The cytoplasmic tyrosines of integrin subunit β1 are involved in focal adhesion kinase activation

Molecular and Cellular Biology

Volumn 20, Issue 15, 2000, Pages 5758-5765

  Wennerberg, Krister ^a,e   Armulik, Annika ^a   Sakai, Takao ^b,c   Karlsson, Marjam ^a   Fässler, Reinhard ^c   Schaefer, Erik M ^d   Mosher, Deane F ^b   Johansson, Staffan ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c LUND UNIVERSITY   (Sweden)

^d BioSource International   (United States)

^e UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; INTEGRIN; TYROSINE;

ARTICLE; CELL CULTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE MUTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMINO ACID SUBSTITUTION; ANTIGENS, CD29; CRK-ASSOCIATED SUBSTRATE PROTEIN; CYTOPLASM; CYTOSKELETAL PROTEINS; ENZYME ACTIVATION; FOCAL ADHESION PROTEIN-TYROSINE KINASES; MICROFILAMENT PROTEINS; MUTATION; PAXILLIN; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTEINS; RETINOBLASTOMA-LIKE PROTEIN P130; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TYROSINE;

EID: 0033942173     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.15.5758-5765.2000     Document Type: Article

References (53)

1. Blystone, S. D., F. P. Lindberg, M. P. Williams, K. P. McHugh, and E. J. Brown. 1996. Inducible tyrosine phosphorylation of the β3 integrin requires the αV integrin cytoplasmic tail. J. Biol. Chem. 271:31458-31462.
2. Bockholt, S. M., and K. Burridge. 1993. Cell spreading on extracellular matrix proteins induces tyrosine phosphorylation of tensin. J. Biol. Chem. 268:14565-14567.
3. Bottger, B. A., U. Hedin, S. Johansson, and J. Thyberg. 1989. Integrin-type fibronectin receptors of rat arterial smooth muscle cells: isolation, partial characterization and role in cytoskeletal organisation and control of differentiated properties. Differentiation 41:158-167.
4. Bouton, A. H., and M. R. Burnham. 1997. Detection of distinct pools of the adapter protein p130CAS using a panel of monoclonal antibodies. Hybridoma 16:403-411.
5. Burridge, K., and M. Chrzanowska-Wodnicka. 1996. Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12:463-518.
6. 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.
7. Cary, L. A., and J. L. Guan. 1999. Focal adhesion kinase in integrin-mediated signaling. Front. Biosci. 4:D102-D113.
8. Cary, L. A., D. C. Han, T. R. Polte, S. K. Hanks, and J. L. Guan. 1998. Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J. Cell Biol. 140:211-221.
9. Clark, E. A., W. G. King, J. S. Brugge, M. Symons, and R. O. Hynes. 1998. Integrin-mediated signals regulated by members of the rho family of GTPases. J. Cell Biol. 142:573-586.
10. Craig, S. W., and R. P. Johnson. 1996. Assembly of focal adhesions: progress, paradigms, and portents. Curr. Opin. Cell Biol. 8:74-85.
11. Dedhar, S., and G. E. Hannigan. 1996. Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr. Opin. Cell Biol. 8:657-669.
12. Eisenmann, K. M., J. B. McCarthy, M. A. Simpson, P. J. Keely, J. L. Guan, K. Tachibana, L. Lim, E. Manser, L. T. Furcht, and J. Iida. 1999. Melanoma chondroitin sulphate proteoglycan regulates cell spreading through Cdc42. Ack-1 and p130cas. Nat. Cell Biol. 1:507-513.
13. Fässler, R., M. Pfaff, J. Murphy, A. A. Noegel, S. Johansson, R. Timpl, and R. Albrecht. 1995. Lack of β1 integrin gene in embryonic stem cells affects morphology, adhesion, and migration but not integration into the inner cell mass of blastocysts. J. Cell Biol. 128:979-988.
14. Hamasaki, K., T. Mimura, N. Morino, H. Furuya, T. Nakamoto, S. Aizawa, C. Morimoto, Y. Yazaki, H. Hirai, and Y. Nojima. 1996. Src kinase plays an essential role in integrin-mediated tyrosine phosphorylation of Crk-associated substrate p130Cas. Biochem. Biophys. Res. Commun. 222:338-343.
