Tissue hyperplasia and enhanced T-cell signalling via ZAP-70 in c-Cbl- deficient mice

Molecular and Cellular Biology

Volumn 18, Issue 8, 1998, Pages 4872-4882

  Murphy, Maria A ^a   Schnall, Ralf G ^a   Venter, Deon J ^a,b   Barnett, Louise ^c   Bertoncello, Ivan ^a   Thien, Christine B F ^d   Langdon, Wallace Y ^d   Bowtell, David D L ^a  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ROYAL MELBOURNE HOSPITAL   (Australia)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; RECEPTOR; T LYMPHOCYTE RECEPTOR; TYROSINE;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EXTRAMEDULLARY HEMATOPOIESIS; GENE DISRUPTION; GENE EXPRESSION; HOMEOSTASIS; LYMPHOID HYPERPLASIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTO ONCOGENE; T LYMPHOCYTE;

EID: 0031858649     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.8.4872     Document Type: Article

References (66)

1. Andoniou, C. E., C. Thien, and W. Y. Langdon. 1994. Tumour induction by activated Abl involves tyrosine phosphorylation of the product of the Cbl oncogene. EMBO J. 13:4515-4523.
2. Blake, T. J., M. Shapiro, H. D. Morse, and W. Y. Langdon. 1991. The sequences of the human and mouse c-Cbl proto-oncogenes show v-Cbl was generated by a large truncation encompassing a proline-rich domain and a leucine zipper-like motif. Oncogene 6:653-657.
3. Bonita, D. P., S. Miyake, M. R. Lupher, W. Y. Langdon, and H. Band. 1997. Phosphotyrosine binding domain-dependent upregulation of PDGF receptor signaling cascade by transforming mutants of Cbl: implications for Cbl's function and oncogenicity. Mol. Cell. Biol. 17:4597-4610.
4. Bowtell, D. Unpublished data.
5. Bowtell, D., and W. Y. Langdon. 1995. The protein product of the c-cbl oncogene rapidly complexes with the EGF receptor and is tyrosine phosphorylated following EGF stimulation. Oncogene 11:1561-1567.
6. Bradley, T. R., G. S. Hodgson, and M. Rosendaal. 1978. The effect of oxygen tension on haemopoietic and fibroblast cell proliferation in vitro. J. Cell. Physiol. 97:517-522.
7. Bradley, T. R., E. R. Stanley, and M. A. Sumner. 1971. Factors from mouse tissues stimulating colony growth of mouse bone marrow cells in vitro. Aust. J. Exp. Biol. Med. Sci. 49:595-603.
8. Brizzi, M. F., P. Dentelli, L. Lanfrancone, A. Rosso, P. G. Pelicci, and L. Pegoraro. 1996. Discrete protein interactions with the Grb2/c-Cbl complex in Scf-and Tpo-mediated myeloid cell proliferation. Oncogene 13:2067-2076.
9. 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. 14:2499-2508.
10. Coffman, R. L. 1982. Surface antigen expression and immunoglobulin gene rearrangement during mouse pre-B cell development. Immunol. Rev. 69:5-23.
11. Coleman, S., G. B. Silberstein, and C. W. Daniel. 1988. Ductal morphogenesis in the mouse mammary gland: evidence supporting a role for epidermal growth factor. Dev. Biol. 127:304-315.
12. Cory, G., R. C. Lovering, S. Hinshelwood, L. MacCarthy-Morrogh, R. J. Levinsky, and C. Kinnon. 1995. The protein product of the c-Cbl protooncogene is phosphorylated after B cell receptor stimulation and binds the SH3 domain of brutons tyrosine kinase. J. Exp. Med. 182:611-615.
13. Curtis, S. W., T. Washburn, C. Sewall, R. Diaugustine, J. Lindzey, J. F. Couse, and K. S. Korach. 1996. Physiological coupling of growth factor and steroid receptor signaling pathways - estrogen receptor knockout mice lack estrogen-like response to epidermal growth factor. Proc. Natl. Acad. Sci. USA 93:12626-12630.
14. Donovan, J. A., R. L. Wange, W. Y. Langdon, and L. E. Samelson. 1994. The protein product of the c-cbl protooncogene is the 120-kDa tyrosine-phosphorylated protein in Jurkat cells activated via the T cell antigen receptor. J. Biol. Chem. 269:22921-22924.
