Negative regulation of receptor tyrosine kinases: Unexpected links to c-Cbl and receptor ubiquitylation

Cell Research

Volumn 15, Issue 1, 2005, Pages 66-71

  Rubin, Chanan ^a   Gur, Gal ^a   Yarden, Yosef ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Endocytosis; Growth factor; Oncogene; Signal transduction; Tyrosine kinase; Ubiquitin

Indexed keywords

CBL PROTEIN; GROWTH PROMOTOR; LRIG1 PROTEIN, HUMAN; MEMBRANE PROTEIN; ONCOPROTEIN; PROTEIN TYROSINE KINASE; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ANIMAL; BIOLOGICAL MODEL; DOWN REGULATION; ENDOCYTOSIS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HUMAN; METABOLISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; DOWN-REGULATION; ENDOCYTOSIS; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GROWTH SUBSTANCES; HUMANS; MEMBRANE GLYCOPROTEINS; MODELS, BIOLOGICAL; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-CBL; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 19644367829     PISSN: 10010602     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cr.7290268     Document Type: Short Survey

References (55)

1. Blume-Jensen P, Hunter T. Oncogenic kinase signaling. Nature 2001; 411:355-65.
2. Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 1995; 80:179-85.
3. Shilo BZ. Signaling by the Drosophila epidermal growth factor receptor pathway during development. Exp Cell Res 2003; 284: 140-9.
4. Casci T, Vinos J, Freeman M. Sprouty, an intracellular inhibitor of Ras signaling. Cell 1999; 96:655-65.
5. Musacchio M, Perrimon N. The Drosophila kekkon genes: novel members of both the leucine-rich repeat and immunoglobulin superfamilies expressed in the CNS. Dev Biol 1996; 178: 63-76.
6. Golembo M, Schweitzer R, Freeman M, et al. Argos transcription is induced by the Drosophila EGF receptor pathway to form an inhibitory feedback loop. Development 1996; 122:223-30.
7. Fiorini M, Ballaro C, Sala G, et al. Expression of RALT, a feedback inhibitor of ErbB receptors, is subjected to an integrated transcriptional and post-translational control. Oncogene 2002; 21:6530-9.
8. Tsang M, Dawid IB. Promotion and attenuation of FGF signaling through the Ras-MAPK pathway. Sci STKE 2004; 6:pe17.
9. Jongeward GD, Clandinin TR, Sternberg PW. sli-1, a negative regulator of let-23-mediated signaling in C. elegans. Genetics 1995; 139:1553-66.
10. Bowtell DD, Langdon WY. The protein product of the c-cbl oncogene rapidly complexes with the EGF receptor and is tyrosine phosphorylated following EGF stimulation. Oncogene 1995; 11:1561-7.
11. Levkowitz G, Waterman H, Ettenberg SA, et al. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell 1999; 4:1029-40.
12. Levkowitz G, Waterman H, Zamir E, et al. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev 1998; 12:3663-74.
13. Thien CB, Langdon WY. Cbl: many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol 2001; 2: 294-307.
14. Marmor MD, Yarden Y. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 2004; 23:2057-70.
15. Burke P, Schooler K, Wiley HS. Regulation of epidermal growth factor receptor signaling by endocytosis and intracellular trafficking. Mol Biol Cell 2001; 12:1897-910.
16. Haglund K, Sigismund S, Polo S, et al. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 2003; 5:461-6.
17. Mosesson Y, Shtiegman K, Katz M, et al. Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J Biol Chem 2003; 278:21323-6.
18. Longva KE, Blystad FD, Stang E, et al. Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J Cell Biol 2002; 156:843-54.
19. Stang E, Johannessen LE, Knardal SL, et al. Polyubiquitination of the epidermal growth factor receptor occurs at the plasma membrane upon ligand-induced activation. J Biol Chem 2000; 275:13940-7.
20. Polo S, Sigismund S, Faretta M, et al. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 2002; 416:451-5.
21. Salcini AE, Confalonieri S, Doria M, et al. Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev 1997; 11:2239-49.
22. Katzmann DJ, Odorizzi G, Emr SD. Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 2002; 3: 893-905.
23. Gur G, Rubin C, Katz M, et al. LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation. EMBO J 2004; 23:3270-81.
24. Hall AB, Jura N, DaSilva J, et al. hSpry2 Is Targeted to the Ubiquitin-Dependent Proteasome Pathway by c-Cbl. Curr Biol 2003; 13:308-14.
25. Laederich MB, Funes-Duran M, Yen L, et al. The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases. J Bil Chem 2004; 279:47050-6.
26. Rubin C, Litvak V, Medvedovsky H, et al. Sprouty fine-tunes EGF signaling through interlinked positive and negative feedback loops. Curr Biol 2003; 13:297-307.
