Distinct tyrosine autophosphorylation sites negatively and positively modulate neu-mediated transformation

Molecular and Cellular Biology

Volumn 17, Issue 9, 1997, Pages 5410-5425

  Dankort, David L ^a   Wang, Zhixiang ^b   Blackmore, Valerie ^a   Moran, Michael F ^b   Muller, William J ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE; TYROSINE;

ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; BREAST CANCER; CELL STRAIN 3T3; CELL TRANSFORMATION; CONTROLLED STUDY; FIBROBLAST CULTURE; MITOGENESIS; NONHUMAN; ONCOGENE C ERB; OVARY CANCER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0030794283     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.9.5410     Document Type: Article

References (77)

1. Akiyama, T., S. Matsuda, Y. Namba, T. Saito, K. Toyoshima, and T. Yamamoto. 1991. The transforming potential of the c-erbB-2 protein is regulated by autophosphorylation at the carboxyl-terminal domain. Mol. Cell. Biol. 11:833-842.
2. Arvidsson, A.-K., E. Rupp, E. Nanberg, J. Downward, L. Ronnstrand, S. Wennstrom, J. Schlessinger, C.-H. Heldin, and L. Claesson-Welsh. 1994. Tyr-716 in the platelet-derived growth factor β-receptor kinase insert is involved in GRB2 binding and Ras activation. Mol. Cell. Biol. 14:6715-6726.
3. Bargmann, C. I., M.-C. Hung, and R. A. Weinberg. 1986. Multiple independent activations of the neu oncogene by a point mutation altering the transmembrane domain of p185. Cell 45:649-657.
4. Bargmann, C. I., M.-C. Hung, and R. A. Weinberg. 1986. The neu oncogene encodes an epidermal growth factor receptor-related protein. Nature 319: 226-230.
5. Bargmann, C. I., and R. A. Weinberg. 1988. Increased tyrosine kinase activity associated with the protein encoded by the activated neu oncogene. Proc. Natl. Acad. Sci. USA 85:5394-5398.
6. Batzer, A. G., P. Blaikie, K. Nelson, and B. Margolis. 1995. The phosphotyrosine interaction domain of Shc binds an LXNPXY motif on the epidermal growth factor receptor. Mol. Cell. Biol. 15:4403-4409.
7. Batzer, A. G., D. Rotin, J. M. Urena, E. Y. Skolnik, and J. Schlessinger. 1994. Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor. Mol. Cell. Biol. 14:5192-5201.
8. Ben-Levy, R., H. F. Paterson, C. J. Marshall, and Y. Yarden. 1994. A single autophosphorylation site confers oncogenicity to the Neu/ErbB-2 receptor and enables coupling to the MAP kinase pathway. EMBO J. 13:3302-3311.
9. Blaikie, P., D. Immanuel, J. Wu, N. Li, V. Yajnik, and B. Margolis. 1994. A region in Shc distinct from the SH2 domain that can bind tyrosine-phosphorylated growth factor receptors. J. Biol. Chem. 269:32031-32034.
10. Bork, P., and B. Margolis. 1995. A phosphotyrosine interaction domain. Cell 80:693-694.
11. Bouchard, L., L. Lamarre, P. J. Trembley, and P. Jolicoeur. 1989. Stochastic appearance of mammary tumors in transgenic mice carrying the c-neu oncogene. Cell 57:931-936.
12. Buday, L., and J. Downward. 1993. Epidermal growth factor regulates p21ras through the formation of a complex of receptor, Grb2 adapter protein, and SOS nucleotide exchange factor. Cell 73:611-620.
13. Chardin, P., J. H. Camonis, N. W. Gale, L. V. Aelst, J. Schlessinger, N. H. Wigler, and D. Bar-Sagi. 1993. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to GRB2. Science 260:1338-1343.