15. Fournel, M., D. Davidson, R. Weil, and A. Veillette. 1996. Association of tyrosine protein kinase zap-70 with the protooncogene product p120(c-cbl) in T lymphocytes. J. Exp. Med. 183:301-306.
16. Fowler, K. J., et al. 1995. A mutation in the epidermal growth factor receptor in waved-2 mice has a profound effect on receptor biochemistry that results in impaired lactation. Proc. Natl. Acad. Sci. USA 92:1465-1469.
17. Fukazawa, T., K. A. Reedquist, T. Trub, S. Soltoff, G. Panchamoorthy, B. Druker, L. Cantley, S. E. Shoelson, and H. Band. 1995. The SH3 domain-binding T cell tyrosyl phosphoprotein p120 - demonstration of its identity with the c-cbl protooncogene product and in vivo complexes with Fyn, Grb2, and phosphatidylinositol 3-kinase. J. Biol. Chem. 270:19141-19150.
18. Galisteo, M. L., I. Dikic, A. G. Batzer, W. Y. Langdon, and J. Schlessinger. 1995. Tyrosine phosphorylation of the c-Cbl proto-oncogene protein product and association with epidermal growth factor (EGF) receptor upon EGF stimulation. J. Biol. Chem. 270:20242-20245.
19. Groves, T., P. Smiley, M. P. Cooke, K. Forbush, R. M. Perlmutter, and C. J. Guidos. 1996. Fyn can partially substitute for Lck in T lymphocyte development. Immunity 5:417-428.
20. Hime, G. R., M. P. Dhungat, A. Ng, and 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 14:2709-2719.
21. Jongeward, G. D., T. R. Clandinin, and P. W. Sternberg. 1995. Sli-1, a negative regulator of let-23-mediated signaling in C. elegans. Genetics 139: 1553-1566.
22. Keane, M. M., O. M. Riverolezcano, J. A. Mitchell, K. C. Robbins, and S. Lipkowitz. 1995. Cloning and characterization of Cbl-b - a SH3 binding protein with homology to the c-Cbl proto-oncogene. Oncogene 10:2367-2377.
23. Kim, T. J., Y. T. Kim, and S. Pillai. 1995. Association of activated phosphatidylinositol 3-kinase with p120(cbl) in antigen receptor-ligated B cells. J. Biol. Chem. 270:27504-27509.
24. Kishihara, K., et al. 1993. Normal B-lymphocyte development but impaired T-cell maturation in cd45-exon6 protein tyrosine phosphatase deficient mice. Cell 74:143-156.
25. Kong, G. H., 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. 16:5026-5035.
26. Kontani, K., I. Kukimoto, H. Nishina, S. Hoshino, O. Hazeki, Y. Kanaho, and T. Katada. 1996. Tyrosine phosphorylation of the c-cbl proto-oncogene product mediated by cell surface antigen cd38 in hl-60 cells. J. Biol. Chem. 271:1534-1537.
27. Kontgen, F., R. J. Grumont, A. Strasser, D. Metcalf, R. L. Li, D. Tarlinton, and S. Gerondakis. 1995. Mice lacking the c-Rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9:1965-1977.
28. Langdon, W. Y., J. W. Hartley, S. P. Klinken, S. K. Ruscetti, and H. C. Morse. 1989. v-cbl, an oncogene from a dual-recombinant murine retrovirus that induces early B-lineage lymphomas. Proc. Natl. Acad. Sci. USA 86: 1168-1172.
29. Langdon, W. Y., C. D. Hyland, R. J. Grumont, and H. D. Morse. 1989. The c-cbl proto-oncogene is preferentially expressed in thymus and testis tissue and encodes a nuclear protein. J. Virol. 63:5420-5424.
30. 2+-stimulated activation of nuclear factor of activated T cells by a constitutively active Cbl mutant in T cells. J. Biol. Chem. 272:168-173.
31. Liu, Y. C., Y. H. Liu, C. Elly, H. Yoshida, S. Lipkowitz, and A. Altman. 1997. Serine phosphorylation of cbl induced by phorbol ester enhances its association with 14-3-3 proteins in T cells via a novel serine-rich 14-3-3-binding motif. J. Biol. Chem. 272:9979-9985.
