Regulation of epidermal growth factor receptor down-regulation by UBPY-mediated deubiquitination at endosomes

Molecular Biology of the Cell

Volumn 16, Issue 11, 2005, Pages 5163-5174

  Mizuno, Emi ^a   Iura, Takanobu ^a   Mukai, Akiko ^a   Yoshimori, Tamotsu ^b   Kitamura, Naomi ^a   Komada, Masayuki ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; LIGAND; MUTANT PROTEIN; PROTEIN HRS; PROTEIN SKD1; PROTEIN TYROSINE KINASE; PROTEIN USP8; PROTEINASE; UB SPECIFIC PROTEASE Y; UNCLASSIFIED DRUG;

ACCELERATION; ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME PURIFICATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UBIQUITINATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; DOWN-REGULATION; ENDOCYTOSIS; ENDOPEPTIDASES; ENDOSOMES; MODELS, BIOLOGICAL; PHOSPHOPROTEINS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA INTERFERENCE; TRANSFECTION;

ANIMALIA;

EID: 27644438783     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-06-0560     Document Type: Article

References (55)

1. Alroy, I. and Yarden, Y. (1997). The ErbB signaling network in embryogenesis and oncogenesis: signal diversification through combinatorial ligand-receptor interactions. FEBS Lett. 410, 83-86.
2. Amerik, A. Y., and Hochstrasser, M. (2004). Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695, 189-207.
3. Amerik, A. Y., Nowak, J., Swaminathan, S., and Hochstrasser, M. (2000). The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol. Biol. Cell 11, 3365-3380.
4. Bache, K. G., Brech, A., Mehlum, A., and Stenmark, H. (2003a). Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162, 435-442.
5. Bache, K. G., Raiborg, C., Mehlum, A., and Stenmark, H. (2003b). STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521.
6. Baker, R. T., Wang, X.-W., Woollatt, E., White, J. A., and Sutherland, G. R. (1999). Identification, functional characterization, and chromosomal localization of USP15, a novel human ubiquitin-specific protease related to the UNP oncoprotein, and a systematic nomenclature for human ubiquitin-specific proteases. Genomics 59, 264-274.
7. Bilodeau, P. S., Urbanowski, J. L., Winistorfer, S. C., and Piper, R. C. (2002). The Vps27p-Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat. Cell Biol. 4, 534-539.
8. Bishop, N., Horman, A., and Woodman, P. (2002). Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J. Cell Biol. 157, 91-102.
9. Bishop, N., and Woodman, P. (2000). ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol. Biol. Cell 11, 227-239.
10. Carlsson, S. R., Roth, J., Piller, F., and Fukuda, M. (1988). Isolation and characterization of human lysosomal membrane glycoproteins, h-lamp-1 and h-lamp-2. J. Biol. Chem. 263, 18911-18919.
11. Duan, L., et al. (2003). Cbl-mediated ubiquitylation is required for lysosomal sorting of epidermal growth factor receptor but is dispensable for endocytosis. J. Biol. Chem. 278, 28950-28960.
12. Dupre, S., and Haguenauer-Tsapis, R. (2001). Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol. Cell. Biol. 21, 4482-4494.
13. Flint, A. J., Tiganis, T., Barford, D., and Tonks, N. K. (1997). Development of "substrate-trapping" mutants to identify physiological substrates of protein tyrosine phosphatases. Proc. Natl. Acad. Sci. USA 94, 1680-1685.
14. Mm/Ras-GRF1. J. Biol. Chem. 276, 39448-39454.
15. Gruenberg, J. (2001). The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell. Biol. 2, 721-730.
16. Haglund, K., Sigismund, S., Polo, S., Szymkiewicz, I., Di Fiore, P. P., and Dikic, I. (2003). Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5, 461-466.
17. Hammond, D. E., Carter, S., McCullough, J., Urbe, S., Vande Woude, G., and Clague, M. J. (2003). Endosomal dynamics of Met determine signaling output. Mol. Biol. Cell 14, 1346-1354.
