The linker phosphorylation site Tyr292 mediates the negative regulatory effect of Cbl on ZAP-70 in T cells

Journal of Immunology

Volumn 164, Issue 9, 2000, Pages 4616-4626

  Rao, Navin ^a   Lupher Jr , Mark L ^a,b   Satoshi, Ota ^a   Reedquist, Kris A ^a,c   Druker, Brian J ^d   Band, Hamid ^a,e  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b ELI LILLY AND COMPANY   (United States)

^c UTRECHT UNIVERSITY   (Netherlands)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e Smith Building ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; ENZYME REGULATION; GENE OVEREXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EID: 0034192088     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.164.9.4616     Document Type: Article

References (53)

1. Lupher, M. L. Jr., C. E. Andoniou, D. Bonita, S. Miyake, and H. Band, 1998. The c-Cbl oncoprotein. Int. J. Biochem. Cell Biol. 30:439.
2. Miyake, S., M. L. Lupher, Jr., C. E. Andoniou, N. L. Lill, S. Ota, P. Douillard, N. Rao, and H. Band. 1997. The Cbl protooncogene product: from an enigmatic oncogene to center stage of signal transduction. Crit. Rev. Oncog. 8:189.
3. Lupher, M. L., Jr., N. Rao, M. J. Eck, and H. Band. 1999. The Cbl protooncoprotein: a negative regulator of immune receptor signal transduction. Immunol. Today 20:375.
4. Langdon, W. Y. 1995. The cbl oncogene: a novel substrate of protein tyrosine kinases. Aust. N. Z. J. Med. 25:859.
5. Liu, Y. C., and A. Altman. 1998. Cbl: complex formation and functional implications. Cell. Signalling 10:377.
6. Smit, L., and J. Borst. 1997. The Cbl family of signal transduction molecules. Crit. Rev. Oncog. 8:359.
7. Feshchenko, E. A., W. Y. Langdon, and A. Y. Tsygankov. 1998. 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.
8. Marengere, L. E., C. Mirtsos, I. Kozieradzki, A. Veillette, T. W. Mak, and J. M. Penninger. 1997. Proto-oncoprotein Vav interacts with c-Cbl in activated thymocytes and peripheral T cells. J. Immunol. 159:70.
9. Keane, M. M., S. A. Ettenberg, M. M. Nau, P. Banerjee, M. Cuello, J. Penninger, and S. Lipkowitz. 1999. cbl-3; a new mammalian cbl family prolein. Oncogene 18-3365.
10. Bonita, D. P., S. Miyake, M. L. Lupher, Jr., W. Y. Langdon, and H, Band. 1997. Phosphotyrosine binding domain-dependent up-regulation of the platelet-derived growth factor receptor a signaling cascade by transforming mutants of Cbl: implications for Cbl's function and oncogenicity. Mol. Cell. Biol. 17:4517.
11. Bowlell, D. D., and W. Y. Langdon. 1995. The protein product of Ihe c-cbl oncogene rapidly complexes with the EGF receptor and is tyrosine phosphorylated following EGF stimulation. Oncagene 11:1561.
12. Lupher, M. L., Jr., K. A. Reedquist, S. Miyake, W. Y. Langdon, and H. Band. 1996. A novel phosphotyrosine-binding domain in the N-terminal transforming region of Cbl interacts directly and selectively with ZAP-70 in T cells. J. Biol. Chem. 271:24063.
13. Lupher, M. L. Jr., Z. Songyang, S. E. Shoelson, L. C. Cantley, and H. Band. 1997. The Cbl phosphotyrosine-binding domain selects a D(N/D)XpY motif and binds to the Tyr292 negative regulatory phosphorylation site of ZAP-70. J. Biol. Chem. 272:33140
14. Lupher, M. L., Jr., N. Rao, N. L. Lill, C. E. Andoniou, S. Miyake, E. A. Clark, B. Druker, and H. Band. 1998. Cbl-mediated negative regulation of the Syk tyrosine kinase: a critical role for Cbl phosphotyrosine-binding domain binding to Syk phosphotyrosine 323. J. Biol. Chem. 273:35273.
15. Deckert, M., C. Elly, A. Altman, and Y. C. Liu. 1998. Coordinated regulation of the lyrosine phosphorylation of Cbl by Fyn and Syk tyrosine kinases. J. Biol. Chem. 273:8867.
