Differences in phosphatase modulation of α4β1 and α5β1 integrin- mediated adhesion and migration of B16F1 cells

Biochemistry and Cell Biology

Volumn 77, Issue 5, 1999, Pages 409-420

  Hangan Steinman, Dolores ^a   Ho, Wai chi ^a   Shenoy, Priti ^a   Chan, Bosco M C ^a   Morris, Vincent L ^b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Cell adhesion; Cell movement; Integrins; Phosphatases

Indexed keywords

ARSENOSOBENZENE; ENZYME INHIBITOR; FIBRONECTIN; INTEGRIN; OKADAIC ACID; PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE; VANADATE SODIUM;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; ENZYME INHIBITION; MODULATION; NONHUMAN; REGULATORY MECHANISM;

ANIMALIA;

EID: 0033406264     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o99-050     Document Type: Article

References (73)

1. Anand-Apte, B., Zetter, B.R., Viswanathan, A., Qiu, R.-G., Chen, J., Ruggieri, R., and Symons, M. 1997. Platelet-derived growth factor and fibronectin-stimulated migration are differentially regulated by the Rac and extracellular signal-regulated kinase pathways. J. Biol. Chem. 272: 30 688-30 692.
2. Arregui, C.O., Balsamo, J., and Lilien, J. 1998. Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant-negative mutant PTP1B. J. Cell Biol. 143: 861-873.
3. Arroyo, A.G., Sanchez-Mateos, P., Campanero, M.R., Martin-Padura, I., Dejana, E., and Sanchez-Madrid, F. 1992. Regulation of the VLA integrin-ligand interactions through the β1 subunit. J. Cell Biol. 117: 659-670.
4. Bazzoni, G., and Hemler, M.E. 1998. Are changes in integrin affinity and conformation overemphasized? Trends Biochem. Sci. 23: 30-34.
5. Bennett, A.M., and Tonks, N.K. 1997. Regulation of distinct stages of skeletal muscle differentiation by mitogen-activated protein kinases. Science (Washington, D.C.), 278: 1288-1291.
6. Bialojan, C., and Takai, A. 1988. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Biochem. J. 256: 283-290.
7. + T cell lines. Cytokine, 9: 333-339.
8. Chan, B.M.C., and Hemler, M.E. 1993. Multiple functional forms of the integrin VLA-2 can be derived from a single alpha 2 cDNA clone: interconversion of forms induced by an anti-beta 1 antibody. J. Cell Biol. 120: 537-543.
9. Chang, H.Y., Takel, K., Sydor, A.M., Born, T., Rusnak, F., and Jay, D.G. 1995. Asymmetric retraction of growth cone filopodia following focal inactivation of calcineurin. Nature (London), 376: 686-690.
10. Chiou, J.-Y., and Westhead, E.W. 1992. Okadaic acid, a protein phosphatase inhibitor, inhibits nerve growth factor-directed neurite outgrowth in PC12 cells. J. Neurochem. 59: 1963-1966.
11. Clark, E.A., and Brugge, J.S. 1995. Integrins and signal transduction pathways: The road taken. Science (Washington, D.C.), 268: 233-239.
12. Defilippi, P., Retta, S.F., Olivo, C., Palmieri, M., Venturino, M., Silengo, L., and Tarone, G. 1995. p125FAK tyrosine phosphorylation and focal adhesion assembly: studies with phosphotyrosine phosphatase inhibitors. Exp. Cell Res. 221: 141-152.
13. DiMilla, P.A., Stone, J.A., Quinn, J.A., Albelda, S.M., and Lauffenburger, D.A. 1993. Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J. Cell Biol. 122: 729-737.
14. Eliceiri, B.P., Klemke, R., Stromblad, S., and Cheresh, D.A. 1998. Integrin αvβ3 requirement for sustained mitogen-activated protein kinase activity during angiogenesis. J. Cell Biol. 140: 1255-1263.
15. Elices, M.J., Urry, L.A., and Hemler, M.E. 1991. Receptor functions for the integrin VLA-3: fibronectin, collagen and laminin binding are differentially influenced by Arg-Gly-Asp peptide and by divalent cations. J. Cell Biol. 112: 169-181.
16. Entschladen, F., Niggemann, B., Zanker, K.S., and Friedl, P. 1997. Differential requirement of protein tyrosine kinases and protein kinase C in the regulation of T cell locomotion in three-dimentional collagen matrices. J. Immunol. 159: 3203-3210.