14. Cleghon, V., U. Gayko, T. D. Copeland, L. A. Perkins, N. Perrimon, and D. K. Morrison. 1996. Drosophila terminal structure development is regulated by the compensatory activities of positive and negative phosphotyrosine signaling sites on the Torso RTK. Genes Dev. 10:566-577.
15. Coussens, L., T. L. Yang-Feng, Y.-C. Liao, E. Chen, A. Gray, J. McGrath, P. H. Seeburg, T. A. Libermann, J. Schlessinger, U. Francke, A. Levinson, and A. Ullrich. 1985. Tyrosine kinase receptor with extensive homology to EGF receptor shares chromosome location with neu oncogene. Science 230:1132-1139.
16. D'Ambrosio, D., K. L. Hippen, S. A. Minskov, I. Mellman, G. Pani, K. A. Siminovitch, and J. C. Cambier. 1995. Recruitment and activation of PTP1C in negative regulation of antigen receptor signalling by FcγRIIB1. Science 268:293-297.
17. Dankort, D. L., and W. J. Muller. Unpublished data.
18. Di Fiore, P. P., O. Segatto, F. Lonardo, F. Fazioli, J. H. Pierce, and S. A. Aaronson. 1990. The carboxy-terminal domain of erbB2 and epidermal growth factor receptor exert different regulatory effects on intrinsic receptor tyrosine kinase function and transforming activity. Mol. Cell. Biol. 10:2749-2756.
19. 1 in BALB/c 3T3 cells. Mol. Cell. Biol. 14:5441-5449.
20. Drebin, J. A., V. C. Link, D. F. Stern, R. A. Weinberg, and M. I. Greene. 1985. Down-modulation of an oncogene protein product and reversion of the transformed phenotype by monoclonal antibodies. Cell 41:695-706.
21. Egan, S. E., B. W. Giddings, M. W. Brooks, L. Buday, A. M. Sizeland, and R. A. Weinberg. 1993. Association of SOS ras exchange protein with GRB2 is implicated in tyrosine kinase signal transduction and transformation. Nature 360:45-51.
22. Fazioli, F., U.-H. Kim, S. G. Rhee, C. J. Molloy, O. Segatto, and P. P. DiFiore. 1991. The erbB-2 mitogenic signaling pathway: tyrosine phosphorylation of phopholipase C-γ and GTPase-activating protein does not correlate with erbB-2 mitogenic potency. Mol. Cell. Biol. 11:2040-2048.
23. Gale, N. W., S. Kaplan, E. J. Lowenstein, J. Schlessinger, and D. Bar-Sagi. 1993. Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature 363:88-92.
24. Goga, A., J. McLaughlin, D. E. H. Afar, D. C. Saffran, and O. N. Witte. 1995. Alternative signals to Ras for hemalopoietic transformation by the BCR-ABL oncogene. Cell 82:981-988.
25. Gotoh, N., A. Tojo, K. Muroya, Y. Hashimoto, S. Hattori, S. Nakamura, T. Takenawa, Y. Yazaki, and M. Shibuya. 1994. Epidermal growth factor-receptor mutant lacking the autophosphorylation sites induces phosphorylation of Shc protein and Shc-Grb2/ASH association and retains mitogenic activity. Proc. Natl. Acad. Sci. USA 91:161-171.
26. Gotoh, N., M. Toyoda, and M. Shibuya. 1997. Tyrosine phosphorylation sites at amino acids 239 and 240 of Shc are involved in epidermal growth factor-induced mitogenic signaling that is distinct from Ras/mitogen-activated protein kinase activation. Mol. Cell. Biol. 17:1824-1831.
27. Guy, C. T., M. A. Webster, M. Schaller, T. J. Parsons, R. A. Cardiff, and W. J. Muller. 1992. Expression of the neu protooncogene in the mammary epithlium of transgenic mice induces metastatic disease. Proc. Natl. Acad. Sci. USA 89:10578-10582.
