Epidermal growth factor receptor internalization through clathrin-coated pits requires Cbl RING finger and proline-rich domains but not receptor polyubiquitylation

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Volumn 4, Issue 8, 2003, Pages 529-543

  Jiang, Xuejun ^a,b   Sorkin, Alexander ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

Clathrin; Endocytosis; Epidermal growth factor; Phosphorylation; Tyrosine

Indexed keywords

CELL PROTEIN; CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; MUTANT PROTEIN; PHOSPHOTYROSINE; YELLOW FLUORESCENT PROTEIN;

ARTICLE; CELL ORGANELLE; COATED PIT; COATED VESICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME SUBSTRATE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; STRUCTURE ACTIVITY RELATION;

EID: 0042202634     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0854.2003.t01-1-00109.x     Document Type: Article

References (36)

1. Waterman H, Yarden Y. Molecular mechanisms underlying endocytosis and sorting of ErbB receptor tyrosine kinases. FEBS Lett 2001;490:142-152.
2. Sorkin A, Von Zastrow M. Signal transduction and endocytosis: close encounters of many kinds. Nat Rev Mol Cell Biol 2002;3:600-614.
3. Thien CB, Langdon WY. Cbl: many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol 2001;2:294-307.
4. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, Langdon WY, Beguinot L, Geiger B, Yarden Y. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev 1998;12:3663-3674.
5. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, Alroy I, Lavi S, Iwai K, Reiss Y, Ciechanover A, Lipkowitz S, Yarden Y. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1 [In Process Citation]. Mol Cell 1999;4:1029-1040.
6. Thien CB, Walker F, Langdon WY. RING finger mutations that abolish c-Cbl-directed polyubiquitination and downregulation of the EGF receptor are insufficient for cell transformation. Mol Cell 2001;7:355-365.
7. Waterman H, Katz M, Rubin C, Shtiegman K, Lavi S, Elson A, Jovin T, Yarden Y. A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. EMBO J 2002;21:303-313.
8. Soubeyran P, Kowanetz K, Szymkiewicz I, Langdon WY, Dikic I. Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 2002;416:183-187.
9. Meng W, Sawasdikosol S, Burakoff SJ, Eck MJ. Structure of the amino-terminal domain of Cbl complexed to its binding site on ZAP-70 kinase. Nature 1999;398:84-90.
10. Joazeiro CA, Wing SS, Huang H, Leverson JD, Hunter T, Liu YC. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 1999;286:309-312.
11. Meisner H, Conway BR, Hartley D, Czech MP. Interactions of Cbl with Grb2 and phosphatidylinositol 3′-kinase in activated Jurkat cells. Mol Cell Biol 1995;15:3571-3578.
12. Thien CB, Langdon WY. Tyrosine kinase activity of the EGF receptor is enhanced by the expression of oncogenic 70Z-Cbl. Oncogene 1997;15:2909-2919.
13. Fukazawa T, Miyake S, Band V, Band H. Tyrosine phosphorylation of Cbl upon epidermal growth factor (EGF) stimulation and its association with EGF receptor and downstream signaling proteins. J Biol Chem 1996;271:14554-14559.
14. Donovan JA, Ota Y, Langdon WY, Samelson LE. Regulation of the association of p120cbl with Grb2 in Jurkat T cells. J Biol Chem 1996;271:26369-26374.
15. de Melker AA, van der Horst G, Calafat J, Jansen H, Borst J. c-Cbl ubiquitinates the EGF receptor at the plasma membrane and remains receptor associated throughout the endocytic route. J Cell Sci 2001;114:2167-2178.
16. Lill NL, Douillard P, Awwad RA, Ota S, Lupher ML Jr, Miyake S, Meissner-Lula N, Hsu VW, Band H. The evolutionarily conserved N-terminal region of Cbl is sufficient to enhance down-regulation of the epidermal growth factor receptor. J Biol Chem 2000;275: 367-377.
