The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor

Molecular and Cellular Biology

Volumn 23, Issue 9, 2003, Pages 3363-3372

  Vecchione, Andrea ^a,b   Marchese, Adriano ^a   Henry, Pauline ^c   Rotin, Daniela ^c   Morrione, Andrea ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b Parco Sci Biomed di R S Raffaele   (Italy)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CHLOROQUINE; DANSYLCADAVERINE; GROWTH FACTOR RECEPTOR BOUND PROTEIN 10; LIGAND; PROTEASOME; PROTEIN TYROSINE KINASE; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENDOSOME; FIBROBLAST; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HALF LIFE TIME; IMMUNOPRECIPITATION; LYSOSOME; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; REGULATORY MECHANISM;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL MEMBRANE; CELLS, CULTURED; CHLOROQUINE; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; FIBROBLASTS; GENE EXPRESSION; GRB10 ADAPTOR PROTEIN; INSULIN-LIKE GROWTH FACTOR I; LEUPEPTINS; LIGANDS; LIGASES; LYSOSOMES; MACROMOLECULAR SUBSTANCES; MICE; MULTIENZYME COMPLEXES; MUTATION; PRECIPITIN TESTS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEINS; RECEPTOR, IGF TYPE 1; RECOMBINANT PROTEINS; SRC HOMOLOGY DOMAINS; TRANSPORT VESICLES; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; INVERTEBRATA; PROTOZOA;

EID: 0345381737     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.9.3363-3372.2003     Document Type: Article

References (63)

