c-Cbl-dependent EphA2 protein degradation is induced by ligand binding

Molecular Cancer Research

Volumn 1, Issue 1, 2002, Pages 79-87

  Walker Daniels, Jennifer ^a   Riese II, David J ^b   Kinch, Michael S ^a,c  

^a PURDUE UNIVERSITY   (United States)

^b Purdue University   (United States)

^c MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN C CBL; EPHRIN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE EPHA2; UNCLASSIFIED DRUG;

ARTICLE; BREAST TUMOR; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INTERNALIZATION; LIGAND BINDING; MALIGNANT NEOPLASTIC DISEASE; PRIORITY JOURNAL; PROSTATE TUMOR; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; TUMOR CELL LINE;

ANTIBODIES, MONOCLONAL; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; ENDOSOMES; EPHRIN-A1; EPITHELIAL CELLS; HUMANS; LIGANDS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-CBL; RECEPTOR, EPHA2; RECOMBINANT FUSION PROTEINS; TUMOR CELLS, CULTURED; UBIQUITIN-PROTEIN LIGASES;

EID: 0344127552     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Kolibaba, K. S. and Druker, B. J. Protein tyrosine kinases and cancer. Biochim. Biophys. Acta., 1333: F217-F248, 1997.
2. Dickson, R. B. and Lippman, M. E. New approaches in the therapy of breast cancer - introduction. Breast Cancer Res. Treat., 38: 1-2, 1996.
3. Patarca, R. Protein phosphorylation and dephosphorylation in physiologic and oncologic processes. Crit. Rev. Oncog., 7: 343-432, 1996.
4. van der Geer, P., Hunter, A. J., and Lindberg, R. A. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell Biol., 10: 251-337, 1994.
5. Rubin, R. and Baserga, R. Insulin-like growth factor-I receptor. Its role in cell proliferation, apoptosis, and tumorigenicity. Lab. Invest., 73: 311-331, 1995.
6. Kim, H. G., Kassis, J., Souto, J. C., Turner, T., and Wells, A. EGF receptor signaling in prostate morphogenesis and tumorigenesis. Histol. Histopathol., 14: 1175-1182, 1999.
7. Malitschek, B., Fornzler, D., and Schartl, M. Melanoma formation in Xiphophorus: a model system for the role of receptor tyrosine kinases in tumorigenesis. BioEssays, 17: 1017-1023, 1995.
8. Shak, S. Overview of the trastuzumab (Herceptin) anti-HER2 monoclonal antibody clinical program in HER2-overexpressing metastatic breast cancer. Herceptin Multinational Investigator Study Group. Semin. Oncol., 26: 71-77, 1999.
9. Levitzki, A. and Gazit, A. Tyrosine kinase inhibition: an approach to drug development. Science, 267: 1782-1788, 1995.
10. Rusch, V., Mendelsohn, J., and Dmitrovsky, E. The epidermal growth factor receptor and its ligands as therapeutic targets in human tumors. Cytokine Growth Factor Rev., 7: 133-141, 1996.
11. Weiner, L. M. Monoclonal antibody therapy of cancer. Semin. Oncol., 26: 43-51, 1999.
12. Press, M. F., Jones, L. A., Godolphin, W., Edwards, C. L., and Slamon, D. J. HER-2/neu oncogene amplification and expression in breast and ovarian cancers. Prog. Clin. Biol. Res., 354A: 209-221, 1990.
13. Baselga, J., Norton, L., Albanell, J., Kim, Y-M., and Mendelsohn, J. Recombinant humanized anti-HER2 antibody (Herceptin) enhances the antitumor activity of paclitaxel and doxorubicin against HER2/neu overexpressing breast cancer xenografts. Cancer Res., 58: 2825-2831, 1998.
