Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant, negative mutant PTP1B

Journal of Cell Biology

Volumn 143, Issue 3, 1998, Pages 861-873

  Arregui, Carlos O ^a   Balsamo, Janne ^a   Lilien, Jack ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Cell signaling; Cell substrate adhesion; Integrins; Protein tyrosine phosphatase; Tyrosine phosphorylation

Indexed keywords

INTEGRIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL SPREADING; DNA TRANSFECTION; FIBROBLAST; FLOW CYTOMETRY; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CATALYSIS; CELL ADHESION; CELL ADHESION MOLECULES; CYTOSKELETAL PROTEINS; ENZYME ACTIVATION; FIBROBLASTS; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; INTEGRINS; L CELLS (CELL LINE); LYSOPHOSPHOLIPIDS; MICE; MUTAGENESIS; PAXILLIN; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; TYROSINE;

ANIMALIA;

EID: 0032476646     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.143.3.861     Document Type: Article

References (84)

1. Aberle, H., H. Schwartz, and R. Kemler. 1996. Cadherin-catenin complex: protein interactions and their implications for cadherin function. J. Cell. Biochem. 61:514-523.
2. Balsamo, J., T.-C. Leung, H. Ernst, M.K.B. Zanin, S. Hoffman, and J. Lilien. 1996. Regulated binding of a PTP1B-like phosphatase to N-cadherin: control of cadherin-mediated adhesion by dephosphorylation of β-catenin. J. Cell Biol. 134:801-813.
3. Balsamo, J., C. Arregui, T.C. Leung, and J. Lilien. 1998. The nonreceptor protein tyrosine phosphatase PTP1B binds to the cytoplasmic domain of N-cadherin and regulates the cadherin-actin linkage. J. Cell Biol. 143:523-532.
4. Bandyopadhyay, D., A. Kusari, K.A. Kenner, F. Liu, J. Chernoff, T.A. Gustafson, and J. Kusari. 1997. Protein-tyrosine phosphatase 1B complexes with the insulin receptor in vivo and is tyrosine-phosphorylated in the presence of insulin. J. Biol. Chem. 272:1639-1645.
5. Barry, S.T., and D.R. Critchley. 1994. The rho-dependent assembly of focal adhesions in Swiss 3T3 cells is associated with increased tyrosine phosphorylation and the recruitment of both pp125FAK and protein kinase C-γ to focal adhesions. J. Cell Sci. 107:2033-2045.
6. Behrens, J., L. Vakaet, R. Friis, E. Winterhager, F. Van Roy, M.M. Mareel, and W. Birchmeier. 1993. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/β-catenin complex in cells transformed with a temperature-sensitive v-src gene. J. Cell Biol. 120:757-766.
7. Bergman, M., V. Joukov, I. Virtanen, and K. Alitalo. 1995. Overexpressed Csk tyrosine kinase is localized in focal adhesions, causes reorganization of αvβ5 integrin, and interferes with HeLa cell spreading. Mol. Cell. Biol. 15:711-722.
8. Black, D.S., and J.B. Bliska. 1997. Identification of p130Cas 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.
9. Bonnekoh, B., A. Wevers, F. Jugert, H. Merk, and G. Mahrle. 1989. Colorimetric growth assay for epidermal cell cultures by their crystal violet binding capacity. Arch. Dermatol. Res. 281:487-490.
10. Brown, M.T., and J.A. Cooper. 1996. Regulation, substrates and functions of Src. Biochim. Biophys. Acta. 1287:121-149.
11. Burridge, K., K. Fath, T. Kelly, G. Nuckolls, and C. Turner. 1988. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4:487-525.
12. Burridge, K., C.E. Turner, and L.H. Romer. 1992. Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119:893-903.
13. Burridge, K., and M. Chrzanowska-Wodnicka. 1996. Focal adhesions, contractility and signaling. Annu. Rev. Cell Biol. 12:463-519.
14. 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.
15. Clark, E.A., and J.S. Brugge. 1993. Redistribution of activated pp60c-src to integrin-dependent cytoskeletal complexes in thrombin-stimulated platelets. Mol. Cell. Biol. 13:1863-1871.
16. Clark, E.A., and J.S. Brugge. 1995. Integrins and signal transduction pathways: the road taken. Science. 268:233-239.
