36
Views
63
CrossRef citations to date
0
Altmetric
Article

A Tale of Two Cbls: Interplay of c-Cbl and Cbl-b in Epidermal Growth Factor Receptor Downregulation

&
Pages 3020-3037 | Received 03 Oct 2007, Accepted 22 Feb 2008, Published online: 27 Mar 2023

REFERENCES

  • Bao, J., G. Gur, and Y. Yarden. 2003. Src promotes destruction of c-Cbl: implications for oncogenic synergy between Src and growth factor receptors. Proc. Natl. Acad. Sci. USA 100:2438–2443.
  • Bowtell, D. 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.
  • Buday, L., A. Khwaja, S. Sipeki, A. Farago, and J. Downward. 1996. Interactions of Cbl with two adapter proteins, Grb2 and Crk, upon T cell activation. J. Biol. Chem. 271:6159–6163.
  • Burgering, B. M., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376:599–602.
  • Carpenter, G. 1987. Receptors for epidermal growth factor and other polypeptide mitogens. Annu. Rev. Biochem. 56:881–914.
  • Davies, G. C., S. A. Ettenberg, A. O. Coats, M. Mussante, S. Ravichandran, J. Collins, M. M. Nau, and S. Lipkowitz. 2004. Cbl-b interacts with ubiquitinated proteins; differential functions of the UBA domains of c-Cbl and Cbl-b. Oncogene 23:7104–7115.
  • de Melker, A. A., G. van der Horst, J. Calafat, H. Jansen, and J. Borst. 2001. c-Cbl ubiquitinates the EGF receptor at the plasma membrane and remains receptor associated throughout the endocytic route. J. Cell Sci. 114:2167–2178.
  • de Melker, A. A., G. van der Horst, and J. Borst. 2004. Ubiquitin ligase activity of c-Cbl guides the epidermal growth factor receptor into clathrin-coated pits by two distinct modes of Eps15 recruitment. J. Biol. Chem. 279:55465–55473.
  • Duan, L., Y. Miura, M. Dimri, B. Majumder, I. L. Dodge, A. L. Reddi, A. Ghosh, N. Fernandes, P. Zhou, K. Mullane-Robinson, N. Rao, S. Donoghue, R. A. Rogers, D. Bowtell, M. Naramura, H. Gu, V. Band, and H. Band. 2003. Cbl-mediated ubiquitinylation is required for lysosomal sorting of epidermal growth factor receptor but is dispensable for endocytosis. J. Biol. Chem. 278:28950–28960.
  • Ettenberg, S. A., Y. R. Rubinstein, P. Banerjee, M. M. Nau, M. M. Keane, and S. Lipkowitz. 1999. cbl-b inhibits EGF-receptor-induced apoptosis by enhancing ubiquitination and degradation of activated receptors. Mol. Cell Biol. Res. Commun. 2:111–118.
  • Ettenberg, S. A., A. Magnifico, M. Cuello, M. M. Nau, Y. R. Rubinstein, Y. Yarden, A. M. Weissman, and S. Lipkowitz. 2001. Cbl-b-dependent coordinated degradation of the epidermal growth factor receptor signaling complex. J. Biol. Chem. 276:27677–27684.
  • Ettenberg, S. A., M. M. Keane, M. M. Nau, M. Frankel, L. M. Wang, J. H. Pierce, and S. Lipkowitz. 1999. cbl-b inhibits epidermal growth factor receptor signaling. Oncogene 18:1855–1866.
  • Feng, Q., D. Baird, X. Peng, J. Wang, T. Ly, J. L. Guan, and R. A. Cerione. 2006. Cool-1 functions as an essential regulatory node for EGF receptor- and Src-mediated cell growth. Nat. Cell Biol. 8:945–956.
  • 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. 271:14554–14559.
  • 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.
  • Grovdal, L. M., E. Stang, A. Sorkin, and I. H. Madshus. 2004. Direct interaction of Cbl with pTyr 1045 of the EGF receptor (EGFR) is required to sort the EGFR to lysosomes for degradation. Exp. Cell Res. 300:388–395.