14. Klapper, L. N., Waterman, H., Sela, M., and Yarden, Y. Tumor-inhibitory antibodies to HER-2/ErbB-2 may act by recruiting c-Cbl and enhancing ubiquitination of HER-2. Cancer Res., 60: 3384-3388, 2000.
15. Reese, D. M. and Slamon, D. J. HER-2/neu signal transduction in human breast and ovarian cancer. Stem Cells, 15: 1-8, 1997.
16. Lindberg, R. A. and Hunter, T. cDNA cloning and characterization of eck, an epithelial cell receptor protein-tyrosine kinase in the eph/elk family of protein kinases. Mol. Cell. Biol., 10: 6316-6324, 1990.
17. Bartley, T. D., Hunt, R. W., Welcher, A. A., Boyle, W. J., Parker, V. P., Lindberg, R. A., Lu, H. S., Colombero, A. M., Elliott, R. L., and Guthrie, B. A. B61 is a ligand for the ECK receptor protein-tyrosine kinase. Nature, 368: 558-560, 1994.
18. Gale, N. W. and Yancopoulos, G. D. Ephrins and their receptors: a repulsive topic? Cell Tissue Res., 290: 227-241, 1997.
19. Pasquale, E. B. The Eph family of receptors. Curr. Opin. Cell Biol., 9: 608-615, 1997.
20. Rosenberg, I. M., Goke, M., Kanai, M., Reinecker, H. C., and Podolsky, D. K. Epithelial cell kinase-B61: an autocrine loop modulating intestinal epithelial migration and barrier function. Am. J. Physiol., 273: G824-G832, 1997.
21. Pandey, A., Shao, H., Marks, R. M., Polverini, P. J., and Dixit, V. M. Role of B61, the ligand for the Eck receptor tyrosine kinase, in TNF-α-induced angiogenesis. Science, 268: 567-569, 1995.
22. Magal, E., Holash, J. A., Toso, R. J., Chang, D., Lindberg, R. A., and Pasquale, E. B. B61, a ligand for the Eck receptor protein-tyrosine kinase, exhibits neurotrophic activity in cultures of rat spinal cord neurons. J. Neurosci. Res., 43: 735-744, 1996.
23. Easty, D. J., Herlyn, M., and Bennett, D. C. Abnormal protein tyrosine kinase gene expression during melanoma progression and metastasis. Int. J. Cancer, 60: 129-136, 1995.
24. Walker-Daniels, J., Coffman, K., Azimi, M., Rhim, J. S., Bostwick, D. G., Snyder, P., Kerns, B. J., Waters, D. J., and Kinch, M. S. Overexpression of the EphA2 tyrosine kinase in prostate cancer. Prostate, 41: 275-280, 1999.
25. Zantek, N. D., Azimi, M., Fedor-Chaiken, M., Wang, B., Brackenbury, R., and Kinch, M. S. E-cadherin regulates the function of the EphA2 receptor tyrosine kinase. Cell Growth & Differ., 10: 629-638, 1999.
26. Zantek, N. D., Walker-Daniels, J., Stewart, J. C., Hansen, R. K., Robinson, D., Miao, H., Wang, B., Kung, H. J., Bissell, M. J., and Kinch, M. S. MCF-10A-NeoST: a new cell system for studying cell-ECM and cell-cell interactions in breast cancer. Clin. Cancer Res., 7(11): 3640-3648, 2001.
27. Zelinski, D. P., Zantek, N. D., Stewart, J., Irizarry, A., and Kinch, M. S. EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res., 61: 2301-2306, 2001.
28. Easty, D. J., Guthrie, B. A., Maung, K., Farr, C. J., Lindberg, R. A., Toso, R. J., Herlyn, M., and Bennett, D. C. Protein B61 as a new growth factor: expression of B61 and up-regulation of its receptor epithelial cell kinase during melanoma progression. Cancer Res., 55: 2528-2532, 1995.
29. Birchmeier, W. E-cadherin as a tumor (invasion) suppressor gene. BioEssays, 17: 97-99, 1995.
30. Volberg, T., Zick, Y., Dror, R., Sabanay, I., Gilon, C., Levitzki, A., and Geiger, B. The effect of tyrosine-specific protein phosphorylation on the assembly of adherens-type junctions. EMBO J., 11: 1733-1742, 1992.