16. Fukazawa, T., S. Miyake, V. Band, and H. Band. 1996. Tyrosine phosphorylation of Cbl upon epidermal growth factor (EGF) stimulation and its association with EGF receptor and downstream signaling proteins. J. Biol. Chem. 271:14554.
17. Meng, W., S. Sawasdikosol, S. J. Burakoff, and M. J. Eck. 1999. Structure of the amino-terminal domain of Cbl complexed to its binding site on ZAP-70 kinase. Nature 398:84.
18. Thien, C. B., and W. Y. Langdon. 1998. c-Cbl: a regulator of T cell receptor-mediated signalling. Immunol. Cell Biol 76:473.
19. Yoon, C. H., J. Lee, G. D. Jongeward, and P. W. Sternberg. 1995. Similarity of sli-1, a regulator of vulval development in C. elegans, to the mammalian protooncogene c-cbl. Science 269:1102.
20. Meisner, H., A. Daga, J. Buxton, B. Fernandez, A. Chawla, U. Banerjee, and M. P. Czech. 1997. Interactions of Drosophila Cbl with epidermal growth factor receptors and role of Cbl in R7 photoreceptor cell development. Mol. Cell. Biol. 17:2217.
21. Hime, G. R., M. P. Dhungat, A. Ng, and D. D. Bowtell. 1997. D-Cbl, the Drosophila homologue of the c-Cbl proto-oncogene, interacts with the Drosophila EGF receptor in vivo, despite lacking C-terminal adaptor binding sites. Oncogene 14:2709.
22. Murphy, M. A., R. G. Schnall, D. J. Venter, L. Barnett, I. Bertoncello, C. B. Thien, W. Y. Langdon, and D. D. Bowtell. 1998. Tissue hyperplasia and enhanced T-cell signalling via ZAP 70 in c-Cbl-delicient mice. Mol. Cell. Biol. 18:4872.
23. Naramura, M. H. K. Kole, R. J. Hu, and H. Gu. 1998. Altered thymic positive selection and intracellular signals in Cbl-deficient mice. Proc. Natl. Acad. Sci. USA 95:15547.
24. Miyake, S., M. L. Lupher, Jr., B. Drukcr, and H. Band. 1998. 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.
25. Miyake, S., K. P. Mullane-Robinson, N. L. Lill, P. Douillard, and H. Band. 1999. Cbl-mediated negative regulation of platelet-derived growth factor receptor-dependent cell proliferation: a critical role for Cbl tyrosine kinase-binding domain. J. Biol. Chem. 274:16619.
26. Thien, C. B., and W. Y. Langdon. 1997. EGF receptor binding and transformation by v-cbl is ablated by the introduction of a loss-of-function mutation from the Caenorhabditis elegans sli-1 gene. Oncogene 14:2239.
27. Lee, P. S., Y. Wang, M. G. Dominguez, Y. G. Yeung, M. A. Murphy, D. D. Bowtell, and E. R. Stanley. 1999. The Cbl protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation. EMBO J. 18:3616.
28. Ota, Y., and L. E. Samelson. 1997. The product of the proto-oncogene c-cbl: a negative regulator of the Syk tyrosine kinase. Science 276:418.
29. Wange, R. L., R. Guitian, N. Isakov, J. D. Watts, R. Aebersold, and L. E. Samelson. 1995. Activating and inhibitory mutations in adjacent lyrosines in the kinasc domain of ZAP-70. J. Biol. Chem. 270:18730.
30. Chan, A. C., M. Dalton, R. Johnson, G. H. Kong, T. Wang, R. Thoma, and T. Kurosaki. 1995. Activation of ZAP-70 kinase activity by phosphorylation of tyrosine 493 is required for lymphocyte antigen receptor function. EMBO J. 14:2499.
31. Zhao, Q. and A. Weiss. 1996. Enhancement of lymphocyte responsiveness by a gain-of-function mutation of ZAP-70. Mol. Cell. Biol. 16:6765.
32. Keshvara, L. M., C. C. Isaacson, T. M. Yankee, R. Sarac, M. L. Harrison, and R. L. Geahlen. 1998. Syk- and Lyn-dependent phosphorylation of Syk on multiple tyrosines following B cell activation includes a site that negatively regulates signaling. J. Immunol. 161:5276.
33. Kong, G., M. Dalton, J. B. Wardenburg, D. Straus, T. Kurosaki, and A. C. Chan. 1996. Distinct tyrosine phosphorylation sites in ZAP-70 mediate activation and negative regulation of antigen receptor function. Mol. Cell. Biol. 16:5026.
34. Thien, C. B., D. D. Bowtell, and W. Y. Langdon. 1999. Perturbed regulation of ZAP-70 and sustained tyrosine phosphorylation of LAT and SLP-76 in c-Cbl-deficient thymocytes. J. Immunol. 162:7133.