17. Carter RE, Sorkin A. Endocytosis of functional epidermal growth factor receptor-green fluorescent protein chimera. J Biol Chem 1998; 273:35000-35007.
18. Sorkina T, Huang F, Beguinot L, Sorkin A. Effect of tyrosine kinase inhibitors on clathrin coated pit recruitment and internalization of epidermal growth factor receptor. J Biol Chem 2002;277:27433-27441.
19. Jiang X, Huang F, Marusyk A, Sorkin A. Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol Biol Cell 2003;14:858-870.
20. Hicke L. A new ticket for entry into budding vesicles-ubiquitin. Cell 2001;106:527-530.
21. Lund KA, Opresko LK, Strarbuck C, Walsh BJ, Wiley HS. Quantitative analysis of the endocytic system involved in hormone-induced receptor internalization. J Biol Chem 1990;265:15713-13723.
22. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994;127:915-934.
23. Petrelli A, Gilestro GF, Lanzardo S, Comoglio PM, Migone N, Giordano S. The endophilin-CIN85-Cbl complex mediates ligand-dependent down-regulation of c-Met. Nature 2002;416:187-190.
24. Yokouchi M, Kondo T, Houghton A, Bartkiewicz M, Horne WC, Zhang H, Yoshimura A, Baron R. Ligand-induced ubiquitination of the epidermal growth factor receptor involves the interaction of the c-Cbl RING finger and UbcH7. J Biol Chem 1999;274: 31707-31712.
25. Stang E, Johannessen LE, Knardal SL, Madshus IH. Polyubiquitination of the epidermal growth factor receptor occurs at the plasma membrane upon ligand-induced activation. J Biol Chem 2000;275: 13940-13947.
26. Szymkiewicz I, Kowanetz K, Soubeyran P, Dinarina A, Lipkowitz S, Dikic I. CIN85 participates in Cbl-b-mediated downregulation of receptor tyrosine kinases. J Biol Chem 2002;277:39666-39672.
27. Haglund K, Shimokawa N, Szymkiewicz I, Dikic I. Cbl-directed monoubiquitination of CIN85 is involved in regulation of ligand-induced degradation of EGF receptors. Proc Natl Acad Sci USA 2002;99: 12191-12196.
28. Hicke L, Riezman H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 1996;84: 277-287.
29. Ettenberg SA, Magnifico A, Cuello M, Nau MM, Rubinstein YR, Yarden Y, Weissman AM, Lipkowitz S. Cbl-b-deperident coordinated degradation of the epidermal growth factor receptor signaling complex. J Biol Chem 2001;276:27677-27684.
30. van Delft S, Govers R, Strous GJ, Verkleij AJ, van Bergen en Henegouwen PMP. Epidermal growth fcator induces ubiquitination of Eps15. J Biol Chem 1997;272:14013-14016.
31. Polo S, Sigismund S, Faretta M, Guidi M, Capua MR, Bossi G, Chen H, De Camilli P, Di Fiore PP. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 2002;416:451-455.
32. Confalonieri S, Salcini AE, Puri C, Tacchetti C, Di Fiore PP. Tyrosine phosphorylation of Eps15 is required for ligand-regulated, but not constitutive, endocytosis. J Cell Biol 2000;150:905-912.
33. Beguinot L, Werth D, Ito S, Richert N, Willingham MC, Pastan I. Functional studies on the EGF receptor with an antibody that recognizes the intracellular portion of the receptor. J Biol Chem 1986;261:1801-1807.
34. Sorkin A, Helin K, Waters CM, Carpenter G, Beguinot L. Multiple autophosphorylation sites of the epidermal growth factor receptor are essential for receptor kinase activity and internalization. J Biol Chem 1992;267:8672-8678.
35. Jiang X, Sorkin A. Coordinated trafficking of Grb2 and Ras during EGF receptor endocytosis visualized in living cells. Mol Biol Cell 2002;13:1522-1535.
36. Kornilova E, Sorkina T, Beguinot L, Sorkin A. Lysosomal targeting of epidermal growth factor receptors via a kinase-dependent pathway is mediated by the receptor carboxyl-terminal residues 1022-1163. J Biol Chem 1996;271:30340-30346.