17. Cooper, J.A., and C.S. King. 1986. Dephosphorylation or antibody binding to the carboxy terminus stimulates pp60c-src. Mol. Cell. Biol. 6:4467-4477.
18. Courtneidge, S.A. 1985. Activation of the pp60c-src kinase by middle T antigen binding or by dephosphorylation. EMBO (Eur. Mol. Biol. Organ.) J. 4:1471-1477.
19. Daniel, J.M., and A.B. Reynolds. 1997. Tyrosine phosphorylation and cadherin/ catenin function. Bioessays. 19:883-891.
20. Eide, B.L., C.W. Turck, and J.A. Escobedo. 1995. Identification of Tyr-397 as the primary site of tyrosine phosphorylation and pp60src association in the focal adhesion kinase, pp125. Mol. Cell. Biol. 15:2819-2827.
21. Ezumi, Y., H. Takayama, and M. Okuma. 1995. Differential regulation of protein-tyrosine phosphatases by integrin αIIbβ3 through cytoskeletal reorganization and tyrosine phosphorylation in human platelets. J. Biol. Chem. 270: 11927-11934.
22. Fang, K.S., H. Sabe, H. Saito, and H. Hanafusa. 1994. Comparative study of three protein-tyrosine phosphatases. J. Biol. Chem. 269:20194-20200.
23. Flint, A.J., T. Tiganis, D. Bradford, and N. Tonks. 1997. Development of "substrate-trapping" mutants to identify physiological substrates of protein tyrosine phosphalases. Proc. Natl. Acad. Sci. USA. 94:1680-1685.
24. Frangioni, J.V., P.M. Beahm, V. Shifrin, C.A. Jost, and B.G. Neel. 1992. The nontransmembrane tyrosine phosphatase PTP-IB localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell. 68:545-560.
25. Frangioni, J.V., A. Oda, M. Smith, E. Salzman, and B.G. Neel. 1993. Calpaincatalyzed cleavage and subcellular relocation of protein phosphotyrosine phosphatase 1B (PTP-1B) in human platelets. EMBO (Eur. Mol. Biol. Organ.) J. 12:4843-4856.
26. Fujii, K., F. Furukawa, and N. Matsuyoshi. 1996. Ligand activation of overexpressed epidermal growth factor receptor results in colony dissociation and disturbed E-cadherin function in HSC-1 human cutaneous squamous carcinoma cells. Exp. Cell Res. 223:50-62.
27. Giancotti, F.G., and E. Ruoslahti. 1990. Elevated levels of the α5β1 fibronectin receptor suppress the transformed phenotype of Chinese hamster ovary cells. Cell. 60:849-859.
28. Garton, A.J., M.R. Burnham, A.H. Bouton, and N.K. Tonks. 1997. Association of PTP-PEST with the SH3 domain of p130Cas; a novel mechanism of protein tyrosine phosphatase substrate recognition. Oncogene. 18:877-885.
29. Guan, J.-L., and D. Shalloway. 1992. Regulation of focal adhesion-associated protein kinase by both cellular adhesion and oncogenic transformation. Nature. 358:690-692.
30. Gumbiner, B.M. 1993. Proteins associated with the cytoplasmic surface of adhesion molecules. Neuron. 11:551-564.
31. Hamaguchi, M., N. Matsuyoshi, Y. Ohnishi, B. Gotoh, M. Takeichi, and Y. Nagai. 1993. p60v-src causes tyrosine phosphorylation and inactivation of the N-cadherin-catenin cell adhesion system. EMBO (Eur. Mol. Biol. Organ.) J. 12:307-314.
32. Hanks, S.K., and T.R. Polte. 1997. Signaling through focal adhesion kinase. Bioessays. 19:137-144.
33. Hazan, R.B., and L. Norton. 1998. The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton. J. Biol. Chem. 273:9078-9084.
34. Hotchin, N.A., and A. Hall. 1995. The assembly of integrin complexes requires both extracellular matrix and intracellular rho/rac GTPases. J. Cell Biol. 131: 1857-1865.
35. Howel, B.W., and J.A. Cooper. 1994. Csk suppression of Src involves movement of Csk to sites of Src activity. Mol. Cell. Biol. 14:5402-5411.
36. Ilic, 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 adhesion contact formation in cells from FAK-deficient mice. Nature. 377:539-544.
37. Imamoto, A., and P. Soriano. 1993. Disruption of the cdk gene, encoding a negative regulator of src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell. 73:1117-1124.