31. Zetter, B. R. Adhesion molecules in tumor metastasis. Semin. Cancer Biol., 4: 219-229, 1993.
32. Miao, H., Burnett, E., Kinch, M. S., Simon, E., and Wang, B. EphA2 kinase associates with focal adhesion kinase and upon activation, inhibits integrin-mediated cell adhesion and migration. Nat. Cell Biol., 2: 62-69, 2000.
33. Pandey, A., Lazar, D. F., Saltiel, A. R., and Dixit, V. M. Activation of the Eck receptor protein tyrosine kinase stimulates phosphatidylinositol 3-kinase activity. J. Biol. Chem., 269: 30154-30157, 1994.
34. Pandey, A., Lindberg, R. A., and Dixit, V. M. Cell signalling. Receptor orphans find a family. Curr. Biol., 5: 986-989, 1995.
35. Carpenter, G. and Cohen, S. Epidermal growth factor. J. Biol. Chem., 265: 7709-7712, 1990.
36. Carpenter, G. The EGF receptor: a nexus for trafficking and signaling. BioEssays, 22: 697-707, 2000.
37. Sorkin, A., Waters, C., Overholser, K. A., and Carpenter, G. Multiple autophosphorylation site mutations of the epidermal growth factor receptor. Analysis ofkinase activity and endocytosis. J. Biol. Chem., 266: 8355-8362, 1991.
38. Meng, W., Sawasdikosol, S., Burakoff, S. J., and Eck, M. J. Structure of the amino-terminal domain of Cbl complexed to its binding site on ZAP-70 kinase. Nature, 398: 84-90, 1999.
39. Miyake, S., Lupher, M. L., Andoniou, C. E., Lill, N. L., Ota, S., Douillard, P., Rao, N., and Band, H. The Cbl protooncogene product: from an enigmatic oncogene to center stage of signal transduction. Crit. Rev. Oncog., 8: 189-218, 1997.
40. Langdon, W. Y. The cbl oncogene: a novel substrate of protein tyrosine kinases. Aust. N. Z. J. Med., 25: 859-864, 1995.
41. Langdon, W. Y., Hartley, J. W., Klinken, S. P., Ruscetti, S. K., and Morse, H. C., III. v-cbl, an oncogene from a dual-recombinant murine retrovirus that induces early B-lineage lymphomas. Proc. Natl. Acad. Sci. USA, 86: 1168-1172, 1989.
42. Thien, C. B. and Langdon, W. Y. EGF receptor binding and transformation by v-cbl is ablated by the introduction of a loss-of-function mutation from the Caenorhabditis elegans sli-I gene. Oncogene, 14: 2239-2249, 1997.
43. Andoniou, C. E., Thien, C. B., and Langdon, W. Y. Tumour induction by activated abl involves tyrosine phosphorylation of the product of the cbl oncogene. EMBO J., 13: 4515-4523, 1994.
44. Pandey, A., Duan, H., and Dixit, V. M. Characterization of a novel src-like adapter protein that associates with the Eck receptor tyrosine kinase. J. Biol. Chem., 270: 19201-19204, 1995.
45. Carles-Kinch, K., Kilpatrick, K. E., Stewart, J. C., and Kinch, M. S. Antibody targeting of the EphA2 tyrosine kinase inhibits malignant cell behavior. Cancer Res., 62: 2840-2847, 2002.
46. Waterman, H., Levkowitz, G., Alroy, I., and Yarden, Y. The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor. J. Biol. Chem., 274: 22151-22154, 1999.
47. Ueno, H., Sasaki, K., Miyagawa, K., Honda, H., Mitani, K., Yazaki, Y., and Hirai, H. Antisense repression of proto-oncogene c-Cbl enhances activation of the JAK-STAT pathway but not the ras pathway in epidermal growth factor receptor signaling. J. Biol. Chem., 272: 8739-8743, 1997.
48. Miyake, S., Lupher, M. L., Jr., Druker, B., and Band, H. The tyrosine kinase regulator Cbl enhances the ubiquitination and degradation of the platelet-derived growth factor receptor α. Proc. Natl. Acad. Sci. USA, 95: 7927-7932, 1998.