17. Fehlner-Gardiner, C.C., Uniyal, S., von Ballestrem, C.G., and Chan, B.M.C. 1996. Differential utilization of VLA-4 (α4β1) and -5 (α5β1) integrins during the development of mouse bone marrow-derived mast cells. Differentiation, 60: 317-325.
18. Gordon, J.A. 1991. Use of vanadate as protein-phosphotyrosine phosphatase inhibitor. Methods Enzymol. 201: 477-482.
19. Graf, K., Xi, X.-P., Yang, D., Fleck, E., Hsueh, W.A., and Law, R.E. 1997. Mitogen-activated protein kinase activation is involved in platelet-derived growth factor-directed migration by vascular smooth muscle cells. Hypertension, 29: 334-339.
20. Gronthos, S., Stewart, K., Graves, S.E., Hay, S., and Simmons, P.J. 1997. Integrin expression and function on human osteoblast-like cells. J. Bone Miner. Res. 12: 1189-1197.
21. 2+. J. Cell Biol. 117: 1109-1117.
22. Gu, J., Tamura, M., and Yamada, K.M. 1998. Tumor suppressor PTEN inhibits integrin-and growth factor-mediated mitogen-activated protein (MAP) kinase signaling pathways. J. Cell Biol. 143: 1375-1383.
23. Guan, K.L., and Butch, E. 1995. Isolation and characterization of a novel dual specific phosphatase, HVH2, which selectively dephosphorylates the mitogen-activated protein kinase. J. Biol. Chem. 270: 7197-7203.
24. Guan, J.-L., and Hynes, R.O. 1990. Lymphoid cells recognize an alternatively spliced segment of fibronectin via the integrin α4β1. Cell, 60: 53-61.
25. Hangan, D., Uniyal, S., Morris, V.L., MacDonald, I.C., von Ballestrem, C., Chau, T., Schmidt, E.E., Chambers, A.F., Groom, A.C., and Chan, B.M.C. 1996. Integrin VLA-2 (α2β1) function in postextravasation movement of human rhabdomyosarcoma RD cells in the liver. Cancer Res. 56: 3142-3149.
26. Hangan, D., Morris, V.L., Boeters, L., von Ballestrem, C., Uniyal, S., and Chan, B.M.C. 1997. An epitope on VLA-6 (α6β1) integrin involved in migration but not adhesion is required for extravasation of murine melanoma B16F1 cells in liver. Cancer Res. 57: 3812-3817.
27. Hauzenberger, D., Klominek, J., and Sundqvist, K.-G. 1994. Functional specialization of fibronectin-binding beta-1 integrins in T lymphocyte migration. J. Immunol. 153: 960-971.
28. Hedman, H., and Lundgren, E. 1996. Regulation of alpha 4 integrin avidity in human B cells: requirement for dephophorylation events for high avidity VCAM-1 binding. Scand. J. Immunol. 44: 239-242.
29. Ho, W.-C., Heinemann, C., Hangan, D., Uniyal, S., Morris, V.L., and Chan, B.M.C. 1997. Modulation of in vivo migratory function of α2β1 integrin in mouse liver. Mol. Biol. Cell 8: 1863-1875.
30. Honkanen, R.E., Zwiller, J., Daily, S.L., Khatra, B.S., Dukelow, M., and Boynton, A.L. 1991. Identification, purification, and characterization of a novel serine/threonine protein phosphatase from bovine brain. J. Biol. Chem. 266: 6614-6619.
31. Hughes, P.E., Renshaw, M.W., Pfaff, M., Forsyth, J., Keivens, V.M., Schwartz, M.A., and Ginsberg, M.H. 1997. Suppression of integrin activation: a novel function of a Ras/Raf-initiated MAP kinase pathway. Cell, 88: 521-530.
32. Huttenlocher, A., Ginsberg, M.H., and Horwitz, A.F. 1996. Modulation of cell migration by integrin-mediated cytoskeletal linkages and ligand-binding affinity. J. Cell Biol. 134: 1551-1562.
33. Hynes, R.O. 1992. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell, 69: 11-25.
34. Ilic, D., Damsky, C.H., and Yamamoto, T. 1997. Focal adhesion kinase: at the crossroads of signal transduction. J. Cell Sci. 110: 401-407.
35. Kassner, P.D., Alon, R., Springer, T.A., and Hemler, M.E. 1995. Specialized functional properties of the integrin α4 cytoplasmic domain. Mol. Biol. Cell 6: 661-674.
