Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts

Journal of Cell Biology

Volumn 144, Issue 5, 1999, Pages 1019-1031

  Angers Loustau, Alexandre ^a   Côté, Jean François ^a   Charest, Alain ^b   Dowbenko, Donald ^c   Spencer, Susan ^c   Lasky, Laurence A ^c   Tremblay, Michel L ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c GENENTECH INC   (United States)

Author keywords

Cytokinesis; Focal adhesion; Migration; PSTPIP; PTP PEST

Indexed keywords

FIBRONECTIN; FOCAL ADHESION KINASE; PAXILLIN; PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CYTOKINESIS; CYTOSKELETON; FIBROBLAST; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION;

ANIMALS; CELL ADHESION MOLECULES; CELL CYCLE; CELL MEMBRANE; CELL MOVEMENT; COS CELLS; CYTOPLASM; CYTOSKELETAL PROTEINS; FIBROBLASTS; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; PAXILLIN; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; SRC HOMOLOGY DOMAINS;

EID: 0345593816     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.144.5.1019     Document Type: Article

References (59)

1. Akasaka, T., R.L. van Leeuwen, I.G. Yoskinaga, M.C. Mihm, Jr., and H.R. Byers. 1995. Focal adhesion kinase (p125FAK) expression correlates with motility of human melanoma cell lines. J. Investig. Dermatol. 105:104-108.
2. Arregui, C.O., J. Balsamo, and J. Lilien. 1998. Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant-negative mutant PTP1B. J. Cell Biol. 143:861-873.
3. CAS as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO (Eur. Mol. Biol. Organ.) J. 16:2730-2744.
4. Burridge, K., and M. Chrzanowska-Wodnicka. 1996. Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12:463-518.
5. 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.
6. Calalb, M.B., X. Zhang, T.R. Polte, and S.K. Hanks. 1996. Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 228:662-668.
7. Cantley, L.C., and Z. Songyang. 1994. Specificity in recognition of phosphopeptides by src-homology 2 domains. J. Cell Sci. Suppl. 18:121-126.
8. Cary, L.A., J.F. Chang, and J.L. Guan. 1996. Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. J. Cell Sci. 109:1787-1794.
9. CAS as a mediator of focal adhesion kinase-promoted cell migration. J. Cell Biol. 140:211-221.
10. Charest, A., J. Wagner, S.U. Shen, and M.L. Tremblay. 1995. Murine protein tyrosine phosphatase-PEST, a stable cytosolic protein tyrosine phosphatase. Biochem. J. 308:425-432.
11. Charest, A., J. Wagner, S. Jacob, C.J. McGlade, and M.L. Tremblay. 1996. Phosphotyrosine-independent binding of SHC to the NPLH sequence of murine protein-tyrosine phosphatase-PEST. Evidence for extended phosphotyrosine binding/phosphotyrosine interaction domain recognition specificity. J. Biol. Chem. 271:8424-8429.
12. Charest, A., J. Wagner, M. Kwan, and M.L. Tremblay. 1997. Coupling of the murine protein tyrosine phosphatase PEST to the epidermal growth factor (EGF) receptor through a Src homology 3 (SH3) domain-mediated association with Grb2. Oncogene. 14:1643-1651.
13. Chrzanowska-Wodnicka, M., and K. Burridge. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133: 1403-1415.
14. Cool, D.E., P.R. Andreassen, N.K. Tonks, E.G. Krebs, E.H. Fischer, and R.L. Margolis. 1992. Cytokinetic failure and asynchronous nuclear division in BHK cells overexpressing a truncated protein-tyrosine-phosphatase. Proc. Natl. Acad. Sci. USA. 89:5422-5426.
15. Côté, J.-F., A. Charest, J. Wagner, and M.L. Tremblay. 1998. Combination of gene targeting and substrate trapping to identify substrates of protein tyrosine phosphatases using PTP-PEST as a model. Biochemistry. 37:13128-13137.