1. + channel by Nedd4 in Liddle's syndrome. J. Clin. Investig. 103:667-673.
2. Aviel, S., G. Winberg, M. Massucci, and A. Ciechanover. 2000. Degradation of the Epstein-Barr virus latent membrane protein 1 (LMP1) by the ubiquitin-proteasome pathway. Targeting via ubiquitination of the N-terminal residue. J. Biol. Chem. 275:23491-23499.
3. Bai, R. Y., T. Jahn, S. Schrem, G. Munzert, K. M. Weidner, J. Y. Wang, and J. Duyster. 1998. The SH2-containing adapter protein GRB10 interacts with BCR-ABL. Oncogene 17:941-948.
4. Beaudenon, S. L., M. R. Huacani, G. Wang, D. P. McDonnell, and J. M. Huibregtse. 1999. Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:6972-6979.
5. Bereziat, V., A. Kasus-Jacobi, D. Perdereau, B. Cariou, J. Girard, and A. F. Burnol. 2002. Inhibition of insulin receptor catalytic activity by the molecular adapter Grb14. J. Biol. Chem. 277:4845-4852.
6. Bork, P., and M. Sudol. 1994. The WW domain: a signalling site in dystrophin? Trends Biochem. Sci. 19:531-533.
7. Chow, J. C., G. Condorelli, and R. J. Smith. 1998. Insulin-like growth factor-I receptor internalization regulates signaling via the Shc/mitogen-activated protein kinase pathway, but not the insulin receptor substrate-1 pathway. J. Biol. Chem. 273:4672-4680.
8. Dey, B. R., K. Frick, W. Lopaczynski, S. P. Nissley, and R. W. Furlanetto. 1996. Evidence for the direct interaction of the insulin-like growth factor I receptor with IRS-1, Shc, and Grb10. Mol. Endocrinol. 10:631-641.
9. Di Fiore, P. P., and P. De Camilli. 2001. Endocytosis and signaling, an inseparable partnership. Cell 106:1-4.
10. Dong, L. Q., H. Du, S. G. Porter, L. F. Kolakowski, Jr., A. V. Lee, L. J. Mandarino, J. Fan, D. Yee, F. Liu, and J. Mandarino. 1997. Cloning, chromosome localization, expression, and characterization of an Src homology 2 and pleckstrin homology domain-containing insulin receptor binding protein hGrb10gamma. J. Biol. Chem. 272:29104-29112.
11. Dong, L. Q., S. Farris, J. Christal, and F. Liu. 1997. Site-directed mutagenesis and yeast two-hybrid studies of the insulin and insulin-like growth factor-1 receptors: the Src homology-2 domain-containing protein hGrb10 binds to the autophosphorylated tyrosine residues in the kinase domain of the insulin receptor. Mol. Endocrinol. 11:1757-1765.
12. Frantz, J. D., S. Giorgetti-Peraldi, E. A. Ottinger, and S. E. Shoelson. 1997. Human GRB-IRβ/GRB10. Splice variants of an insulin and growth factor receptor-binding protein with PH and SH2 domains. J. Biol. Chem. 272:2659-2667.
13. + channel by interaction of Nedd4 with a PY motif deleted in Liddle's syndrome. J. Biol. Chem. 273:30012-30017.
14. Hansen, H., U. Svensson, J. Zhu, L. Laviola, F. Giorgino, G. Wolf, R. J. Smith, and H. Riedel. 1996. Interaction between the Grb10 SH2 domain and the insulin receptor carboxyl terminus. J. Biol. Chem. 271:8882-8886.
15. He, W., D. W. Rose, J. M. Olefsky, and T. A. Gustafson. 1998. Grb10 interacts differentially with the insulin receptor, insulin-like growth factor I receptor, and epidermal growth factor receptor via the Grb10 Src homology 2 (SH2) domain and a second novel domain located between the pleckstrin homology and SH2 domains. J. Biol. Chem. 273:6860-6867.
16. Helliwell, S. B., S. Losko, and C. A. Kaiser. 2001. Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease. J. Cell Biol. 153:649-662.
17. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
18. Hicke, L. 2001. A new ticket for entry into budding vesicles - ubiquitin. Cell 106:527-530.
19. Huibregtse, J. M., M. Scheffner, S. Beaudenon, and P. M. Howley. 1995. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 92:5249.
20. Jahn, T., P. Seipel, S. Urschel, C. Peschel, and J. Duyster. 2002. Role for the adaptor protein Grb10 in the activation of Akt. Mol. Cell. Biol. 22:979-991.
21. Jeffers, M., G. A. Taylor, K. M. Weidner, S. Omura, and G. F. Vande Woude. 1997. Degradation of the Met tyrosine kinase receptor by the ubiquitin-proteasome pathway. Mol. Cell. Biol. 17:799-808.
22. + channel. FASEB J. 15:204-214.
23. Kanelis, V., D. Rotin, and J. D. Forman-Kay. 2001. Solution structure of a Nedd4 WW domain-ENaC peptide complex. Nat. Struct. Biol. 8:407-412.
24. Kikonyogo, A., F. Bouamr, M. L. Vana, Y. Xiang, A. Aiyar, C. Carter, and J. Leis. 2001. Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc. Natl. Acad. Sci. USA 98:11199-11204.
25. Kumar, S., Y. Tomooka, and M. Noda. 1992. Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem. Biophys. Res. Commun. 185:1155-1161.
26. Laviola, L., F. Giorgino, J. C. Chow, J. A. Baquero, H. Hansen, J. Ooi, J. Zhu, H. Riedel, and R. J. Smith. 1997. The adapter protein Grb10 associates preferentially with the insulin receptor as compared with the IGF-I receptor in mouse fibroblasts. J. Clin. Investig. 99:830-837.
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. 18:3616-3628.
28. 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.
29. Liu, F., and R. A. Roth. 1995. Grb-IR: a SH2-domain-containing protein that binds to the insulin receptor and inhibits its function. Proc. Natl. Acad. Sci. USA 92:10287-10291.
30. Lyons, R. J., R. Deane, D. K. Lynch, Z. S. Ye, G. M. Sanderson, H. J. Eyre, G. R. Sutherland, and R. J. Daly. 2001. Identification of a novel human tankyrase through its interaction with the adaptor protein Grb14. J. Biol. Chem. 276:17172-17180.
31. Miyake, S., M. L. Lupher, Jr., B. Druker, and H. Band. 1998. 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.
32. 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. 274:16619-16628.