32. Lupher, M. L., 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. 271:24063-24068.
33. Lupher, M. L., Z. Songyan, S. E. Shoeson, L. C. Cantley, and H. Band. 1997. The Cbl phosphotyrosine-binding domain selects a D(N/D)XpY motif and binds to the TyrP292 negative regulatory phosphorylation site of ZAP-70. J. Biol. Chem. 272:33140-33144.
34. Marcilla, A., O. M. Riverolezcano, A. Agarwal, and K. C. Robbins. 1995. Identification of the major tyrosine kinase substrate in signaling complexes formed after engagement of Fc gamma receptors. J. Biol. Chem. 270:9115-9120.
35. Meisner, H., A. Daga, J. Buxton, B. Fernández, 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. 17:2217-2225.
36. Oda, A., K. Ozaki, B. J. Druker, Y. Miyakawa, H. Miyazaki, M. Handa, H. Morita, H. Ohasni, and Y. Ikeda. 1996. P120(c-Cbl) is present in human blood platelets and is differentially involved in signaling by thrombopoietin and thrombin. Blood 88:1330-1338.
37. Odai, H., K. Sasaki, Y. Hanazono, H. Ueno, T. Tanaka, K. Miyagawa, K. Mitani, Y. Yazaki, and H. Hirai. 1995. c-Cbl is inducibly tyrosine-phosphorylated by epidermal growth factor stimulation in fibroblasts, and constitutively tyrosine-phosphorylated and associated with v-Src in v-Src-transformed fibroblasts. Jpn. J. Cancer Res. 86:1119-1126.
38. Ojaniemi, M., S. S. Martin, F. Dolfi, J. M. Olefsky, and K. Vuori. 1997. The proto-oncogene product p 120(Cbl) links c-Src and phosphatidylinositol 3′-kinase to the integrin signaling pathway. J. Biol. Chem. 272:3780-3787.
39. Ota, Y., L. O. Beitz, A. M. Scharenberg, J. A. Donovan, J. P. Kinet, and L. E. Samelson. 1996. Characterization of cbl tyrosine phosphorylation and a Cbl-Syk complex in rbl-2h3 cells. J. Exp. Med. 184:1713-1723.
40. Ota, Y., and L. E. Samelson. 1997. The product of the proto-oncogene c-Cbl - a negative regulator of the Syk tyrosine kinase. Science 276:418-420.
41. Panchamoorthy, G., T. Fukazawa, S. Miyake, S. Soltoff, K. Reedquist, B. Druker, S. Shoelson, L. Cantley, and H. Band. 1996. P120(Cbl) is a major substrate of tyrosine phosphorylation upon B cell antigen receptor stimulation and interacts in vivo with Fyn and Syk tyrosine kinases, Grb2 and Shc adaptors, and the p85 subunit of phosphatidylinositol 3-kinase. J. Biol. Chem. 271:3187-3194.
42. Qian, D., and A. Weiss. 1997. T cell antigen receptor signal transduction. Curr. Opin. Cell Biol. 9:205-212.
43. Racke, F. K., K. Lewandowska, S. Goueli, and A. N. Goldfarb. 1997. Sustained activation of the extracellular signal-regulated kinase/mitogen-activated protein kinase pathway is required for megakaryocyte differentiation in K562 cells. J. Biol. Chem. 272:23366-23370.
44. Rellahan, B. L., L. J. Graham, B. Stocia, K. E. DeBell, and E. Bonvini. 1997. Cbl-mediated regulation of T cell receptor-induced AP1 activation. J. Biol. Chem. 272:30806-30811.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
46. Samelson, L. Personal communication.
47. Sasaki, K., et al. 1995. Tpo/c-Mpl ligand induces tyrosine phosphorylation of multiple cellular proteins including proto-oncogene products, vav and c-Cbl, and Ras signaling molecules. Biochem. Biophys. Res. Commun. 216:338-347.
48. Savage, P. D., M. Shapiro, W. Y. Langdon, A. D. Geurts van Kessel, H. N. Seuanez, Y. Akao, C. Croce, H. D. Morse, and J. H. Kersey. 1991. Relationship of the human protooncogene CBL2 ort 11q23 to the t(4;11), t(11;22), and t(11:14) breakpoints. Cytogenet. Cell Genet. 56:112-115.
