Serine and threonine phosphorylation of the paxillin LIM domains regulates paxillin focal adhesion localization and cell adhesion to fibronectin

Molecular Biology of the Cell

Volumn 9, Issue 7, 1998, Pages 1803-1816

  Brown, Michael C ^a   Perrotta, Joseph A ^a   Turner, Christopher E ^a  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; PAXILLIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CELL ADHESION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALIA; AVES;

EID: 0031847578     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.7.1803     Document Type: Article

References (60)

1. Arber, S., and Caroni, P. (1996). Specificity of single LIM motifs in targeting and LIM/LIM interactions in situ. Genes Dev. 10, 289-300.
2. 3 mediates chemotactic and haptotactic motility in human melanoma cells through different signaling pathways. J. Biol. Chem. 271, 3247-3254.
3. 1 integrin localization. Exp. Cell Res. 222, 10-15.
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. Bellis, S.L., Perrotta, J.A., Curtis, M.S., and Turner, C.E. (1997). Adhesion of fibroblasts to fibronectin stimulates both serine and tyrosine phosphorylation of paxillin. Biochem. J. 325, 375-381.
6. 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.
7. Burridge, K. (1986). Substrate adhesion in normal and transformed fibroblasts: organization and regulation of cytoskeletal, membrane and extracellular matrix components at focal contacts. Cancer Rev. 4, 18-78.
8. Burridge, K., and Chrzanowska-Wodnicka, M. (1996). Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12, 463-518.
9. FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119, 893-903.
10. Burridge, K., Fath, K., Kelly, T., Nuckolls, G., and Turner, C. (1988). Focal adhesions: transmembrane junctions between extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4, 487-525.
11. Cary, L.A., Chang, J.F., and Guan, J-L. (1996). Stimulation of cell migration by overexpression of focal adhesion kinase and its association with src and fyn. J. Cell Sci. 109, 1787-1794.
12. Cheng, A.K., and Robertson, E.J. (1995). The murine LIM-kinase gene (limk) encodes a novel serine threonine kinase expressed predominantly in trophoblast giant cells and the developing nervous system. Mech. Dev. 52, 187-197.
13. Dedhar, S., and Hannigan, G.E. (1996). Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr. Opin. Cell Biol. 8, 657-669.
14. 5-dependent serine phosphorylation of paxillin in cultured human macrophages adherent to vitronectin. J. Biol. Chem. 271, 11016-11022.
15. Derman, M.P., Toker, A., Hartwig, J.H., Spokes, K., Falck, J.R., Chen, C.S., Cantley, L.C., and Cantley, L.G. (1997). The lipid products of phosphoinositide 3-kinase increase cell motility through protein kinase C. J. Biol. Chem. 272, 6465-6470.
16. Domann, R., and Martinez, J. (1995). Alternative to cloning cylinders for isolation of adherent cell clones. Biotechniques 18, 594-595.
17. Feuerstein, R., Wang, X., Song, D., Cooke, N.E., and Liebhaber, S.A. (1494). The LIM/double zinc-finger motif functions as a protein dimerization domain. Proc. Natl. Acad. Sci. USA 91, 10655-10659.
18. Gill, G.N. (1995). The enigma of LIM domains. Structure 3, 1285-1289.
19. Ginsberg, M.H., Du, X., and Plow, E.F. (1992). Inside-out integrin signalling. Curr. Opin. Cell Biol. 4, 766-771.
20. Ginsberg, M.H., Schwartz, M.A., and Schaller, M.D. (1995). Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11, 549-600.
21. 1-integrin-linked protein kinase. Nature 379, 91-96.
22. 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.
23. Jaken, S., Leach, K., and Klauck, T. (1989). Association of type 3 protein kinase C with focal contacts in rat embryo fibroblasts. J. Cell Biol. 109, 697-704.
24. Kuroda, S., Tokunaga, C., Kiyohara, Y., Higuchi, O., Konishi, H., Mizuno, K., Gill, G.N., and Kikkawa, U. (1996). Protein-protein interaction of zinc finger LIM domains with protein kinase C. J. Biol. Chem. 271, 31029-31032.
25. Lauffenburger, D.A., and Horwitz, A.F. (1996). Cell migration: a physically integrated molecular process. Cell, 84, 359-369.
26. Leung, T., Chen, X.-Q., Manser, E., and Lim, L. (1996). The p160 RhoA-binding kinase ROKα is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16, 5313-5327.
27. Li, J., Meyer, A.N., and Donoghue, D.J. (1997). Nuclear localization of cyclin B1 mediates its biological activity and is regulated by phosphorylation. Proc. Natl. Acad. Sci. USA 94, 502-507.
28. Lund, K., Petersen, J.S., Jensen, J., Blume, N., Edlund, T., Thor, S., and Madsen, O.D. (1995). Islet expression of rhombotin and Isl-1 suggests cell type specific exposure of LIM-domain epitopes. Endocrine 3, 399-408.
29. Melamed, I., Turner, C.E., Aktories, K., Kaplan, D.R., and Gelfand, E.W. (1995). Nerve growth factor triggers microfilament assembly and paxillin phosphorylation in human B lymphocytes. J. Exp. Med. 181, 1071-1079.