38. Jockusch, B.M., P. Bubeck, K. Gichl, M. Kroemker, J. Moschner, M. Rothkegel, M. Rüdiger, K. Schlüter. G. Stanke, and J. Winkler. 1995. The molecular architecture of focal adhesions. Annu. Rev. Cell Dev. Biol. 11:379-116.
39. c-src in vitro. Biochem. Biophys. Res. Commun. 246:238-242.
40. Kaplan, K.B., K.B. Bibbins, J.R. Swedlow, M. Arnaud, D.O. Morgan, and H.E. Varmus. 1994. Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylalion of tyrosine 527. EMBO (Eur. Mol. Biol. Organ.) J. 13:4745-4756.
41. Kaplan, K.B., J.R. Swedlow, D.O. Morgan, and H.E. Varmus. 1995. c-Src enhances the spreading of src-/-fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev. 9:1505-1517.
42. Kemler, R. 1993. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 9:317-321.
43. Kenner, K.A., E. Anyanwu, J.M. Olefsky, and J. Kusari. 1996. Protein-tyrosine phosphatase 1B is a negative regulator of insulin- and insulin-like growth factor-1-stimulated signaling. J. Biol. Chem. 271:19810-19816.
44. Kornberg, L., H.S. Earp, J.T. Parsons, M. Schaller, and R.L. Juliano. 1992. Cell adhesion of integrin clustering increases phosphorylation of a focal adhesion associated tyrosine kinase. J. Biol. Chem. 267:23439-23442.
45. Krueger, J.G., E.A. Garber, and A.R. Goldberg. 1983. Subcellular localization of pp60src in RSV-transformed cells. Curr. Top. Microbiol. Immunol. 107: 52-124.
46. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
47. Lilien, J., S. Hoffman, C. Eisenberg, and J. Balsamo. 1997. β-Catenin is a target for extracellular signals controlling cadherin function: the neurocan-Gal-NAcPTase connection. Curr. Top. Dev. Biol. 35:161-189.
48. Lipfert, L., B. Haimovich, M.D. Schaller, B.S. Cobb, J.T. Parsons, and J.S. Brugge. 1992. Integrin-dependent phosphorylation and activation of the protein tyrosine kinase pp125FAK in platelets. J. Cell Biol. 119:905-912.
49. Liu, F., and J. Chernoff. 1997. Protein tyrosine phosphatase 1B interacts with and is tyrosine phosphorylated by the epidermal growth factor receptor. Biochem. J. 327:139-145.
50. 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.
51. Liu, F., M.A. Sells, and J. Chernoff. 1998. Protein tyrosine phosphatase 1B negatively regulates integrin signaling. Curr. Biol. 8:173-176.
52. Luna, E.J., and A.L. Hitt. 1992. Cytoskeleton-plasma membrane interactions. Science (Wash. DC). 258:955-964.
53. Machesky, L.M., and A. Hall. 1996. Rho: a connection between membrane receptor signalling and the cytoskeleton. Trends Cell Biol. 6:304-310.
54. Milarski, K.L., G. Zhu, C.G. Pearl, D.J. McNamara, E.M. Dobrusin, D. Mac-Lean, A. Thieme-Sefler, Z.-Y. Zhang, T. Sawyer, S.J. Decker, et al. 1993. Sequence specificity in recognition of the epidermal growth factor receptor by protein tyrosine phosphatase 1B. J. Biol. Chem. 268:23634-23639.
55. Nada, S., M. Okada, A. MacAuley, J.A. Cooper, and H. Nakagawa. 1991. Cloning of a complementary DNA for a protein tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature. 351:69-72.
56. Nada, S., T. Yagi, H. Takeda, T. Tokunaga, H. Nakagawa, Y. Ikawa, M. Okada, and S. Aizawa. 1993. Constitutive activation of Src family kinases in mouse embryos that lack CSK. Cell. 73:1125-1136.
57. Nermut, M.V., P. Eason, E.M.A. Hirst. and S. Kellie. 1991. Cell/substratum adhesions in RSV-transformed rat fibroblasts. Exp. Cell Res. 193:382-397.
58. Nigg, E.A., B.M. Sefton, T. Hunter, G. Walter, and S.J. Singer. 1982. Immunofluorescent localization of the transforming protein of Rous sarcoma virus with antibodies against a synthetic Src peptide. Proc. Natl. Acad. Sci. USA. 79:5322-5326.
59. Nobes, C.D., and A. Hall. 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.
60. Okada, M., S. Nada, Y. Yamanishi, T. Yamamoto, and H. Nakagawa. 1991. CSK: a protein-tyrosine kinase involved in regulation of src family kinases. J. Biol. Chem. 266:24249-24252.