33. Miyoshi, N., Y. Kuroiwa, T. Kohda, H. Shitara, H. Yonekawa, T. Kawabe, H. Hasegawa, S. C. Barton, M. A. Surani, T. Kaneko-Ishino, and F. Ishino. 1998. Identification of the Meg1/Grb10 imprinted gene on mouse proximal chromosome 11, a candidate for the Silver-Russell syndrome gene. Proc. Natl. Acad. Sci. USA 95:1102-1107.
34. Mori, S., K. Tanaka, S. Omura, and Y. Saito. 1995. Degradation process of ligand-stimulated platelet-derived growth factor beta-receptor involves ubiquitin-proteasome proteolytic pathway. J. Biol. Chem. 270:29447-29452.
35. Morrione, A. 2000. Grb10 proteins in insulin-like growth factor and insulin receptor signaling. Int. J. Mol. Med. 5:151-154.
36. Morrione, A., P. Plant, B. Valentinis, O. Staub, S. Kumar, D. Rotin, and R. Baserga. 1999. mGrb10 interacts with Nedd4. J. Biol. Chem. 274:24094-24099.
37. Morrione, A., B. Valentinis, S. Li, J. Y. Ooi, B. Margolis, and R. Baserga. 1996. Grb10: a new substrate of the insulin-like growth factor I receptor. Cancer Res. 56:3165-3167.
38. Morrione, A., B. Valentinis, M. Resnicoff, S. Xu, and R. Baserga. 1997. The role of mGrb10α in insulin-like growth factor I-mediated growth. J. Biol. Chem. 272:26382-26387.
39. Moutoussamy, S., F. Renaudie, F. Lago, P. A. Kelly, and J. Finidori. 1998. Grb10 identified as a potential regulator of growth hormone (GH) signaling by cloning of GH receptor target proteins. J. Biol. Chem. 273:15906-15912.
40. Myat, A., P. Henry, V. McCabe, L. Flintoft, D. Rotin, and G. Tear. 2002. Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron 35:447-459.
41. Nantel, A., K. Mohammad-Ali, J. Sherk, B. I. Posner, and D. Y. Thomas. 1998. Interaction of the Grb10 adapter protein with the Raf1 and MEK1 kinases. J. Biol. Chem. 273:10475-10484.
42. Nawaz, Z., D. M. Lonard, A. P. Dennis, C. L. Smith, and B. W. O'Malley. 1999. Proteasome-dependent degradation of the human estrogen receptor. Proc. Natl. Acad. Sci. USA 96:1858-1862.
43. O'Neill, T. J., D. W. Rose, T. S. Pillay, K. Hotta, J. M. Olefsky, and T. A. Gustafson. 1996. Interaction of a GRB-IR splice variant (a human GRB10 homolog) with the insulin and insulin-like growth factor I receptors. Evidence for a role in mitogenic signaling. J. Biol. Chem. 271:22506-22513.
44. Ooi, J., V. Yajnik, D. Immanuel, M. Gordon, J. J. Moskow, A. M. Buchberg, and B. Margolis. 1995. The cloning of Grb10 reveals a new family of SH2 domain proteins. Oncogene 10:1621-1630.
45. Orsini, M. J., J. L. Parent, S. J. Mundell, A. Marchese, and J. L. Benovic. 1999. Trafficking of the HIV coreceptor CXCR4. Role of arrestins and identification of residues in the c-terminal tail that mediate receptor internalization. J. Biol. Chem. 274:31076-31086.
46. Pham, N., I. Cheglakov, C. A. Koch, C. L. de Hoog, M. F. Moran, and D. Rotin. 2000. The guanine nucleotide exchange factor CNrasGEF activates ras in response to cAMP and cGMP. Curr. Biol. 10:555-558.
47. Pham, N., and D. Rotin. 2001. Nedd4 regulates ubiquitination and stability of the guanine-nucleotide exchange factor CNrasGEF. J. Biol. Chem. 276:46995-47003.
48. Plant, P. J., F. Lafont, S. Lecat, P. Verkade, K. Simons, and D. Rotin. 2000. Apical membrane targeting of Nedd4 is mediated by an association of its C2 domain with annexin XIIIb. J. Cell Biol. 149:1473-1484.
49. 2+-dependent plasma membrane localization. J. Biol. Chem. 272:32329-32336.
50. Reiss, K., B. Valentinis, X. Tu, S. Q. Xu, and R. Baserga. 1998. Molecular markers of IGF-I-mediated mitogenesis. Exp. Cell Res. 242:361-372.
51. Rotin, D., O. Staub, and R. Haguenauer-Tsapis. 2000. Ubiquitination and endocytosis of plasma membrane proteins: role of Nedd4/Rsp5p family of ubiquitin-protein ligases. J. Membr. Biol. 176:1-17.
52. Sepp-Lorenzino, L., Z. Ma, D. E. Lebwohl, A. Vinitsky, and N. Rosen. 1995. Herbimycin A induces the 20 S proteasome- and ubiquitin-dependent degradation of receptor tyrosine kinases. J. Biol. Chem. 270:16580-16587.
53. Staub, O., S. Dho, P. Henry, J. Correa, T. Ishikawa, J. McGlade, and D. Rotin. 1996. WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle's syndrome. EMBO J. 15:2371-2380.
54. Staub, O., I. Gautschi, T. Ishikawa, K. Breitschopf, A. Ciechanover, L. Schild, and D. Rotin. 1997. Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J. 16:6325-6336.
55. Stein, E., D. P. Cerretti, and T. O. Daniel. 1996. Ligand activation of ELK receptor tyrosine kinase promotes its association with Grb10 and Grb2 in vascular endothelial cells. J. Biol. Chem. 271:23588-23593.
56. Stein, E. G., T. A. Gustafson, and S. R. Hubbard. 2001. The BPS domain of Grb10 inhibits the catalytic activity of the insulin and IGF1 receptors. FEBS Lett. 493:106-111.
57. Treier, M., L. M. Staszewski, and D. Bohmann. 1994. Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78:787-798.
58. Valentinis, B., P. L. Porcu, K. Quinn, and R. Baserga. 1994. The role of the insulin-like growth factor I receptor in the transformation by simian virus 40 T antigen. Oncogene 9:825-831.
59. van Kerkhof, P., R. Govers, C. M. Alves dos Santos, and G. J. Strous. 2000. Endocytosis and degradation of the growth hormone receptor are proteasome-dependent. J. Biol. Chem. 275:1575-1580.
60. Vojtek, A. B., S. M. Hollenberg, and J. A. Cooper. 1993. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74:205-214.
61. Wang, H. Y., Y. Altman, D. Fang, C. Elly, Y. Dai, Y. Shao, and Y. C. Liu. 2001. Cbl promotes ubiquitination of the T cell receptor zeta through an adaptor function of Zap-70. J. Biol. Chem. 276:26004-26011.
62. Wang, J., H. Dai, N. Yousaf, M. Moussaif, Y. Deng, A. Boufelliga, O. R. Swamy, M. E. Leone, and H. Riedel. 1999. Grb10, a positive, stimulatory signaling adapter in platelet-derived growth factor BB-, insulin-like growth factor I-, and insulin-mediated mitogenesis. Mol. Cell. Biol. 19:6217-6228.
63. 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.