49. Schafer, A. I. 1995. Essential (primary) thrombocythemia, p. 340-345. In E. Beutler, M. A. Lichtman, B. S. Coller, and T. J. Kipps (ed.), Williams hematology. McGraw-Hill, New York, N.Y.
50. Sieh, M., A. Batzer, J. Schlessinger, and A. Weiss. 1994. GRB2 and phospholipase C-γ1 associate with a 36-to 38-kilodalton phosphotyrosine protein after T-cell receptor stimulation. Mol. Cell. Biol. 14:4435-4442.
51. Snedeker, S. M., C. F. Brown, and R. P. DiAugustine. 1991. Expression and functional properties of transforming growth factor alpha and epidermal growth factor during mouse mammary gland ductal morphogenesis. Proc. Natl. Acad. Sci. USA 88:276-280.
52. 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.
53. Tanaka, S., M. Amling, L. Neff, A. Peyman, E. Uhlmann, J. B. Levy, and R. Baron. 1996. c-Cbl is downstream of c-Src in a signalling pathway necessary for bone resorption. Nature 383:528-531.
54. Tanaka, S., L. Neff, R. Baron, and J. B. Levy. 1995. Tyrosine phosphorylation and translocation of the c-Cbl protein after activation of tyrosine kinase signaling pathways. J. Biol. Chem. 270:14347-14351.
55. Thien, C., and W. Y. Langdon. 1997. EGF receptor binding and transformation by v-chl is ablated by the introduction of a loss-of-function mutation from the Caenorhabditis elegans Sli-1 gene. Oncogene 14:2239-2249.
56. Thien, C. B. F., and W. Y. Langdon. 1997. Tyrosine kinase activity of the EGF receptor is enhanced by the expression of oncogenic 70Z-Cbl. Oncogene 15:2909-2920.
57. Tsygankov, A. Y., S. Mahajan, J. E. Fincke, and J-B. Bolen. 1996. Specific association of tyrosine-phosphorylated c-Cbl with Fyn tyrosine kinase in T cells. J. Biol. Chem. 271:27130-27137.
58. Ueno, H., K. Sasaki, K. Miyagawa, H. Honda, K. Mitani, Y. Yazaki, and H. Hirai. 1997. 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.
59. Vonderhaar, B. K. 1987. Local effects of EGF, alpha-TGF, and EGF-like growth factors on lobuloalveolar development of the mouse mammary gland in vivo. J. Cell. Physiol. 132:581-584.
60. Vonderhaar, B. K., and A. E. Greco, 1979. Lobulo-alveolar development of mouse mammary glands is regulated by thyroid hormones. Endocrinology 104:409-418.
61. Wang, D. Z.-M., V. E. Hammond, H. E. Abud, I. Bertoncello, J. W. McAvoy, and D. D. L. Bowtell. 1997. Mutation in Sos1 dominantly enhances a weak allele of the EGFR. demonstrating a requirement for Sos1 in EGFR signaling and development. Genes Dev. 11:309-320.
62. Wang, Y., Y. G. Yeung, W. Y. Langdon, and E. R. Stanley. 1996. c-Cbl is transiently tyrosine-phosphorylated, ubiquitinated, and membrane-targeted following Csf-1 stimulation of macrophages. J. Biol. Chem. 271:17-20.
63. Wange, R. L., R. Guitian, N. Isakov, J. D. Watts, R. Aebersold, and L. E. Samelson. 1995. Activating and inhibitory mutations in adjacent tyrosines in the kinase domain of Zap-70. J. Biol. Chem. 270:18730-18733.
64. Wardenburg, J. B., et al. 1996. Phosphorylation of Sip-76 by the Zap-70 protein-tyrosine kinase is required for T-cell receptor function. J. Biol. Chem. 271:19641-19644.
65. Wiest, D. L., J. M. Ashe, R. Abe, J. B. Bolen, and A. Singer. 1996. TCR activation of Zap70 is impaired in cd4(+)cd8(+) thymocytes as a consequence of intrathymic interactions that diminish available p56(lck). Immunity 4:495-504.
66. Yoon, C. H., J. H. Lee, G. D. Jongeward, and P. W. Sternberg. 1995. Similarity of Sli-1, a regulator of vulval development in C. elegans, to the mammalian proto-oncogene c-Cbl. Science 269:1102-1105.