The Cbl protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation

EMBO Journal

Volumn 18, Issue 13, 1999, Pages 3616-3628

  Lee, Pierre S W ^a   Wang, Yun ^a   Dominguez, Melissa G ^a   Yeung, Yee Guide ^a   Murphy, Maria A ^b   Bowtell, David D L ^b   Stanley, E Richard ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

Cbl; Cell proliferation; CSF 1 receptor tyrosine kinase; Endocytosis; Multiubiquitination

Indexed keywords

COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR RECEPTOR; ONCOPROTEIN;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL SURFACE; COLONY FORMATION; CONTROLLED STUDY; ENDOCYTOSIS; INTERNALIZATION; LYSOSOME; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTO ONCOGENE;

ANIMALS; CELL DIVISION; CELL SIZE; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; DOWN-REGULATION; ENDOCYTOSIS; GENE DELETION; LYSOSOMES; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; MICE, INBRED C57BL; PEPTIDE HYDROLASES; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-CBL; RAS PROTEINS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; SIGNAL TRANSDUCTION; TYROSINE; UBIQUITIN-PROTEIN LIGASES; UBIQUITINS;

ANIMALIA;

EID: 0033169024     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.13.3616     Document Type: Article

References (57)

1. Baccarini, M., Li, W., Dello Sbarba, P. and Stanley, E.R. (1991) Increased phosphorylation of the colony stimulating factor-1 receptor following transmembrane signalling. Receptor, 1, 243-259.
2. Bowtell, D.D.L. and Langdon, W.Y. (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.
3. Büscher, D., Dello Sbarba, P., Hipskind, R.A., Rapp, U.R., Stanley, E.R. and Baccarini, M. (1993) v-raf confers CSF-1 independent growth to a macrophage cell line and leads to immediate early gene expression without MAP-kinase activation. Oncogene, 8, 3323-3332.
4. Davis, J.N., Rock, C.O., Cheng, M., Watson, J.B., Ashmun, R.A., Kirk, H., Kay, R.J. and Roussel, M.F. (1997) Complementation of growth factor receptor-dependent mitogenic signalling by a truncated type I phosphatidylinositol 4-phosphate 5-kinase. Mol. Cell. Biol., 17, 7398-7406.
5. Feshchenko, E., Shore, S. and Tsygankov, A. (1998) Tyrosine phosphorylation of c-CBL facilitates adhesion and cytoskeletal rearrangements of v-Abl-transformed NIH 3T3 fibroblasts. Proceedings of the 10th International Conference on Second Messengers and Phospho-proteins, pp. 85-86.
6. Galan, J.M., Mareau, V. Andre, B., Vaolland, C. and Haguenauer-Tsapis, R. (1996) Ubiquitination mediated by the npi1p/rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem., 271, 10946-10952.
7. Galcheva-Gargova, Z., Theroux, S.J. and Davis, R.J. (1995) The epidermal growth factor receptor is covalently linked to ubiquitin. Oncogene, 11, 2649-2655.
8. Gavrieli, Y., Sherman, Y. and Ben-Sasson, S.A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol., 119, 493-501.
9. Govers, R., ten Broeke, T., Van Kerkhof, P., Schwartz, A.L. and Strous, G.J. (1999) Identification of a novel ubiquitin conjugation motif, required for ligand-induced internalization of the growth hormone receptor. EMBO J., 18, 28-36.
10. 125I-colony stimulating factor-1 with bone marrow-derived macrophages. J. Biol. Chem., 261, 4024-4032.
11. 125I-CSF-1 by peritoneal exudate macrophages. J. Cell. Biochem., 31, 203-216.
12. Hicke, L. (1997) Ubiquitin-dependent internalization and down-regulation of plasma membrane proteins. FASEB J., 11, 1215-1226.
13. Hicke, L. and Reizman, H. (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell, 84, 277-287.
14. Hime, G.R., Dhungat, M.P., Ng, A. and Bowtell, D.D.L. (1997) D-Cbl, the Drosophila homologue of the c-Cbl protooncogene, interacts with the Drosophila EGF receptor in vivo, despite lacking C-terminal adaptor binding sites. Oncogene, 14, 2709-2719.
15. Hofmann, K. and Bucher, P. (1996) The UBA domain: a sequence motif present in multiple enzyme classes of ubiquitination pathway. Trends Biochem. Sci., 21, 172-173.
16. Husson, H., Mograbi, B., Schmid-Antomarchi, H., Fischer, S. and Rossi, B. (1997) CSF-1 stimulation induces the formation of a multiprotein complex including CSF-1 receptor, c-Cbl, PI 3-kinase, Crk-II and Grb2. Oncogene, 14, 2331-2338.