36. Keely, P.J., Fong, A.M., Zutter, M.M., and Santoro, S.A. 1995. Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense α2 integrin mRNA in mammary cells. J. Cell Sci. 108: 595-607.
37. Klemke, R.L., Cai, S., Giannini, A.L., Gallagher, P.J., de Lanerolle, P., and Cheresh, D.A. 1997. Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137: 481-492.
38. Kornberg, L.J., Earp, H.S., Turner, C.E., Prockop, C., and Juliano, R.L. 1991. Signal transduction by integrins: Increased protein tyrosine phosphorylation caused by clustering of β1 integrins. Proc. Natl. Acad. Sci. U.S.A. 88: 8392-8396.
39. Lauffenburger, D.A., and Horwitz, A.F. 1996. Cell migration: A physically integrated molecular process. Cell, 84: 359-369.
40. Liu, F., Sells, M.A., and Chernoff, J. 1998. Protein tyrosine phosphatase 1B negatively regulates integrin signaling. Curr. Biol. 8: 173-176.
41. Lozano, Y., Taitz, A., Petruzzelli, G.J., Djordjevic, A., and Young, M.R. 1996. Prostaglandin E2-protein kinase A signaling and protein phosphatases-1 and -2A regulate human head and neck squamous cell carcinoma motility, adherence, and cytoskeletal organization. Prostaglandins, 51: 35-48.
42. Lu, T.T., Yan, L.G., and Madri, J.A. 1996. Integrin engagement mediates tyrosine dephosphorylation on platelet-endothelial cell adhesion molecule 1. Proc. Natl. Acad. Sci. U.S.A. 93: 11 808-11 813.
43. Maa, M.-C., and Leu, T.-H. 1998. Vanadate-dependent FAK activation is accomplished by the sustained FAK Tyr-576/577 phosphorylation. Biochem. Biophys. Res. Comm. 251: 344-349.
44. Maier, G.D., Wright, M.A., Lozano, Y., Djordjevic, A., Matthews, J.P., and Young, M.R.I. 1995. Regulation of cytoskeletal organization in tumor cells by protein phosphatases-1 and 2A. Int. J. Cancer, 61: 54-61.
45. Meisinger, J., Patel, S., Vellody, K., Bergstrom, R., Benefield, J., Lozano, Y., and Young, M.R.I. 1997. Protein phosphatase-2A associated with microtubules and its role in restricting the invasiveness of human head and neck squamous cell carcinoma cells. Cancer Lett. 111: 87-95.
46. Merry, C., Puri, P., and Reen, D.J. 1998. Phosphorylation and the actin cytoskeleton in defective newborn neutrophil chemotaxis. Pediatr. Res. 44: 259-264.
47. Misra-Press, A., Rim, C.S., Yao, H., Roberson, M.S., and Stork, P.J. 1995. A novel mitogen-activated protein kinase phosphatase. Structure, expression and regulation. J. Biol. Chem. 270: 14 587-14 596.
48. Muda, M., Boschert, U., Dickinson, R., Martinou, J.C., Martinou, I., Camps, M., Schlegel, W., and Arkinstall, S. 1996. MKP-3, a novel cytosolic protein-tyrosine phosphatase that exemplifies a new class of mitogen-activated protein kinase phosphatase. J. Biol. Chem. 271: 4319-4326.
49. Oliver, B.L., Garat, C., Pytela, R., and Matthay, M.A. 1997. Protein tyrosine phosphatases mediate cell readhesion in alveolar epithelial cells mechanically separtated from in vitro matrix. Am. J. Respir. Cell Mol. Biol. 16: 613-620.
50. Palecek, S.P., Loftus, J.C., Ginsberg, M.H., Lauffenburger, D.A., and Horwitz, A.F. 1997. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature (London), 385: 537-540.
51. Pukac, L., Huangpu, J., and Karnovsky, M.J. 1998. Platelet-derived growth factor-BB, insulin-like growth factor-I, and phorbol ester activate different signaling pathways for stimulation of vascular smooth muscle cell migration. Exp. Cell Res. 242: 548-560.
52. Retta, S.F., Barry, S.T., Critchley, D.R., Defilippi, P., Silengo, L., and Tarone, G. 1996. Focal adhesion and stress fiber formation is regulated by tyrosine phosphatase activity. Exp. Cell Res. 229: 307-317.
53. Rogers, M.V., Buensuceso, C., Montague, F., and Mahadevan, L. 1994. Vanadate stimulates differentiation and neurite outgrowth in rat pheochromocytoma PC 12 cells and neurite extension in human neuroblastoma SH-SY5Y cells. Neuroscience, 60: 479-494.
