori, S. Nakamura, H. Kitayama. M. Noda, Y. Takai, K. Kaibuchi, H. Matsui, O. Hatase, H. Takahashi, T. Kurata, and M. Matsuda. 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. Gout, I., R. Dhand, I. D. Hiles, M. J. Fry, G. Panayotou, P. Das, O. Truong, N. F. Totty, J. Hsuan, and G. W. Booker. 1993. The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell 75:25-36.
23. Guinebault, C., B. Payrastre. C. Racaud-Sultan, H. Mazarguil, M. Breton, G. Mauco, M. Plantavid, and H. Chap. 1995. Integrin-dependent translocation of phosphoinositide 3-kinase to the cytoskeleton of thrombin-activated platelets involves specific interactions of p85 a with actin filaments and focal adhesion kinase. J. Cell Biol. 129:831-842.
24. Hata, Y., A. Kikuchi, T. Sasaki, M. D. Schaber, J. B. Gibbs, and Y. Takai. 1990. Inhibition of the ras p21 GTPase-activating protein-stimulated GTPase activity of c-Ha-ras p21 by smg p21 having the same putative effector domain as ras p21s. J. Biol. Chem. 265:7104-7107.
25. FAK, to cellular focal adhesions. J. Cell Biol. 123:993-1005.
26. c-src. Mol. Cell. Biol. 10:1307-1318.
27. Hynes, R. O. 1992. Integrins: versatility, modulation and signaling in cell adhesion. Cell 69:11-25.
28. Ille, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, T. Yamamoto, and S. Aizawa. 1995. Reduced cell motility and enhanced focal contact formation in cells from FAK-deficient mice. Nature (London) 377:539-544.
29. Imamoto, A., and P. Soriano. 1993. Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell 73:1117-1124.
30. Jhun, B. H., D. W. Rose, B. L. Seely, L. Rameh, L. Cantley, A. R. Saltiel, and J. M. Olefsky. 1994. Microinjection of the SH2 domain of the 85-kilodalton subunit of phosphatidylinositol 3-kinase inhibits insulin-induced DNA syn-thesis and c-fos expression. Mol. Cell. Biol. 14:7465-7475.
31. Juliano, R. L., and S. Haskill. 1993. Signal transduction from the extracellular matrix. J. Cell Biol. 120:577-585.
32. Kanner, S. B., A. B. Reynolds, R. R. Vines, and J. T. Parsons. 1990. Monoclonal antibodies to individual tyrosine-phosphorylated protein substrates of oncogene-encoded tyrosine kinases. Proc. Natl. Acad. Sci. USA 87:3328-3332.
33. Kanner, S. B., A. B. Reynolds, H. C. Wang, R. R. Vines, and J. T. Parsons. 1991. The SH2 and SH3 domains of pp60src direct stable association with tyrosine phosphorylated proteins p130 and p110. EMBO J. 10:1689-1698.
34. Knudsen, B. S., S. M. Feller, and H. Hanafusa. 1994. Four proline-rich sequences of the guanine-nucleotide exchange factor C3G hind with unique specificity to the first Src homology 3 domain of Crk. J. Biol. Chem. 269:32781-32787.
35. 2+-induced regulation of ion channel and MAP kinase functions. Nature (London) 376:737-745.
36. Lowenstein, E. J., R. J. Daly, A. G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E. Y. Skolnik, D. Bar-Sagi, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70:431-442.
37. Matsuda, M., Y. Hashimoto, K. Muroya, H. Hasegawa, T. Kurata, S. Tanaka, S. Nakamura, and S. Hattori. 1994. CRK protein binds to two guanine nucleotide-releasing proteins for the Ras family and modulates nerve growth factor-induced activation of Ras in PC12 cells. Mol. Cell. Biol. 14:5495-5500.
38. Matsuda, M., B. J. Mayer, Y. Fukui, and H. Hanafusa. 1990. Binding of transforming protein, P47gag-crk, to a broad range of phosphotyrosine-containing proteins. Science 248:1537-1539.
39. crk-2. J. Biol. Chem. 270:269-273.
40. Nada, S., M. Okada, S. Aizawa, and H. Nakagawa. 1994. Identification of major tyrosine-phosphorylated proteins in Csk-deficient cells. Oncogene 9:3571-3578.
41. Nassar, N., G. Horn, C. Herrman, A. Sherer, F. McCormick, and A. Wittinghofer. 1995. The 2.2 Å crystal structure of the Ras-binding domain of the serine-threonine kinase c-Raf-1 in complex with Rap1A and a GTP analogue. Nature (London) 375:554-560.