49. Levkowitz, G., Waterman, H., Ettenberg, S. A., Katz, M., Tsygankov, A. Y., Alroy, I., Lavi, S., Iwai, K., Reiss, Y., Ciechanover, A., Lipkowitz, S., and Yarden, Y. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell, 4: 1029-1040, 1999.
50. Joazeiro, C. A., Wing, S. S., Huang, H., Leverson, J. D., Hunter, T., and Liu, Y. C. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science, 286: 309-312, 1999.
51. Yokouchi, M., Kondo, T., Houghton, A., Bartkiewicz, M., Horne, W. C., Zhang, H., Yoshimura, A., and Baron, R. Ligand-induced ubiquitination of the epidermal growth factor receptor involves the interaction of the c-Cbl RING finger and UbcH7. J. Biol. Chem., 274: 31707-31712, 1999.
52. Feshchenko, E. A., Langdon, W. Y., and Tsygankov, A. Y. Fyn, Yes, and Syk phosphorylation sites in c-Cbl map to the same tyrosine residues that become phosphorylated in activated T cells. J. Biol. Chem., 273: 8323-8331, 1998.
53. de Jong, R., ten Hoeve, J., Heisterkamp, N., and Groffen, J. Crk1 is complexed with tyrosine-phophorylated cbl in PH-positive leukemia. J. Biol. Chem., 270: 21468-21471, 1995.
54. Jain, S. K., Langdon, W. Y., and Varticovski, L. Tyrosine phosphorylation of p120cbl in BCR/abl transformed hematopoietic cells mediates enhanced association with phosphatidylinositol 3-kinase. Oncogene, 14: 2217-2228, 1997.
55. Tanaka, S., Amling, M., Neff, L., Peyman, A., Uhlmann, E., Levy, J. B., and Baron, R. c-Cbl is downstream of c-Src in a signalling pathway necessary for bone resorption. Nature, 383: 528-531, 1996.
56. Garcia-Guzman, M., Larsen, E., and Vuori, K. The proto-oncogene c-Cbl is a positive regulator of Met-induced MAP kinase activation: a role for the adaptor protein Crk. Oncogene, 19: 4058-4065, 2000.
57. Yoon, C. H., Lee, J., Jongeward, G. D., and Sternberg, P. W. Similarity of sli-1, a regulator of vulval development in C. elegans, to the mammalian proto-oncogene c-cbl. Science, 269: 1102-1105, 1995.
58. Wang, Y., Yeung, Y. G., Langdon, W. Y., and Stanley, E. R. c-Cbl is transiently tyrosine-phosphorylated, ubiquitinated, and membrane-targeted following CSF-1 stimulation of macrophages. J. Biol. Chem., 271: 17-20, 1996.
59. Kinch, M. S. and Burridge, K. Altered adhesions in ras-transformed breast epithelial cells. Biochem. Soc. Trans., 23: 446-450, 1995.
60. Davis, S., Gale, N. W., Aldrich, T. H., Maisonpierre, P. C., Lhotak, V., Pawson, T., Goldfarb, M., and Yancopoulos, G. D. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science, 266: 816-819, 1994.
61. Kinch, M. S., Kilpatrick, K., and Zhong, C. Identification of tyrosine phosphorylated adhesion proteins in human cancer cells. Hybridoma, 17: 227-235, 1998.
62. Bae, S., Arand, G., Azzam, H., Pavasant, P., Torri, J., Frandsen, T., and Thompson, E. Molecular and cellular analysis of basement membrane invasion by human breast cancer cells in Matrigel-based in vitro assays. Breast Cancer Res, Treat., 24: 241-255, 1993.
63. Kinch, M. S., Clark, G. J., Der, C. J., and Burridge, K. Tyrosine phosphorylation regulates the adhesions of ras-transformed breast epithelia. J. Cell Biol., 130: 461-471, 1995.
64. Riese, D. J. and DiMaio, D. An intact PDGF signaling pathway is required for efficient growth transformation of mouse C127 cells by the bovine papillomavirus E5 protein. Oncogene, 10: 1431-1439, 1995.