54. Rousseau, S., Houle, F., Landry, J., and Huot, J. 1997. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene, 15: 2169-2177.
55. Ruoslahti, E., and Pierschbacher, M.D. 1987. New perspectives in cell adhesion: RGD and integrins. Science (Washington, D.C.), 238: 491-497.
56. Schaller, M.D., and Sasaki, T. 1997. Differential signaling by the focal adhesion kinase and cell adhesion kinase β. J. Biol. Chem. 272: 25 319-25 325.
57. Schaller, M.D., Borgman, C.A., Cobb, B.S., Vines, R.R., Reynolds, A.B., and Parsons, J.T. 1992. pp125Fak, a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. U.S.A. 89: 5192-5196.
58. Schlaepfer, D.D., and Hunter, T. 1997. Focal adhesion kinase overexpression enhances ras-dependent integrin signaling to ERK2/mitogen-activated protein kinase through interactions with and activation of c-Src. J. Biol. Chem. 272: 13 189-13 195.
59. Schlaepfer, D.D., and Hunter, T. 1998. Integrin signalling and tyrosine phosphorylation: just the FAKs? Trends Cell Biol. 8: 151-157.
60. Schlaepfer, D.D., Hanks, S.K., Hunter, T., and van der Geer, P. 1994. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature (London), 372: 786-791.
61. Silberman, S., Janulis, M., and Schultz, R.M. 1997. Characterization of downstream Ras signals that induce alternative protease-dependent invasive phenotypes. J. Biol. Chem. 272: 5927-5935.
62. Stewart, M., and Hogg, N. 1996. Regulation of leukocyte integrin function: affinity vs. avidity. J. Cell. Biochem. 61: 554-561.
63. Sun, H., Tonks, N.K., and Bar-Sagi, D. 1994. Inhibition of Ras-induced DNA synthesis by expression of the phosphatase MKP-1. Science (Washington, D.C.), 266: 285-288.
64. Tamura, M., Gu, J., Matsumoto, K., Aota, S.-I., Parsons, R., and Yamada, K.M. 1998. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science (Washington, D.C.), 280: 1614-1617.
65. Wary, K.K., Mainiero, F., Isakoff, S.J., Marcantonio, E.E., and Giancotti, F.G. 1996. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell, 87: 733-743.
66. Weitzman, J.B., Pujades, C., and Hemler, M.E. 1997. Integrin alpha chain cytoplasmic tails regulate "antibody-redirected" cell adhesion, independently of ligand binding. Eur. J. Immunol. 27: 78-84.
67. Wilkins, J.A., Stupack, D., Stewart, S., and Caixia, S. 1991. Beta1 integrin-mediated lymphocyte adherence to extracellular matrix is enhanced by phorbol ester treatment. Eur. J. Immunol. 21: 517-522.
68. Wright, M.B., Hugo, C., Seifert, R., Disteche, C.M., and Bowen-Pope, D.F. 1998. Proliferating and migrating mesangial cells responding to injury express a novel receptor protein-tyrosine phosphatase in experimental mesangial proliferative glomerulonephritis. J. Biol. Chem. 273: 23 929-23 937.
69. Wu, P., Hoying, J.B., Williams, S.K., Kozikowski, B.A., and Lauffenburger, D.A. 1994. Integrin-binding peptide in solution inhibits or enhances endothelial cell migration, predictably from cell adhesion. Ann. Biomed. Eng. 22: 144-152.
70. Yauch, R.L., Felsenfeld, D.P., Kraeft, S.K., Chen, L.B., Sheetz, M.P., and Hemler, M.E. 1997. Mutational evidence for control of cell adhesion through integrin diffusion/clustering, independent of ligand binding. J. Exp. Med. 186: 1347-1355.
71. Young, M.R.I., Lozano, Y., Djordjevic, A., and Maier, G.D. 1993. Protein phosphatases limit tumor motility. Int. J. Cancer, 55: 1036-1041.
72. Yu, D.-H., Qu, C.-K., Henegariu, O., Lu, X., and Feng, G.-S. 1998. Protein-tyrosine phosphatase Shp-2 regulates cell spreading, migration, and focal adhesion. J. Biol. Chem. 273: 21 125-21 131.
73. Zhang, Z., Vuori, K., Wang, H.-G., Reed, J.C., and Ruoslahti, E. 1996. Integrin activation by R-ras. Cell, 85: 61-69.