15. Hibbs, M. L., S. Jakes, S. A. Stacker, R. W. Wallace, and T. A. Springer. 1991. The cytoplasmic domain of the integrin lymphocyte function-associated antigen 1 β subunit: sites required for binding to intercellular adhesion molecule 1 and the phorbol ester-stimulated phosphorylation site. J. Exp. Med. 174:1227-1238.
16. Hibbs, M. L., H. Xu, S. A. Stacker, and T. A. Springer. 1991. Regulation of adhesion of ICAM-1 by the cytoplasmic domain of LFA-1 integrin β subunit. Science 251:1611-1613.
17. Hirst, R., A. Horwitz, C. Buck, and L. Rohrschneider. 1986. Phosphorylation of the fibronectin receptor complex in cells transformed by oncogenes that encode tyrosine kinases. Proc. Natl. Acad. Sci. USA 83:6470-6474.
18. Ilic, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, T. Yamamoto, et al. 1995. Reduced cell motilily and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539-544.
19. Johansson, M. W., E. Larsson, B. Luning, E. B. Pasquale, and E. Ruoslahti. 1994. Altered localization and cytoplasmic domain-binding properties of tyrosine-phosphorylated β1 integrin. J. Cell Biol. 126:1299-1309.
20. Khwaja, A., P. Rodriguez-Viciana, S. Wennstrom, P. H. Warne, and J. Downward. 1997. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J. 16:2783-2793.
21. Klemke, R. L., J. Leng, R. Molander, P. C. Brooks, K. Vuori, and D. A. Cheresh. 1998. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J. Cell Biol. 140:961-972.
22. Klint, P., S. Kanda, and L. Claesson-Welsh. 1995. She and a novel 89-kDa component couple to the Grb2-Sos complex in fibroblast growth factor-2-stimulated cells. J. Biol. Chem. 270:23337-23344.
23. LaFlamme, S. E., L. A. Thomas, S. S. Yamada, and K. M. Yamada. 1994. Single suhunit chimeric integrins as mimics and inhibitors of endogenous integrin functions in receptor localization, cell spreading and migration, and matrix assembly. J. Cell Biol. 126:1287-1298.
24. Law, D. A., F. R. DeGuzman, P. Heiser, K. Ministri-Madrid, N. Killeen, and D. R. Phillips. 1999. Integrin cytoplasmic tyrosine motif is required for outside-in αIIbβ3 signalling and platelet function. Nature 401:808-811.
25. Law, D. A., L. Nannizzi-Alaimo, and D. R. Phillips. 1996. Outside-in integrin signal transduction. αIIbβ3-(GP IIb IIIa) tyrosine phosphorylation induced by platelet aggregation. J. Biol. Chem. 271:10811-10815.
26. Leong, L., P. E. Hughes, M. A. Schwartz, M. H. Ginsberg, and S. J. Shattil. 1995. Integrin signaling: roles for the cytoplasmic tails of αIIbβ3 in the tyrosine phosphorylation of pp125FAK. J. Cell Sci. 108:3817-3825.
27. Lewis, J. M., and M. A. Schwartz. 1995. Mapping in vivo associations of cytoplasmic proteins with integrin β1 cytoplasmic domain mutants. Mol. Biol. Cell 6:151-160.
28. Longhurst, C. M., and L. K. Jennings. 1998. Integrin-mediated signal transduction. Cell. Mol. Life Sci. 54:514-526.
29. Marcantonio, E. E., J. L. Guan, J. E. Trevithick, and R. O. Hynes. 1990. Mapping of the functional determinants of the integrin β1 cytoplasmic domain by site-directed mutagenesis. Cell Regul. 1:597-604.
30. Murakami, H., T. Iwashita, N. Asai, Y. Iwata, S. Narumiya, and M. Takahashi. 1999. Rho-dependent and -independent tyrosine phosphorylation of focal adhesion kinase, paxillin and p130Cas mediated by Ret kinase. Oncogene 18:1975-1982.
31. Nojima, Y., N. Morino, T. Mimura, K. Hamasaki, H. Furuya, R. Sakai, T. Sato, K. Tachibana, C. Morimoto, Y. Yazaki, et al. 1995. Integrin-mediated cell adhesion promotes tyrosine phosphorylation of p130Cas, a Src homology 3-containing molecule having multiple Src homology 2-binding motifs. J. Biol. Chem. 270:15398-15402.
32. O'Toole, T. E., Y. Katagiri, R. J. Faull, K. Peter, R. Tamura, V. Quaranta, J. C. Loftus, S. J. Shattil, and M. H. Ginsberg. 1994. Integrin cytoplasmic domains mediate inside-out signal transduction. J. Cell Biol. 124:1047-1059.
33. O'Toole, T. E., D. Mandelman, J. Forsyth, S. J. Shattil, E. F. Plow, and M. H. Ginsberg. 1991. Modulation of the affinity of integrin αIIbβ3 (GPIIb-IIIa) by the cytoplasmic domain of αIIb. Science 254:845-847.