  • Haglund, K., P. P. Di Fiore, and I. Dikic. 2003. Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem. Sci. 28:598–603.
  • Haglund, K., S. Sigismund, S. Polo, I. Szymkiewicz, P. P. Di Fiore, and I. Dikic. 2003. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5:461–466.
  • Haglund, K., N. Shimokawa, I. Szymkiewicz, and I. Dikic. 2002. Cbl-directed monoubiquitination of CIN85 is involved in regulation of ligand-induced degradation of EGF receptors. Proc. Natl. Acad. Sci. USA 99:12191–12196.
  • Hicke, L., and H. Riezman. 1996. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84:277–287.
  • Huang, F., and A. Sorkin. 2005. Growth factor receptor binding protein 2-mediated recruitment of the RING domain of Cbl to the epidermal growth factor receptor is essential and sufficient to support receptor endocytosis. Mol. Biol. Cell 16:1268–1281.
  • Jiang, X., F. Huang, A. Marusyk, and A. Sorkin. 2003. Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol. Biol. Cell 14:858–870.
  • Joazeiro, C. A., S. S. Wing, H. Huang, J. D. Leverson, T. Hunter, and Y. C. Liu. 1999. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 286:309–312.
  • Kassenbrock, C. K., S. Hunter, P. Garl, G. L. Johnson, and S. M. Anderson. 2002. Inhibition of Src family kinases blocks epidermal growth factor (EGF)-induced activation of Akt, phosphorylation of c-Cbl, and ubiquitination of the EGF receptor. J. Biol. Chem. 277:24967–24975.
  • 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 protein. Oncogene 18:3365–3375.
  • Keane, M. M., O. M. Rivero-Lezcano, 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.
  • Levkowitz, G., H. Waterman, S. A. Ettenberg, M. Katz, A. Y. Tsygankov, I. Alroy, S. Lavi, K. Iwai, Y. Reiss, A. Ciechanover, S. Lipkowitz, and Y. Yarden. 1999. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4:1029–1040.
  • Levkowitz, G., H. Waterman, E. Zamir, Z. Kam, S. Oved, W. Y. Langdon, L. Beguinot, B. Geiger, and Y. Yarden. 1998. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12:3663–3674.
  • Lill, N. L., P. Douillard, R. A. Awwad, S. Ota, M. L. Lupher, Jr., S. Miyake, N. Meissner-Lula, V. W. Hsu, and H. Band. 2000. The evolutionarily conserved N-terminal region of Cbl is sufficient to enhance down-regulation of the epidermal growth factor receptor. J. Biol. Chem. 275:367–377.
  • Longva, K. E., F. D. Blystad, E. Stang, A. M. Larsen, L. E. Johannessen, and I. H. Madshus. 2002. Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J. Cell Biol. 156:843–854.
  • 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. 271:24063–24068.
  • Reference deleted.
  • Marmor, M. D., and Y. Yarden. 2004. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23:2057–2070.
  • Marshall, C. J. 1996. Cell signalling. Raf gets it together. Nature 383:127–128.
  • Miyake, S., M. L. Lupher, Jr., B. Druker, and H. Band. 1988. The tyrosine kinase regulator Cbl enhances the ubiquitination and degradation of the platelet-derived growth factor receptor alpha. Proc. Natl. Acad. Sci. USA 95:7927–7932.
  • Mizuno, E., T. Iura, A. Mukai, T. Yoshimori, N. Kitamura, and M. Komada. 2005. Regulation of epidermal growth factor receptor down-regulation by UBPY-mediated deubiquitination at endosomes. Mol. Biol. Cell 16:5163–5174.
  • Mosesson, Y., K. Shtiegman, M. Katz, Y. Zwang, G. Vereb, J. Szollosi, and Y. Yarden. 2003. Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J. Biol. Chem. 278:21323–21326.