61. Ozawa, M., and R. Kemler. 1998. Altered cell adhesion activity by pervanadate due to the dissociation of α-catenin from the E-cadherin/catenin complex. J. Biol. Chem. 273:6166-6170.
62. Parsons, J.T. 1996. Integrin-mediated signalling: regulation by protein tyrosine kinases and small GTP-binding proteins. Curr. Opin. Cell Biol. 8:146-152.
63. Parsons, J.T., and S.J. Parsons. 1997. Src family protein tyrosine kinases: cooperating with growth factor and adhesion signaling pathways. Curr. Opin. Cell Biol. 9:187-192.
64. Ridley, A.J., and A. Hall. 1992. The small GTP-binding prolein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70:389-399.
65. Rock, M.T., W.H. Brooks, and T.L. Rozman. 1997. Calcium-dependent signaling pathways in T cells. J. Biol. Chem. 272:33377-33383.
66. Rohrschneider, L.R. 1980. Adhesion plaques of Rous sarcoma virus-transformed cells contain the src gene product. Proc. Natl. Acad. Sci. USA. 77: 3514-3518.
67. Schaller, M.D., and J.T. Parsons. 1995. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell Biol. 15:2635-2645.
68. Schaller, M.D., J.D. Hildebrand, J.D. Shannon, J.W. Fox, R.R. Vines, and T. Parsons. 1994. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH-dependent binding of pp60src. Mol Cell Biol. 14: 1680-1685.
69. Schwartz, M.A., M.D. Schaller, and M.H. Ginsberg. 1995. Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11:549-599.
70. Seely, B.L., P.A. Staubs, D.R. Reichart, P. Berhanu, K.L. Milarski, A.R. Saltiel, J. Kusari, and J.M. Olefsky. 1996. Protein tyrosine phosphatase 1B interacts with the activated insulin receptor. Diabetes. 45:1379-1385.
71. Seufferlein, T., and E. Rozengurt. 1994. Lysophosphatidic acid stimulates tyrosine phosphorylation of focal adhesion kinase, paxillin and p130. J. Biol. Chem. 269:9345-9351.
72. Shen, Y., G. Schneider, J.-F. Cloutier, A. Veillete, and M.D. Schaller. 1998. Direct association of protein-tyrosine phosphatase PTP-PEST with paxillin. J. Biol. Chem. 273:6474-6481.
73. Soltesz, S.A., E.A. Powers, J.G. Geng, and C. Fisher. 1997. Adhesion of HT-29 colon carcinoma cells to E-selectin results in increased tyrosine phosphorylation and decreased activity of c-src. Int. J. Cancer. 71:645-653.
74. Somani, A.-K., J.S. Bignon, G.B. Mills, K.A. Siminovitch, and D.R. Branch. 1997. Src kinase activity is regulated by the SHP-1 protein-tyrosine phosphatase. J. Biol. Chem. 272:21113-21119.
75. 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.
76. Takeya, T., and H. Hanafusa. 1983. Structure and sequence of the cellular gene homologous to the RSV src gene and the mechanism for generating the transforming virus. Cell. 32:881-890.
77. Tamura, M., J. Gu, K. Matsumoto, S.A. Aota, R. Parsons, and K.M. Yamada. 1998. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science. 280:1614-1617.
78. Terasaki, M., and T.S. Reese. 1992. Characterization of endoplasmic reticulum by co-localization of BiP and dicarbocyanine dyes. J. Cell Sci. 101:315-322.
79. Thomas, S.M., P. Soriano, and A. Imamoto. 1995. Specific and redundant roles of Src and Fyn in organizing the cytoskeleton. Nature. 376:267-271.
80. Woodford-Thomas, T.A., J.D. Rhodes, and J.E. Dixon. 1992. Expression of a protein tyrosine phosphatase in normal and v-src-transformed mouse 3T3 fibroblasts. J. Cell Biol. 117:401-414.
81. Xing, Z., H.C. Chen, J.K. Nowlen, S.L. 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.
82. Yamada, K.M. 1997. Integrin signaling. Matrix Biol. 16:137-141.
83. Yamada, K.M., and B. Geiger. 1997. Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol. 9:76-85.
84. Zachary, I., J. Sinnet-Smith, C.E. Turner, and E. Rozengurt. 1993. Bombesin, vasopresin and endothelin rapidly stimulate tyrosine phosphorylation of the focal adhesion associated protein paxillin in Swiss 3T3 cells. J. Biol. Chem. 268:22060-22065.