30. Okano, I., Hiraoka, J., Otera, H., Nunoue, K., Ohashi, K., Iwashita, S., Hirai, M., and Mizuno, K. (1995). Identification and characterization of a novel family of serine/threonine kinases containing two N-terminal LIM motifs. J. Biol. Chem. 270, 31321-31330.
31. O'Toole, T.E., Loftus, J.C., Du, X.P., Glass, A.A., Ruggeri, Z.M., Shattil, S.J., Plow, E.F., and Ginsberg, M.H. (1990). Affinity modulation of the alpha IIb beta 3 integrin (platelet GPIIb-IIIa) is an intrinsic property of the receptor. Cell. Regul. 1, 883-893.
32. O'Toole, T.E., Katagiri, Y., Faull, R.J., Peter, K., Tamura, R., Quaranta, V., Loftus, J.C., Shattil, S.J., and Ginsberg, M.H. (1994). Integrin cytoplasmic domains mediate inside-out signal transduction. J. Cell Biol. 124, 1047-1060.
33. Pearson, R.B., and Kemp, B.E. (1991). Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 200, 62-81.
34. Plopper, G.E., McNamee, H.P., Dike, L.E., Bojanowski, K., and Ingber, D.E. (1995). Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol. Biol. Cell 6, 1349-1365.
35. Pröschel, C., Blouin, M-J., Gutowski, N.J., Ludwig, R., and Noble, M. (1995). Limk1 is predominantly expressed in neural tissues and phosphorylates serine, threonine and tyrosine residues in vitro. Oncogene 11, 1271-1281.
36. Qwarnström, E.E., MacFarlane, S.A., Page, R.C., and Dower, S.K. (1991). Interleukin 1β induces rapid phosphorylation and redistribution of talin: a possible mechanism for modulation of fibroblast focal adhesion. Proc. Natl. Acad. Sci. USA 88, 1232-1236.
37. 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.
38. Rozengurt, E. (1995). Convergent signalling in the action of integrins, neuropeptides, growth factors and oncogenes. Cancer Surv. 24, 81-96.
39. Salgia, R. et al. (1995). Molecular cloning of human paxillin, a focal adhesion protein phosphorylated by p210 (bcr/abl). J. Biol. Chem. 270, 5039-5047.
40. Sánchez-García, I., and Rabbitts, T.H. (1994) The LIM domain: a new structural motif found in zinc-finger-like proteins. Trends Genet. 10, 315-320.
41. FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for crk. Mol. Cell. Biol. 15, 2635-2645.
42. Schmeichel, K.L., and Beckerle, M.C. (1994). The LIM domain is a modular protein-binding interface. Cell 79, 211-219.
43. Schmeichel, K.L., and Beckerle, M.C. (1997). Molecular dissection of a LIM domain. Mol. Biol. Cell 8, 219-230.
44. Schwartz, M.A. (1997). Integrins, oncogenes, and anchorage independence. J. Cell. Biol. 139, 575-578.
45. Songyang, Z., Blechner, S., Hoagland, N., Hoekstra, M.F., Piwnica, W.H., and Cantley, L.C. (1994). Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4, 973-982.
46. Songyang, Z., et al. (1996). A structural basis for substrate specificities of protein ser/thr kinases: primary sequence preferences of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and erk1. Mol. Cell. Biol, 16, 6486-6493.
47. Stuiver, I., and O'Toole, T.E. (1995). Regulation of integrin function and cellular adhesion. Stem Cells 13, 250-262.
48. Tanaka, T., Yamaguchi, R., Sabe, H., Sekiguchi, K., and Healy, J.M. (1996). Paxillin association in vitro with integrin cytoplasmic domain peptides. FEBS Lett. 399, 53-58.
49. Turner, C.E. (1991). Paxillin is a major phosphotyrosine-containing protein during embryonic development. J. Cell Biol. 115, 201-207.
50. FAK binding region. J. Cell Sci. 107, 1583-1591.
51. Turner, C.E., Pavalko, F.M., and Burridge, K. (1989). The role of phosphorylation and limited proteolytic cleavage of talin and vinculin in the disruption of focal adhesion integrity. J. Biol. Chem. 264, 11938-11944.
52. Turner, C.E., Glenney, J.R., and Burridge, K. (1990). Paxillin: a new vinculin-binding protein present in focal adhesions. J. Cell Biol. 111, 1059-1068.
53. Turner, C.E. (1994). Paxillin: a cytoskeletal target for tyrosine kinases. Bioessays 16, 47-52.
54. Turner, C.E., and Burridge, K. (1990). Transmembrane molecular assemblies in cell-extracellular matrix interactions. Curr. Opin. Cell Biol. 3, 849-853.
55. Turner, C.E., Pietras, K.M., Taylor, D.S., and Molloy, C.J. (1995). Angiotensin II stimulation of rapid paxillin tyrosine phosphorylation correlates with formation of focal adhesions in rat aortic smooth muscle cells. J. Cell Sci. 108, 333-342.
56. FAK during development: relation to paxillin. J. Cell Sci. 105, 637-645.
57. Vande Pol, S.B., Brown, M.C., and Turner, C.E. (1998). Association of bovine papillomavirus Type 1 E6 oncoprotein with the focal adhesion protein paxillin through a conserved protein interaction motif. Oncogene 16, 43-52.
58. van der Geer, P., and Hunter, T. (1994). Phosphopeptide mapping and phosphoamino acid analysis by electrophoresis and chromatography on thin-layer cellulose plates. Electrophoresis 15, 544-554.
59. Woods, A., and Couchman, J.R. (1992). Protein kinase C involvement in focal adhesion formation. J. Cell Sci. 101, 277-290.
60. Zachary, I., Sinnett-Smith, J., Turner, C.E., and Rozengurt, E. (1993). Bombesin, vasopressin, and endothelin rapidly stimulate tyrosine phosphorylation of the focal adhesion-associated protein paxillin in Swiss 3T3 cells. J. Biol. Chem. 268, 22060-22065.