18. Hicke, L. (2001). A new ticket for entry into budding vesicles-ubiquitin. Cell 106, 527-530.
19. Kanazawa, C., Morita, E., Yamada, M., Ishii, N., Miura, S., Asao, H., Yoshimori, T., and Sugamura, K. (2003). Effects of deficiencies of STAMs and Hrs, mammalian class E Vps proteins, on receptor downregulation. Biochem. Biophys. Res. Commun. 309, 848-856.
20. Kaneko, T., Kumasaka, T., Ganbe, T., Sato, T., Miyazawa, K., Kitamura, N., and Tanaka, N. (2003). Structural insight into modest binding of a non-PXXP ligand to the signal transducing adaptor molecule-2 Src homology 3 domain. J. Biol. Chem. 278, 48162-48168.
21. Kato, M., Miyazawa, K., and Kitamura, N. (2000). A deubiquitinating enzyme UBPY interacts with the SrC homology 3 domain of Hrs-binding protein via a novel binding motif PX(V/I)(D/N)RXXKP. J. Biol. Chem. 275, 37481-37487.
22. Katzmann, D. J., Babst, M., and Emr, S. D. (2001). Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155.
23. Katzmann, D. J., Odorizzi, G., and Emr, S. D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell. Biol. 3, 893-905.
24. Komada, M., and Kitamura, N. (1995). Growth factor-induced tyrosine phosphorylation of Hrs, a novel 115-kilodalton protein with a structurally conserved putative zinc finger domain. Mol. Cell. Biol. 15, 6213-6221.
25. Komada, M., and Kitamura, N. (2005). The Hrs/STAM complex in the downregulation of receptor tyrosine kinases. J. Biochem. 137, 1-8.
26. Komada, M., Masaki, R., Yamamoto, A., and Kitamura, N. (1997). Hrs, a tyrosine kinase substrate with a conserved double zinc finger domain, is localized to the cytoplasmic surface of early endosomes. J. Biol. Chem. 272, 20538-20544.
27. Lenferink, A.E.G., Pinkas-Kramarski, R., van de Poll, M.L.M., van Vugt, M.J.H., Klapper, L. N., Tzahar, E., Waterman, H., Sela, M., van Zoelen, E.J.J., and Yarden, Y. (1998). Differential endocytic routing of homo- and heterodimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers. EMBO J. 17, 3385-3397.
28. Levkowitz, G., Waterman, H., Zamir, E., Kam, Z., Oved, S., Langdon, W. Y., Beguinot, L., Geiger, 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.
29. Liu, P., and Chernoff, J. (1997). Protein tyrosine phosphatase 1B interacts with and is tyrosine phosphorylated by the epidermal growth factor receptor. Biochem. J. 327, 139-145.
30. Lloyd, T. E., Atkinson, R., Wu, M. N., Zhou, Y., Pennetta, G., and Bellen, H. J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269.
31. Longva, K. E., Blystad, F. D., Stang, E., Larsen, A. M., Johannessen, L. E., and Madshus, I. H. (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.
32. Losko, S., Kopp, F., Kranz, A., and Kolling, R. (2001). Uptake of the ATP-binding cassette (ABC) transporter Ste6 into the yeast vacuole is blocked in the doa4 mutant. Mol. Biol. Cell 12, 1047-1059.
33. Lu, Q., Hope, L. W., Brasch, M., Reinhard, C., and Cohen, S. N. (2003). TSG101 interaction with HRS mediates endosomal trafficking and receptor downregulation. Proc. Natl. Acad. Sci. USA 100, 7626-7631.
34. McCullough, J., Clague, M. J., and Urbe, S. (2004). AMSH is an endosome-associated ubiquitin isopeptidase. J. Cell Biol. 166, 487-492.
35. Mizuno, E., Kawahata, K., Kato, M., Kitamura, N., and Komada, M. (2003). STAM proteins bind ubiquitinated proteins on the early endosome via the VHS domain and ubiquitin-interacting motif. Mol. Biol. Cell 14, 3675-3689.
36. Mizuno, E., Kawahata, K., Okamoto, A., Kitamura, N., and Komada, M. (2004). Association with Hrs is required for the early endosomal localization, stability, and function of STAM. J. Biochem. 135, 385-396.