34. Owen, J. D., P. J. Ruest, D. W. Fry, and S. K. Hanks. 1999. Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto-and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2. Mol. Cell. Biol. 19:4806-4818.
35. Qi, J. H., N. Ito, and L. Claesson-Welsh. 1999. Tyrosine phosphatase SHP-2 is involved in regulation of platelet-derived growth factor-induced migration. J. Biol. Chem. 274:14455-14463.
36. Reiske, H. R., S. C. Kao, L. A. Cary, J. L. Guan, J. F. Lai, and H. C. Chen. 1999. Requirement of phosphatidylinositol 3-kinase in focal adhesion kinase-promoted cell migration. J. Biol. Chem. 274:12361-12366.
37. Richardson, A., R. K. Malik, J. D. Hildebrand, and J. T. Parsons. 1997. Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation. Mol. Cell. Biol. 17:6906-6914.
38. Sakai, T., Q. Zhang, R. Fässler, and D. F. Mosher. 1998. Modulation of β1A integrin functions by tyrosine residues in the β1 cytoplasmic domain. J. Cell Biol. 141:527-538.
39. Schaffner-Reckinger, E., V. Gouon, C. Melchior, S. Plancon, and N. Kieffer. 1998. Distinct involvement of β3 integrin cytoplasmic domain tyrosine residues 747 and 759 in integrin-mediated cytoskeletal assembly and phospho-tyrosine signaling. J. Biol. Chem. 273:12623-12632.
40. src. Mol. Cell. Biol. 14: 1680-1688.
41. FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15:2635-2645.
42. Schlaepfer, D. D., and T. Hunter. 1998. Integrin signalling and tyrosine phosphorylation: just the FAKs? Trends Cell Biol. 8:151-157.
43. Schlaepfer, D. D., K. C. Jones, and T. Hunter. 1998. Multiple Grb2-mediated integrin-stimulated signaling pathways to ERK2/mitogen-activated protein kinase: summation of both c-Src-and focal adhesion kinase-initiated tyrosine phosphorylation events. Mol. Cell. Biol. 18:2571-2585.
44. Shen, Y., and M. D. Schaller. 1999. Focal adhesion targeting: the critical determinant of FAK regulation and substrate phosphorylation. Mol. Biol. Cell 10:2507-2518.
45. Sieg, D. J., D. Ilic, K. C. Jones, C. H. Damsky, T. Hunter, and D. D. Schlaepfer. 1998. Pyk2 and src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but pyk2 does not fully function to enhance FAK-cell migration. EMBO J. 17:5933-5947.
46. Smilenov, L., E. Forsberg, I. Zeligman, M. Sparrman, and S. Johansson. 1992. Separation of fibronectin from a plasma gelatinase using immobilized metal affinity chromatography. FEBS Lett. 302:227-230.
47. Tachibana, K., T. Urano, H. Fujita, Y. Ohashi, K. Kamiguchi, S. Iwata, H. Hirai, and C. Morimoto. 1997. Tyrosine phosphorylation of Crk-associated substrates by focal adhesion kinase. A putative mechanism for the integrin-mediated tyrosine phosphorylation of Crk-associated substrates. J. Biol. Chem. 272:29083-29090.
48. Tahiliani, P. D., L. Singh, K. L. Auer, and S. E. LaFlamme. 1997. The role of conserved amino acid motifs within the integrin β3 cytoplasmic domain in triggering focal adhesion kinase phosphorylation. J. Biol. Chem. 272:7892-7898.
49. Vuori, K. 1998. Integrin signaling: tyrosine phosphorylation events in focal adhesions. J. Membr. Biol. 165:191-199.
50. cas signaling complex formation upon integrin-mediated cell adhesion: a role for Src family kinases. Mol. Cell. Biol. 16:2606-2613.
51. Wennerberg, K., R. Fässler, B. Wärmegåard, and S. Johansson. 1998. Mutational analysis of the potential phosphorylation sites in the cytoplasmic domain of integrin β1A. Requirement for threonines 788-789 in receptor activation. J. Cell Sci. 111:1117-1126.
52. Wennerberg, K., L. Lohikangas, D. Gullberg, M. Pfaff, S. Johansson, and R. Fässler. 1996. β1 integrin-dependent and -independent polymerization of fibronectin. J. Cell Biol. 132:227-238.
53. Yatohgo, T., M. Izumi, H. Kashiwagi, and M. Hayashi. 1988. Novel purification of vitronectin from human plasma by heparin affinity chromatography. Cell Struct. Funct. 13:281-292.