17. Jeffers, M., Taylor, G.A., Weidner, K.M., Omura, S. and Van de Woude, G.F. (1997) Degradation of the Met tyrosine kinase receptor by the ubiquitin-proteasome pathway. Mol. Cell. Biol., 17, 799-808.
18. Jongeward, G.D., Clandinin, T.R. and Sternberg, P.W. (1995) sli-1, a negative regulator of let-23-mediated signalling in C.elegans. Genetics, 139, 1553-1566.
19. Kanagasundaram, V., Jaworowski, A. and Hamilton, J.A. (1996) Association between phosphatidylinositol-3 kinase, Cbl and other tyrosine phosphorylated proteins in colony-stimulating factor-1-stimulated macrophages. Biochem. J., 320, 69-77.
20. Keane, M.M., Rivero-Lezcano, O.M., Mitchell, J.A., Robbins, K.C. and Lipkowitz, S. (1995) Cloning and characterization of cbl-b: a SH3 binding protein with homology to the c-cbl protooncogene. Oncogene, 10, 2367-2377.
21. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
22. Langdon, W.Y., Hartley, J.W., Klinken, S.P. Ruscetti, S.K. and Morse, H.C., III (1989a) v-cbl, an oncogene from a dual-recombinant marine retrovirus that induces early B-lineage lymphomas. Proc. Natl Acad. Sci. USA, 86, 1168-1172.
23. Langdon, W.Y., Hyland, C.D., Grumont, R.J. and Morse, H.C., III (1989b) The c-cbl protooncogene is preferentially expressed in thymus and testis tissue and encodes a nuclear protein. J. Virol., 63, 5420-5424.
24. Lee, J., Jongeward, G.D. and Sternberg, P.W. (1994) unc-101, a gene required for many aspects of Caenorhabditis elegans development and behavior, encodes a clathrin-associated protein. Genes Dev., 8, 60-73.
25. Levkowitz, G., Waterman, H., Zamir, E., Kam, Z., Oved, S., Langdon, W.Y., Beguinot, L., Geigr, B. and Yarden, Y. (1998) c-Cbl/Sli-1 regulates endocytic sorting and Ubiquitination of the epidermal growth factor receptor. Genes Dev., 12, 3663-3674.
26. Li, W. and Stanley, E.R. (1991) Role of dimerization and modification of the CSF-1 receptor in its activation and internalization during the CSF-1 response. EMBO J., 10, 277-288.
27. Li, W., Yeung, Y.-G. and Stanley, E.R. (1991) Tyrosine phosphorylation of a common 57-kDa protein in growth factor-stimulated and -transformed cells. J. Biol. Chem., 266, 6808-6814.
28. ras activity. Trends Genet., 7, 346-351.
29. Meisner, H., Daga, A., Buxton, J., Fernandez, B., Chawla, A., Banerjee, U. and Czech, M.P. (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.
30. 1 integrin signalling pathway involving Src-family kinases, Cbl and PI-3 kinase is required for macrophage spreading and migration. EMBO J., 17, 4391-4403.
31. Miyake, S., Lupher, M.L., Jr, Andoniou, C.E., Lill, N.L., Ota, S., Douillard, P., Rao, N. and Band, H. (1997) The Cbl protoncogene product: from an enigmatic oncogene to center stage of signal transduction. Crit. Rev. Oncogenet., 8, 189-218.
32. Miyake, S., Lupher, M.L., Druker, B. and Band, H. (1998) The tyrosine kinase regulator Cbl enhances the ubiquitination and degradation of the platelet-derived growth factor α. Proc. Natl Acad. Sci. USA, 95, 7927-7932.
33. Mori, S., Claesson-Welsh, L., Okuyama, Y. and Saito, Y. (1995a) Ligand-induced polyubiquitination of receptor tyrosine kinases. Biochem. Biophys. Res. Commun., 213, 32-39.
34. Mori, S., Tanaka, K., Omura, S. and Saito, Y. (1995b) Degradation process of ligand-stimulated platelet-derived growth factor β-receptor involves ubiquitin-proteasome proteolytic pathway. J. Biol. Chem., 270, 29447-29452.
35. Murphy, M.A., Schnall, R.G., Venter, D.J., Barnett, L., Bertoncello, I., Thien, C.B.F., Langdon, W.Y. and Bowtell, D.D.L. (1998) Tissue hyperplasia and enhanced T-cell signalling via ZAP-70 in c-Cbl-deficient mice. Mol. Cell. Biol., 18, 4872-4882.
36. Ota, Y. and Samelson, L.E. (1997) The product of the protooncogene c-cbl: a negative regulator of the Syk tyrosine kinase. Science, 276, 418-420.
37. Ribon, V., Herrera, R. and Kay, B.K. (1998) A role for CAP, a novel, multifunctional src homology 3 domain-containing protein in formation of actin stress fibers and focal adhesions. J. Biol. Chem., 273, 4073-4080.