16. Dowbenko, D., S. Spencer, C. Quan, and L.A. Lasky. 1998. Identification of a novel polyproline recognition site in the cytoskeletal associated protein, proline serine threonine phosphatase interacting protein. J. Biol. Chem. 273: 989-996.
17. Fankhauser, C., A. Reymond, L. Cerutti, S. Utzig, K. Hofmann, and V. Simanis. 1995. The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis. Cell. 82:435-444.
18. Fincham, V.J., and M.C. Frame. 1998. The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility. EMBO (Eur. Mol. Biol. Organ.) J. 17:81-92.
19. Fukui, Y., A. De Lozanne, and J.A. Spudich. 1990. Structure and function of the cytoskeleton of a Dictyostelium myosin-defective mutant. J. Cell Biol. 110:367-378.
20. Garton, A.J., A.J. Flint, and N.K. Tonks. 1996. Identification of p130(cas) as a substrate for the cytosolic protein tyrosine phosphatase PTP-PEST. Mol. Cell. Biol. 16:6408-6418.
21. Garton, A.J., M.R. Burnham, A.H. Bouton, and N.K. Tonks. 1997. Association of PTP-PEST with the SH3 domain of p130(Cas) a novel mechanism of protein tyrosine phosphalase substrate recognition. Oncogene. 15:877-885.
22. Gilmore, A.P., and K. Burridge. 1996. Molecular mechanisms for focal adhesion assembly through regulation of protein-protein interactions. Structure. 4:647-651.
23. Hanks, S.K., and T.R. Polte. 1997. Signaling through focal adhesion kinase. Bioessays. 19:137-145.
24. Harder, K.W., N.P.H. Moller, J.W. Peacock, and F.R. Jirik. 1998. Protein-tyrosine phosphatase alpha regulates Src family kinases and alters cell-substratum adhesion. J. Biol. Chem. 273:31890-31900.
25. CAS, a substrate associated with v-Src and v-Crk. localizes to focal adhesions and binds to focal adhesion kinase. J. Biol. Chem. 271:13649-13655.
26. Ilìc, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, T. Yamamoto, et al. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature. 377:539-544.
27. 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.
28. Lauffenburger, D.A., and A.F. Horwitz. 1996. Cell migration: a physically integrated molecular process. Cell. 84:359-369.
29. Li, R. 1997. Beel, a yeast protein with homology to Wiscott-Aldrich syndrome protein, is critical for the assembly of cortical actin cytoskeleton. J. Cell Biol. 136:649-658.
30. Liu, F., D.E. Hill, and J. Chernoff. 1996. Direct binding of the proline-rich region of protein tyrosine phosphatase 1B to the Src homology 3 domain of p130(Cas). J. Biol. Chem. 271:31290-31295.
31. Liu, F., M.A. Sells, and J. Chernoff. 1998. Protein tyrosine phosphatase 1B negatively regulates integrin signaling. Curr. Biol. 8:173-176.
32. Liu, T., J.G. Williams, and M. Clarke. 1992. Inducible expression of calmodulin antisense RNA in Dictyostelium cells inhibits the completion of cytokinesis. Mol. Biol. Cell. 3:1403-1413.
33. Nakamoto, T., R. Sakai, H. Honda, S. Ogawa, H. Ueno, T. Suzuki, S. Aizawa, Y. Yazaki, and H. Hirai. 1997. Requirements for localization of p130(cas) to focal adhesions. Mol. Cell. Biol. 17:3884-3897.
34. Nobes, C.D., and A. Hall. 1995. Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23:456-459.
35. CAS and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO (Eur. Mol. Biol. Organ.) J. 16:2307-2318.
36. CAS. Proc. Natl. Acad. Sci. USA. 92:10678-10682.
37. Retta, S.F., S.T. Barry, D.R. Critchley, P. Defilippi, L. Silengo, and G. Tarone. 1996. Focal adhesion and stress fiber formation is regulated by tyrosine phosphatase activity. Exp. Cell Res. 229:307-317.
38. 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 analytically inactive FAK: a role for paxillin tyrosine phosphorylation. Mol. Cell. Biol. 17:6906-6914.