42. Cas, a src homology 3-containing molecule having multiple Src homology 2-binding motifs. J. Biol. Chem. 270:15398-15402.
43. Ogawa, S., H. Toyoshima, H. Kozutsumi, K. Hagiwara, R. Sakai, T. Tanaka, N. Hirano, H. Mano, Y. Yazaki, and H. Hirai. 1994. The C-terminal SH3 domain of the mouse c-Crk protein negatively regulates tyrosine-phosphorylation of Crk associated p130 in rat 3Y1 cells. Oncogene 9:1669-1678.
44. Pawson, T. 1995. Protein modules and signaling networks. Nature (London) 373:573-580.
45. Petch, L. A., S. M. Bockholt, A. Bouton, J. T. Parsons, and K. Burridge. 1995. Adhesion-induced tyrosine phosphorylation of the p130 SRC substrate. J. Cell Sci. 108:1371-1379.
46. Cas. Proc. Natl. Acad. Sci. USA 92:10678-10682.
47. Ren, R, Z. S. Ye, and D. Baltimore. 1994. Abl protein-tyrosine kinase selects the Crk adapter as a substrate using SH3-binding sites. Genes Dev. 8:783-795.
48. Ruoslahti, E. 1991. Integrins. J. Clin. Invest. 87:1-5.
49. Sabe, H., A. Hata, M. Okada, H. Nakagawa, and H. Hanafusa. 1994. Analysis of the binding of the Src homology 2 domain of Csk to tyrosine-phosphorylated proteins in the suppression and mitotic activation of c-Src, Proc. Natl. Acad. Sci. USA 91:3984-3988.
50. Sakai, R., A. Iwaniatsu, N. Hirano, S. Ogawa, T. Tanaka, H. Mano, Y. Yazaki, and H. Hirai. 1994. A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylation-dependent manner. EMBO J. 13:3748-3756.
51. Sasaki, H., K. Nagura, M. Ishino, H. Tobioka, K. Kotani, and T. Sasaki. 1995. Cloning and characterization of cell adhesion kinase β, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily. J. Biol. Chem. 270:21206-21219.
52. Sasaoka, T., D. W. Rose, B. H. Jhun, A. R. Saltiel, B. Draznin, and J. M. Olefsky. 1994. Evidence for a functional role of She proteins in mitogenic signaling induced by insulin, insulin-like growth factor-1, and epidermal growth factor. J. Biol. Chem. 269:13689-13694.
53. src. Mol. Cell. Biol. 14:1680-1688.
54. Schaller, M. D., C. A. Otey, J. D. Hildebrand, and J. T. Parsons. 1995. Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J. Cell Biol. 130:1181-1187.
55. FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15:2635-2645.
56. Schlaepfer, D. D., S. K. Hanks, T. Hunter, and P. van der Geer. 1994. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature (London) 372:786-791.
57. Sells, M. A., and J. Chernoff. 1995. Epitope-tag vectors for eukaryotic protein production. Gene 152:187-189.
58. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherjchia coli as fusions with glutathione S-transferase. Gene 67:31-40.
59. Soriano, P., C. Montgomery, R. Geske, and A. Bradley. 1991. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64:693-702.
60. fyn mutant mice display differential signaling in thymocytes and peripheral T cells. Cell 70:741-750.
61. Tanaka, S., T. Morishita, Y. Hashimoto, S. Hattori, S. Nakamura, M. Shibuya, K. Matuoka, T. Takenawa, T. Kurata, and K. Nagashima. 1994. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins. Proc. Natl. Acad. Sci. USA 91:3443-3447.
62. Thomas, S. M., P. Soriano, and A. Imamoto. 1995. Specific and redundant roles of Src and Fyn in organizing the cytoskeleton. Nature (London) 376:267-271.
63. Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem. 270:22259-22262.
64. Xing, Z., H.-C. Chen, J. K. Nowlen, S. J. Taylor, D. Shalloway, and J.-L. Guan. 1994. Direct interaction of v-Src with the focal adhesion kinase mediated by the Src SH2 domain. Mol. Biol. Cell 5:413-421.
65. Yoshlda, Y., M. Kawata, Y. Miura, T. Musha, T. Sasaki, A. Kikuchi, and Y. Takai. 1992. Microinjection of smg/rap1/Krev-1 p21 into Swiss 3T3 cells induces DNA synthesis and morphological changes. Mol. Cell. Biol. 12:3407-3414.
66. Zhu, X, and R. K. Assoinn. 1995. Integrin-dependent activation of MAP kinase: a link to shape-dependent cell proliferation. Mol. Biol. Cell 6:273-282.