  • Opresko, L. K., C. P. Chang, B. H. Will, P. M. Burke, G. N. Gill, and H. S. Wiley. 1995. Endocytosis and lysosomal targeting of epidermal growth factor receptors are mediated by distinct sequences independent of the tyrosine kinase domain. J. Biol. Chem. 270:4325–4333.
  • 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.
  • Peles, E., and Y. Yarden. 1993. Neu and its ligands: from an oncogene to neural factors. Bioessays 15:815–824.
  • Petrelli, A., G. F. Gilestro, S. Lanzardo, P. M. Comoglio, N. Migone, and S. Giordano. 2002. The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature 416:187–190.
  • Ravid, T., J. M. Heidinger, P. Gee, E. M. Khan, and T. Goldkorn. 2004. c-Cbl-mediated ubiquitinylation is required for epidermal growth factor receptor exit from the early endosomes. J. Biol. Chem. 279:37153–37162.
  • Schlessinger, J., and A. Ullrich. 1992. Growth factor signaling by receptor tyrosine kinases. Neuron 9:383–391.
  • Soubeyran, P., K. Kowanetz, I. Szymkiewicz, W. Y. Langdon, and I. Dikic. 2002. Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 416:183-187. (Erratum, 417:102.)
  • Stang, E., F. D. Blystad, M. Kazazic, V. Bertelsen, T. Brodahl, C. Raiborg, H. Stenmark, and I. H. Madshus. 2004. Cbl-dependent ubiquitination is required for progression of EGF receptors into clathrin-coated pits. Mol. Biol. Cell 15:3591–3604.
  • Stang, E., L. E. Johannessen, S. L. Knardal, and I. H. Madshus. 2000. Polyubiquitination of the epidermal growth factor receptor occurs at the plasma membrane upon ligand-induced activation. J. Biol. Chem. 275:13940–13947.
  • Szymkiewicz, I., K. Kowanetz, P. Soubeyran, A. Dinarina, S. Lipkowitz, and I. Dikic. 2002. CIN85 participates in Cbl-b-mediated down-regulation of receptor tyrosine kinases. J. Biol. Chem. 277:39666–39672.
  • 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.
  • Thien, C. B., F. Walker, and W. Y. Langdon. 2001. RING finger mutations that abolish c-Cbl-directed polyubiquitination and downregulation of the EGF receptor are insufficient for cell transformation. Mol. Cell 7:355–365.
  • Thien, C. B., and W. Y. Langdon. 2001. Cbl: many adaptations to regulate protein tyrosine kinases. Nat. Rev. Mol. Cell Biol. 2:294–307.
  • Wang, Q., G. Villeneuve, and Z. Wang. 2005. Control of epidermal growth factor receptor endocytosis by receptor dimerization, rather than receptor kinase activation. EMBO Rep. 6:942–948.
  • Wang, Q., F. Zhu, and Z. Wang. 2007. Identification of EGF receptor C-terminal sequences 1005-1017 and di-leucine motif (1010)LL(1011) as essential in EGF receptor endocytosis. Exp. Cell Res. 313:3349–3363.
  • Wang, Y., S. Pennock, X. Chen, and Z. Wang. 2002. Endosomal signaling of epidermal growth factor receptor stimulates signal transduction pathways leading to cell survival. Mol. Cell. Biol. 22:7279–7290.
  • 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.
  • Waterman, H., G. Levkowitz, I. Alroy, and Y. Yarden. 1999. The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor. J. Biol. Chem. 274:22151–22154.
  • Wu, W. J., S. Tu, and R. A. Cerione. 2003. Activated Cdc42 sequesters c-Cbl and prevents EGF receptor degradation. Cell 114:715–725.
  • Yokouchi, M., T. Kondo, A. Houghton, M. Bartkiewicz, W. C. Horne, H. Zhang, A. Yoshimura, and R. Baron. 1999. 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.
  • 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 proto-oncogene c-cbl. Science 269:1102–1105.
  • Zheng, N., P. Wang, P. D. Jeffrey, and N. P. Pavletich. 2000. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 102:533–539.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.