27. Hacohen N, Kramer S, Sutherland D, et al. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 1998; 92:253-63.
28. Reich A, Sapir A, Shilo B. Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development 1999; 126:4139-47.
29. Impagnatiello MA, Weitzer S, Gannon G, et al. Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J Cell Biol 2001; 152:1087-98.
30. Lee CC, Putnam AJ, Miranti CK, et al. Overexpression of sprouty 2 inhibits HGF/SF-mediated cell growth, invasion, migration, and cytokinesis. Oncogene 2004; 23:5193-202.
31. Egan JE, Hall AB, Yatsula BA, et al. The bimodal regulation of epidermal growth factor signaling by human Sprouty proteins. Proc Natl Acad Sci U S A 2002; 99:6041-6.
32. Tefft D, Lee M, Smith S, et al. mSprouty2 inhibits FGF10-activated MAP kinase by differentially binding to upstream target proteins. Am J Physiol Lung Cell Mol Physiol 2002; 283: L700-6.
33. Wong ES, Lim J, Low BC, et al. Evidence for direct interaction between Sprouty and Cbl. J Biol Chem 2001; 276:5866-75.
34. Hanafusa H, Toril S, Yasunaga T, et al. Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signaling pathway. Nat Cell Biol 2002; 4:850-8.
35. Sasaki A, Taketomi T, Wakioka T, et al. Identification of a dominant negative mutant of Sprouty that potentiates fibroblast growth factor- but not epidermal growth factor-induced ERK activation. J Biol Chem 2001; 276:36804-8.
36. Yusoff P, Lao DH, Ong SH, et al. Sprouty2 inhibits the Ras/MAP kinase pathway by inhibiting the activation of Raf. J Biol Chem 2002; 277:3195-201.
37. Wong ES, Fong CW, Lim J, et al. Sprouty2 attenuates epidermal growth factor receptor ubiquitylation and endocytosis, and consequently enhances Ras/ERK signaling. Embo J 2002; 21:4796-808.
38. Fong CW, Leong HF. Wong ES, et al. Tyrosine phosphorylation of Sprouty2 enhances its interaction with c-Cbl and is crucial for its function. J Biol Chem 2003; 278:33456-64.
39. Tsygankov AY, Teckchandani AM, Feshchenko EA, et al. Beyond the RING: CBL proteins as multivalent adapters. Oncogene 2001; 20:6382-402.
40. Ghiglione C, Carraway KL, Amundadottir LT, et al. The transmembrane molecule kekkon 1 acts in a feedback loop to negatively regulate the activity of the Drosophila EGF receptor during oogenesis. Cell 1999; 96:847-56.
41. Ghiglione C, Amundadottir L, Andresdottir M, et al. Mechanism of inhibition of the Drosophila and mammalian EGF receptors by the transmembrane protein Kekkon 1. Development 2003; 130:4483-93.
42. Alvarado D, Rice AH, Duffy JB. Bipartite inhibition of Drosophila epidermal growth factor receptor by the extracellular and transmembrane domains of Kekkonl. Genetics 2004; 167:187-202.
43. MacLaren CM, Evans TA, Alvarado D, et al. Comparative analysis of the Kekkon molecules, related members of the LIG superfamily. Dev Genes Evol 2004; 214:360-6.
44. Guo D, Holmlund C, Henriksson R, et al. The LRIG gene family has three vertebrate paralogs widely expressed in human and mouse tissues, and a homolg in Ascidiacea. Genomics 2004; 84: 157-65.
45. Holmlund C, Nilsson J, Guo D, et al. Characterization and tissue-specific expression of human LRIG2. Gene 2004; 332:35-43.
46. Nilsson J, Vallbo C, Guo D, et al. Cloning, characterization, and expression of human LIG1. Biochem Biophys Res Commun 2001; 284:1155-61.
47. Suzuki Y, Sato N, Tohyama M, et al. cDNA cloning of a novel membrane glycoprotein that is expressed specifically in glial cells in the mouse brain. LIG-1, a protein with leucine-rich repeats and immunoglobulin-like domains. J Biol Chem 1996; 271:22522-7.
48. Suzuki Y, Miura H, Tanemura A, et al. Targeted disruption of LIG-1 gene results in psoriasiform epidermal hyperplasia. FEBS Lett 2002; 521:67-71.
49. Bai J, Chiu W, Wang J, et al. The cell adhesion molecule Echinoid defines a new pathway that antagonizes the Drosophila EGF receptor signaling pathway. Development 2001; 128:591-601.
50. Murdaca J, Treins C, Monthouel-Kartmann MN, et al. Grb10 prevents Nedd4-mediated vascular endothelial growth factor receptor-2 degradation. J Biol chem 2004; 279:26754-61.
51. Vecchione A, Marchese A, Henry P, et al. The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Mol Cell Biol 2003; 23: 3363-72.
52. Torii S, Kusakabe M, Yamamoto T, et al. Sef is a spatial regulator for Ras/MAP kinase signaling. Dev Cell 2004; 7:33-41.
53. Frankfort BJ, Mardon G. Senseless represses nuclear transduction of Egfr pathway activation. Development 2004; 131:563-70.
54. Jiang J, Ballinger CA, Wu Y, et al. CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J Biol Chem 2001; 276:42938-44.
55. Wakioka T, Sasaki A, Kato R, et al. Spred is a Sprouty-related suppressor of Ras signaling. Nature 2001; 412:647-51.