39. Sakai, R., A. Iwamatsu, 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 (Eur. Mol. Biol. Organ.) J. 13:3748-3756.
40. Sasaki, H., K. Nagura, M. Ishino, H. Tobioka, K. Kotani, and T. Sasaki. 1995. Cloning and characterization of cell adhesion kinase beta, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily. J. Biol. Chem. 270: 21206-21219.
41. Schaller, M.D., J.D. Hildebrand, J.D. Shannon, J.W. Fox, R.R. Vines, and J.T. Parsons. 1994. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 14: 1680-1688.
42. Schlaepfer, D.D., and T. Hunter. 1996. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 16:5623-5633.
43. Schlaepfer, D.D., S.K. Hanks, T. Hunter, and P. van der Geer. 1994. Integrinmediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature. 372:786-791.
44. CAS, and Nck adaptor proteins. Mol. Cell. Biol. 17:1702-1713.
45. Schwarzbauer, J.E. 1997. Cell migration: may the force be with you. Curr. Biol. 7:R292-R294.
46. Serra-Pages, C., N. Kadersha, L. Fazikas, Q. Medly, A. Debant, and M. Struli. 1995. The LAR transmembrane protein tyrosine phosphatase and a coiled-coil LAR interacting protein co-localize at focal adhesions. EMBO (Eur. Mol. Biol. Organ.) J. 14:2827-2838.
47. Shen, Y., G. Schneider, J.F. Cloutier, A. Veillette, and M.D. Schaller. 1998. Direct association of protein-tyrosine phosphatase PTP-PEST with paxillin. J. Biol. Chem. 273:6474-6481.
48. Spencer, S., D. Dowbenko, J. Cheng, W.L. Li, J. Brush, S. Utzig, V. Simanis, and L.A. Lasky. 1997. PSTPIP a tyrosine phosphorylated cleavage furrow-associated protein that is a substrate for a PEST tyrosine phosphatase. J. Cell Biol. 138:845-860.
49. Symons, M., J.M. Derry, B. Karlak, S. Jiang, V. Lemabieu, F. McCormick, U. Francke, and A. Abo. 1996. Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell. 84:723-734.
50. Tapon, N., and A. Hall. 1997. Rho, Rac and Cdc42 GTPases regulate the organization of the actin cyloskeleton. Curr. Opin. Cell Biol. 1:86-92.
51. Turner, C.E., and J.T. Miller. 1994. Primary sequence of paxillin contains putative SH2 and SH3 domain binding motifs and multiple LIM domains: identification of a vinculin and pp125Fak-binding region. J. Cell Sci. 107:1583-1591.
52. Vithalani, K.K., J.D. Shoffner, and A. De Lozanne. 1996. Isolation and characterization of a novel cytokinesis-deficient mutant in Dictyostelium discoideum. J. Cell. Biochem. 62:290-301.
53. CAS and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem. 270:22259-22262.
54. Wilson, L., M.J. Carrier, and S. Kellie. 1995. pp125FAK tyrosine kinase activity is not required for the assembly of F-actin stress fibres and focal adhesions in cultured mouse aortic smooth muscle cells. J. Cell Sci. 108:2381-2391.
55. Wu, H., and J.T. Parsons. 1993. Cortactin, an 80/85-kilodalton pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J. Cell Biol. 120:1417-1426.
56. Wu, H., A.B. Reynolds, S.B. Kanner, R.R. Vines, and J.T. Parsons. 1991. Identification and characterization of a novel cytoskeleton-associated pp60src substrate. Mol. Cell. Biol. 11:5113-5124.
57. Wu, Y., D. Dowbenko, and L.K. Lasky. 1998a. PSTPIP 2, a second tyrosine phosphorylated, cytoskelelal-associaled protein that binds a PEST-type protein-tyrosine phosphatase. J. Biol. Chem. 273:30487-30496.
58. Wu, Y., S.D. Spencer, and L.A. Lasky. 1998b. Tyrosine phosphorylation regulates the SH3-mediated binding of the Wiskott-Aldrich syndrome protein to PSTPIP, a cytoskeletal-associated protein. J. Biol. Chem. 273:5765-5770.
59. Yu, D.H., C.K. Qu, O. Henegariu, X. Lu, and G.S. Feng. 1998. Protein-tyrosine phosphatase SHP-2 regulates cell spreading, migration and local adhesion. J. Biol. Chem. 273:21125-21131.