38. Roth, A.F. and Davis, N.G. (1996) Ubiquitination of the yeast α-factor receptor. J. Cell Biol., 134, 661-674.
39. Sengupta, A., Liu, W.-K., Yeung, Y.-G., Yeung, D.C.-Y., Frackelton, A.R. and Stanley, E.R. (1988) Identification and subcellular localization of proteins that are rapidly phosphorylated in tyrosine in response to colony stimulating factor 1. Proc. Natl Acad. Sci. USA, 85, 8062-8066.
40. Smit, L. and Borst, J. (1997) The Cbl family of signal transduction molecules. Crit. Rev. Oncogenet., 8, 359-379.
41. Stanley, E.R. (1979) Colony-stimulating factor (CSF) radioimmunoassay: detection of a CSF subclass stimulating macrophage production. Proc. Natl Acad. Sci. USA, 76, 2969-2973.
42. Stanley, E.R. (1985) The macrophage colony-stimulating factor, CSF-1. Methods Enzymol., 116, 564-587.
43. Stanley, E.R. (1990) Murine bone marrow-derived macrophages. In Pollard, J.W. and Walker, J.M. (eds), Methods in Molecular Biology. Humana Press, Clifton, NJ, pp. 299-302.
44. Stanley, E.R. (1998) Macrophage colony stimulating factor (CSF-1). In Delves, P.J. and Roitt, I.M. (eds), Encyclopedia of Immunology. Academic Press, Orlando, FL, pp. 1650-1654.
45. Stanley, E.R. and Guilbert, L.J. (1981) Methods for the purification, assay, characterization and target cell binding of a colony stimulating factor (CSF-1). J. Immunol. Methods, 42, 253-284.
46. Strous, G.J., vanKerkhof, P., Govers, R., Ciechanover, A. and Schwartz, A.L. (1996) The ubiquitin conjugation system is required for ligand-induced endocytosis and degradation of the growth hormone receptor. EMBO J., 15, 3806-3812.
47. Tushinski, R.J., Oliver, I.T., Guilbert, L.J., Tynan, P.W., Warner, J.R. and Stanley, E.R. (1982) Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell, 28, 71-81.
48. Ueno, H., Sasaki, K., Miyagawa, K., Honda, H., Mitani, K., Yazaki, Y. and Hirai, H. (1997) Antisense repression of protooncogene c-Cbl enhances activation of the JAK-STAT pathway but not the Ras pathway in epidermal growth factor receptor signalling. J. Biol. Chem., 272, 8739-8743.
49. Van der Geer, P. and Hunter, T. (1990) Identification of tyrosine 706 in the kinase insert as the major colony-stimulating factor 1 (CSF-1)-stimulated autophosphorylation site in the CSF-1 receptor in a murine macrophage cell line. Mol. Cell. Biol., 10, 2991-3002.
50. Vieira, A.V., Lamaze, C. and Schmid, S.L. (1996) Control of EGF receptor signalling by clathrin-mediated endocytosis. Science, 274, 2086-2089.
51. Wang, Y., Yeung, Y-G., Langdon, W.Y. and Stanley, E.R. (1996) The c-cbl protooncogene product is transiently tyrosine phosphorylated, ubiquitinated and membrane targeted following CSF-1 stimulation of macrophages. J. Biol. Chem., 271, 17-20.
52. Wang, Y., Yeung, Y.-G. and Stanley, E.R. (1999) CSF-1 stimulated multiubiquitination of the CSF-1 receptor and of Cbl follows their tyrosine phosphorylation and association with other signalling proteins. J. Cell. Biochem., 72, 119-134.
53. Xu, X.-X., Tessner, T.G., Rock, C.O. and Jackowski, S. (1993) Phosphatidylcholine hydrolysis and c-myc expression are in collaborating mitogenic pathways activated by colony-stimulating factor 1. Mol. Cell. Biol., 13, 1522-1533.
54. Yeung, Y.-G., Jubinsky, P.T., Sengupta, A., Yeung, D.C.-Y. and Stanley, E.R. (1987) Purification of the colony-stimulating factor 1 receptor and demonstration of its tyrosine kinase activity. Proc. Natl Acad. Sci. USA, 84, 1268-1271.
55. Yeung, Y.-G., Berg, K.L., Pixley, F.J., Angeletti, R.H. and Stanley, E.R. (1992) Protein tyrosine phosphatase-1C is rapidly phosphorylated in tyrosine in macrophages in response to colony stimulating factor-1. J. Biol. Chem., 267, 23447-23450.
56. Yoon, C.H., Lee, J., Jongeward, G.D. and Sternberg, P.W. (1995) Similarity of sli-1, a regulator of vulval development in C.elegans, to the mammalian protooncogene c-cbl. Science, 269, 1102-1105.
57. Zell, T., Warden, C.S., Chan, A.S.H., Cook, M.E., Dell, C.L., Hunt, S.W., III and Shimizu, Y. (1998) Regulation of β1-integrin-mediated cell adhesion by the Cbl adaptor protein. Curr. Biol., 8, 814-822.