35. Williams, B. L., K. L. Schreiber, W. Zhang, R. L. Wange, L. E. Samelson, P. J. Leibson, and R. T. Abraham. 1998. Genetic evidence for differential coupling of Syk family kinases to the T-cell receptor: reconstitution studies in a ZAP-70-deficient Jurkat T-cell line. Mol. Cell. Biol. 18:1388.
36. Reedquist, K. A., T. Fukazawa, G. Panchamoorthy, W. Y. Langdon, S. E. Shoelson, B. J. Druker, and H. Band. 1996. Stimulation through the T cell receptor induces Cbl association with Crk proteins and the guanine nucleolide exchange protein C3G. J Biol. Chem. 271:8435.
37. Druker, B. J., H. J. Mamon, and T. M. Roberts, 1989. Oncogenes, growth factors, and signal transduction. N. Engl. J. Med. 321:1383.
38. Spits, H., G. Keizer, J. Borst, C. Terhorst, A. Hekman, and J. E. de Vries. 1983. Characterization of monoclonal antibodies against cell surface molecules associated with cytotoxic activity of natural and activated killer cells and cloned CTL lines. Hybridoma 2:423.
39. Wilson, I. A., H. L. Niman, R. A. Houghten, A. R. Cherenson, M. L. Connolly, and R. A. Lerner. 1984. The structure of an antigenic determinant in a protein. Cell 37:767.
40. Barnstable, C. J., W. F. Bodmer, G. Brown, G. Galfre, C. Milstein, A. F. Williams, and A. Ziegler. 1978. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens: new tools for genetic analysis. Cell 14:9.
41. lck, a protein tyrosine kinase which mediates interleukin-2-induced activation of the c-fos gene. Mol. Cell. Biol. 14:5812.
42. Andoniou, C. E., C. B. Thien, and W. Y. Langdon. 1994. Tumor induction by activated abl involves tyrosine phosphorylalion of the product of the cbl oncogene. EMBO J. 13:4515.
43. Garcia-Rodriguez, C., and A. Rao. 1998. Nuclear factor of activated T cells (NFAT)-dependent transactivation regulated by the coactivalors p300/CREB-binding protein (CBP). J. Exp. Med. 187:2031.
44. Cantrell, D. 1996. T cell antigen receptor signal transduction pathways. Annu. Rev. Immunol 14:259.
45. Zhao, Q., B. L. Williams, R. T. Abraham, and A. Weiss. 1999. Interdomain B in ZAP-70 regulates but is not required for ZAP-70 signaling function in lymphocytes. Mol Cell. Biol. 19:948.
46. 2+ stimulated activation of nuclear factor of activated T cells by a constitutively active Cbl mutant in T cells. J. Biol. Chem. 272:168.
47. Van Leeuwen, J. E., P. K. Paik, and L. E. Samelson, 1999. Activation of nuclear factor of activated T cells (NFAT) and activating protein 1 (AP-1) by oncogenic 70Z Cbl requires an intact phosphotyrosine binding domain but not Crk(L) or p85 phosphatidylinositol 3-kinase association. J. Biol. Chem. 274:5153.
48. Zhang, Z., C. Elly, A. Altman, and Y. C. Liu. 1999. Dual regulation of T cell receptor-mediated signaling by oncogenic Cbl mutant 70Z. J. Biol. Chem. 274: 4883.
49. Chu, D. H., C. T. Morita, and A. Weiss. 1998. The Syk family of protein tyrosine kinases in T-cell activation and development. Immunol. Rev. 165:167.
50. Chu, D. H., H. Spits, J. F. Peyron, R. B. Rowky, J. B. Bolen, and A. Weiss. 1996. The Syk protein tyrosine kinase can function independently of CD45 or Lck in T cell antigen receptor signaling. EMBO J. 15:6251.
51. Kolanus, W., C. Romeo, and B. Seed. 1993. T cell activation by clustered tyrosine kinases. Cell 74:171.
52. Latour, S., L. M. L. Chow, and A. Veillette. 1996. Differential intrinsic enzymatic activity of Syk and Zap-70 protein-tyrosine kinases. J. Biol. Chem. 271:22782.
53. Penna, D., S. Muller, F. Martinon, S. Demotz, M. Iwashima, and S. Valitutti. 1999. Degradation of ZAP-70 following antigenic stimulation in human T lymphocytes: role of calpain proteolytic pathway. J. Immunol 163:50.