28. Harlow, E., and D. L. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
29. Hazan, R., B. Margolis, M. Dombalagian, A. Ullrich, A. Ziilberstein, and J. Schlessinger. 1989. Identification of autophosphorylation sites of HER2/neu. Cell Growth Differ. 1:3-7.
30. Hu, Q., D. Milfay, and L. T. Williams. 1995. Binding of NCK to SOS and activation of Ras-dependent gene expression. Mol. Cell. Biol. 15:1169-1174.
31. Hynes, N. E., and D. F. Stern. 1994. The biology of erbB-2/neu/HER-2 and its role in cancer. Biochim. Biophys. Acta 1198:165-184.
32. Jallal, B., J. Schlessinger, and A. Ullrich. 1992. Tyrosine phosphatase inhibition permits analysis of signal transduction complexes in p185HER2/neu-overexpressing human tumor cells. J. Biol. Chem. 267:4357-4363.
33. Janes, P. W., R. J. Daly, A. deFazio, and R. L. Sutherland. 1994. Activation of the Ras signalling pathway in human breast cancer cells overexpressing erbB-2. Oncogene 9:3601-3608.
34. Kavanaugh, W. M., C. W. Turck, and L. T. Williams. 1995. PTB domain binding to signaling proteins through a sequence motif containing phosphotyrosine. Science 268:1177-1179.
35. Klingmuller, U., U. Lorenz, L. C. Cantley, B. G. Neel, and H. F. Lodish. 1995. Specific recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of JAK2 and termination of proliferative signals. Cell 80: 729-738.
36. Laminet, A. A., G. Apell, L. Conroy, and W. M. Kavanaugh. 1996. Affinity, specificity, and kinetics of the interaction of the SHC phosphotyrosine binding domain with asparagine-X-X - phosphotyrosine motifs of growth factor receptors. J. Biol. Chem. 271:264-269.
37. Li, N., A. Batzer, R. Daly, V. Yajnik, E. Skolnik, P. Chardin, D. Bar-Sagi, B. Margolis, and J. Schlessinger. 1993. Guanine-nucleotide-releasing factor hSOS1 binds to GRB2 and links receptor tyrosine kinases to ras signalling. Nature 363:85-88.
38. Li, W., R. Nishimura, A. Kashishian, A. G. Batzer, W. J. H. Kim, J. A. Cooper, and J. Schlessinger. 1994. A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol. Cell. Biol. 14:509-517.
39. Lowy, D. R., and B. M. Willumsen. 1993. Function and regulation of Ras. Annu. Rev. Biochem. 62:851-891.
40. Lutrell, D. K., A. Lee, T. J. Lansing, R. M. Crosby, K. D. Jung, D. Willard, M. Luther, M. Rodriguez, J. Berman, and T. M. Gilmer. 1994. Involvement of pp60c-src with two major signaling pathways in human breast cancer. Proc. Natl. Acad. Sci. USA 91:83-97.
41. Mansour, E. G., P. M. Ravdin, and L. Dressier. 1994. Prognostic factors in early breast carcinoma. Cancer 74:381-400.
42. Matsuda, M., Y. Hashimoto, K. Muroya, H. Hasegawa, T. Kurata, S. Tanaka, S. Nakamura, and S. Hattori. 1994. CRK protein binds two guanine nucleotide-releasing proteins for the Ras family and modulates nerve growth factor-induced activation of Ras in PC12 cells. Mol. Cell. Biol. 14:5495-5500.
43. McGlade, C. J., C. Ellis, M. Reedijk, D. Anderson, G. Mbamalu, A. D. Reith, G. Panayotou, P. End, A. Bernstein, A. Kazlauskas, M. D. Waterfield, and T. Pawson. 1992. SH2 domains of the p85a subunit of phosphatidylinositol 3-kinase regulate binding to growth factor receptors. Mol. Cell. Biol. 12:991-997.
44. McGlade, C. J., A. Cheng, G. Pelicci, P. G. Pelicci, and T. Pawson. 1992. Shc proteins are tyrosine phosphorylated and regulated by the v-src and v-fps protein-tyrosine-kinases. Proc. Natl. Acad. Sci. USA 89:8869-8873.