37. Morino, C., Kato, M., Yamamoto, A., Mizuno, E., Hayakawa, A., Komada, M., and Kitamura, N. (2004). A role for Hrs in endosomal sorting of ligand-stimulated and unstimulated epidermal growth factor receptor. Exp. Cell Res. 297, 380-391.
38. Mosesson, Y., Shtiegman, K., Katz, M., Zwang, Y., Vereb, G., Szollosi, J., and Yarden, Y. (2003). Endocytosis of receptor tyrosine kinases is driven by monoubiquitination, not polyubiquitination. J. Biol. Chem. 278, 21323-21326.
39. Naviglio, S., Matteucci, C., Matoskova, B., Nagase, T., Nomura, N., Di Fiore, P. P., and Draetta, G. F. (1998). UBPY: a growth-regulated human ubiquitin isopeptidase. EMBO J 17, 3241-3250.
40. Peschard, P., Fournier, T. M., Lamorte, L., Naujokas, M. A., Band, H., Langdon, W. Y., and Park, M. (2001). Mutation of the c-Cbl TKB domain binding site on the Met receptor tyrosine kinase converts it into a transforming protein. Mol. Cell 8, 995-1004.
41. Raiborg, C., Bache, K. G., Gillooly, D. J., Helene Madshus, I., Stang, E., and Stenmark, H. (2002). Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4, 394-398.
42. Shih, S. C., Katzmann, D. J., Schnell, J. D., Sutanto, M., Emr, S. D., and Hicke, L. (2002). Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4, 389-393.
43. Sigismund, S., Woelk, T., Puri, C., Maspero, E., Tacchetti, C., Transidico, P., Di Fiore, P. P., and Polo, S. (2005). Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. USA 102, 2760-2765.
44. Soares, L., Seroogy, C., Skrenta, H., Anandasabapathy, N., Lovelace, P., Chung, C. D., Engleman, E., and Fathman, C. G. (2004). Two isoforms of otubain 1 regulate T cell anergy via GRAIL. Nat. Immunol. 5, 45-54.
45. Soboleva, T. A., and Baker, R. T. (2004). Deubiquitinating enzymes: their functions and substrate specificity. Curr. Protein Pept. Sci. 5, 191-200.
46. Swaminathan, S., Amerik, A. Y., and Hochstrasser, M. (1999). The Doa4 deubiquitinating enzyme is required for ubiquitin homeostasis in yeast. Mol. Biol. Cell 10, 2583-2594.
47. Tanaka, N., Kaneko, K., Asao, H., Kasai, H., Endo, Y., Fujita, T., Takeshita, T., and Sugamura, K. (1999). Possible involvement of a novel STAM-associated molecule "AMSH" in intracellular signal transduction mediated by cytokines. J. Biol. Chem. 274, 19129-19135.
48. Thien, C.B.F., and Langdon, W. Y. (2001). Cbl: many adaptations to regulate protein tyrosine kinases. Nat. Rev. Mol. Cell. Biol. 2, 294-305.
49. Verma, R., Aravind, L., Oania, R., McDonald, W. H., Yates Spaceiiiqq, J. R., Koonin, E. V., and Deshaies, R. J. (2002). Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611-615.
50. Wang, Z., Zhang, L., Yeung, T. K., and Chen, X. (1999). Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation. Mol. Biol. Cell 10, 1621-1636.
51. Wing, S. S. (2003). Deubiquitinating enzymes - the importance of driving in reverse along the ubiquitin-proteasome pathway. Int. J. Biochem. Cell Biol. 35, 590-605.
52. Worthylake, R., Opresko, L. K., and Wiley, H. S. (1999). ErbB-2 amplification inhibits down-regulation and induces constitutive activation of both ErbB-2 and epidermal growth factor receptors. J. Biol. Chem. 274, 8865-8874.
53. Wu, X., Yen, L., Irwin, L., Sweeney, C., and Carraway Spaceiiiqq, K. L. (2004). Stabilization of the E3 ubiquitin ligase Nrdp1 by the deubiquitinating enzyme USP8. Mol. Cell. Biol. 24, 7748-7757.
54. Yao, T., and Cohen, R. E. (2002). A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419, 403-407.
55. Yoshimori, T., Yamagata, F., Yamamoto, A., Mizushima, N., Kabeya, Y., Nara, A., Miwako, I., Ohashi, M., Ohsumi, M., and Ohsumi, Y. (2000). The mouse SKD1, a homologue of yeast Vps4p, is required for normal endosomal trafficking and morphology in mammalian cells. Mol. Biol. Cell 11, 747-763.