45. Mikami, Y., J. G. Davis, K. Dobashi, W. C. Dougall, J. N. Myers, V. I. Brown, and M. I. Greene. 1992. Carboxyl-terminal deletion and point mutations decrease the transforming potential of the activated rat neu oncogene product. Proc. Natl. Acad. Sci. USA 89:7335-7339.
46. Morgenstern, J. P., and H. Land. 1990. A series of mammalian expression vectors and characterisation of their expression of a reporter gene in stably and transiently transfected cells. Nucleic Acids Res. 18:1068.
47. Muller, W. J. E. Sinn, P. K. Pattengale, R. Wallace, and P. Leder. 1988. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54:105-115.
48. Muthuswamy, S. K., and W. J. Muller. 1995. Direct and specific interaction of c-Src with Neu is involved in signaling by the epidermal growth factor receptor. Oncogene 11:271-279.
49. Muthuswamy, S. K., P. S. Siegel, D. L. Dankort, M. A. Webster, and W. J. Muller. 1994. Mammary tumors expressing the neu proto-oncogene possess elevated c-Src tyrosine kinase activity. Mol. Cell. Biol. 14:735-743.
50. Obermeier, A., I. Tinhofer, H. H. Grunicke, and A. Ullrich. 1996. Transforming potentials of epidermal growth factor and nerve growth factor receptors inversely correlate with their phospholipase Cg affinity and signal activation. EMBO J. 15:73-82.
51. Pawson, T. 1995. Protein modules and signalling networks. Nature 373:573-580.
52. Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, F. Grignani, T. Pawson, and P. G. Pelicci. 1992. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70:93-104.
53. Ricci, A., L. Lanfrancone, R. Chiari, G. Berlardo, C. Pertica, P. G. Natali, P. G. Pelicci, and O. Segatto. 1995. Analysis of protein-protein interactions involved in the activation of the Shc/Grb-2 pathway by the ErbB-2 kinase. Oncogene 11:1519-1529.
54. Ron, D., and H. Dressler. 1992. pGSTag - a versatile bacterial expression plasmid for enzymatic labeling of recombinant proteins. BioTechniques 13: 866-869.
55. Roussel, M. F., T. J. Dull, C. W. Rettenmier, P. Ralph, A. Ullrich, and C. J. Sherr. 1987. Transforming potential of the c-fms proto-oncogene (CSF-1 receptor). Nature 325:549-552.
56. Rozakis-Adcock, M., R. Fernley, J. Wade, T. Pawson, and D. Bowtell. 1993. The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the ras activator mSOS1. Nature 363:83-85.
57. Rozakis-Adcock, M., J. McGlade, G. Mbamalu, G. Pelicci, R. Daly, W. Li, A. Batzer, S. Thomas, J. Brugge, P. G. Pelicci, J. Schlessinger, and T. Pawson. 1992. Association of the Shc and Grb2/sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360: 689-692.
58. Sainsbury, J. R. C., S. Nicholson, B. Angus, J. R. Farndon, A. J. Malcolm, and A. L. Harris. 1988. Epidermal growth factor receptor status of histological sub-types of breast cancer. Br. J. Cancer 58:458-460.
59. Salcini, A. E., J. McGlade, G. Pelicci, I. Nicoletti, T. Pawson, and P. G. Pelicci. 1994. Formation of Shc-Grb2 complexes necessary to induce neoplastic transformation by overexpression of Shc proteins. Oncogene 9:2827-2836.
60. Segatto, O., F. Lonardo, K. Helin, D. Wexler, F. Fazioli, S. G. Rhee, and P. P. Di Fiore. 1992. erbB-2 autophosphorylation is required for mitogenic action and high-affinity substrate coupling. Oncogene 7:1339-1346.
61. Segatto, O., F. Lonardo, J. H. Pierce, D. P. Bottaro, and P. P. Di Fiore. 1990. The role of autophosphorylation in modulation of erbB-2 transforming function. New Biol. 2:187-195.
62. Segatto, O., G. Pelicci, S. Giuli, G. Digeiesi, P. P. Di Fiore, J. McGlade, T. Pawson, and P. G. Pelicci. 1993. Shc products are substrates of erbB-2 kinase. Oncogene 8:2105-2112.
63. Siegel, P. M., D. L. Dankort, W. R. Hardy, and W. J. Muller. 1994. Novel activating mutations in the neu proto-oncogene involved in induction of mammary tumors. Mol. Cell. Biol. 14:7068-7077.
64. Iamon, D. J., G. M. Clark, S. G. Wong, W. J. Levin, A. Ullrich, and W. L. McGuire. 1987. Human breast cancer: correlation of relapse and survival with the amplification of the HER-2/neu oncogene. Science 235:177-182.
65. Slamon, D. J., W. Godolphin, L. A. Jones, J. A. Holt, S. G. Wong, D. E. Keith, W. J. Levin, S. G. Stuart, J. Udove, A. Ullrich, and M. F. Press. 1989. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244:707.
66. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli with glutathione S-transferase. Gene 67:31-46.
67. Songyang, Z., S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, B. G. Neel, R. B. Birge, J. E. Farjardo, M. M. Chou, H. Hanafusa, B. Schaffhausen, and L. C. Cantley. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767-778.
68. Songyang, Z., S. E. Shoelson, J. McGlade, P. Olivier, T. Pawson, X. R. Bustelo, M. Barbacid, H. Sabe, H. Hanafusa, T. Yi, R. Ren, D. Baltimore, S. Ratnofsky, R. A. Feldman, and L. C. Cantley. 1994. Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/fes, Grb2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 14:2777-2785.
69. Stein, D., J. Wu, S. A. Fuqua, C. Roonprapunt, V. Yajnik, P. D'Eustachio, J. J. Moskow, A. M. Buchberg, C. K. Osborne, and B. Margolis. 1994. The SH2 domain protein GRB7 is co-amplified, overepressed and in a tight complex with HER2 in breast cancer. EMBO J. 13:1331-1340.
70. Valius, M., and A. Kazlauskas. 1993. Phospholipase C-γ1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal. Cell 73:321-324.
71. van der Greer, P., S. Wiley, V. K.-M. Lai, J. P. Olivier, G. D. Gish, R. Stephens, D. Kaplan, S. Shoelson, and T. Pawson. 1995. A conserved aminoterminal Shc domain binds to phosphotyrosine motifs in activated receptors and phosphopeptides. Curr. Biol. 5:404-412.
72. Vogel, W., R. Lammers, J. Huang, and A. Ullrich. 1993. Activation of a phosphotyrosine phosphatase by tyrosine phosphorylation. Science 259:1611-1614.
73. Wang, Z., D. L. Dankort, W. J. Muller, and M. F. Moran. Unpublished data.
74. Wang, Z., and M. F. Moran. 1996. Requirement for the adapter protein GRB2 in EGF receptor endocytosis. Science 272:1935-1939.
75. Weiner, D. B., J. Lui, A. Cohen, W. V. Williams, and M. I. Greene. 1989. A point mutation in the neu oncogene mimics ligand induction of receptor aggregation. Nature 339:230-231.
76. Wigler, M., S. Silverstein, L. S. Lee, A. Pellicer, Y.-C. Chen, and R. Axel. 1977. Transfer of purified herpes virus thymidine kinase gene to cultured mouse cells. Cell 11:223-232.
77. Yamamoto, T., S. Ikawa, T. Akiyama, K. Semba, N. Nomura, N. Miyajima, T. Saito, and K. Toyoshima. 1986. Similarity of protein encoded by the human c-erb-B-2 gene to the epidermal growth factor receptor. Nature 319: 230-234.