UBE4B protein couples ubiquitination and sorting machineries to enable epidermal growth factor receptor (EGFR) degradation

Journal of Biological Chemistry

Volumn 289, Issue 5, 2014, Pages 3026-3039

  Sirisaengtaksin, Natalie ^a   Gireud, Monica ^a   Yan, Qing ^a   Kubota, Yoshihisa ^a   Meza, Denisse ^a   Waymire, Jack C ^a   Zage, Peter E ^b   Bean, Andrew J ^a,c  

^a UNIVERSITY OF TEXAS   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEUBIQUITINATION; E3 UBIQUITIN LIGASE; ENDOCYTOSIS; ENDOSOMES; ESCRT; PROTEIN SORTING; UBIQUITINATION; USP8;

CELL MEMBRANE; ENDOPEPTIDASES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; HELA CELLS; HUMANS; MEMBRANE PROTEINS; PHOSPHOPROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN THIOLESTERASE; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITINATION;

EID: 84893465860     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.495671     Document Type: Article

References (54)

1. Lemmon, M. A., and Schlessinger, J. (2010) Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134
2. Yan, Q., Sun, W., Kujala, P., Lotfi, Y., Vida, T. A., and Bean, A. J. (2005) CART. An Hrs/actinin-4/BERP/myosin V protein complex required for efficient receptor recycling. Mol. Biol. Cell 16, 2470-2482
3. Komada, M., and Kitamura, N. (2005) The Hrs/STAM complex in the downregulation of receptor tyrosine kinases. J. Biochem. 137, 1-8
4. Katzmann, D. J., Odorizzi, G., and Emr, S. D. (2002) Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 893-905
5. Nakayama, K. (2004) Membrane traffic. Editorial overview. J. Biochem. 136, 751-753
6. Piper, R. C., and Luzio, J. P. (2001) Late endosomes. Sorting and partitioning in multivesicular bodies. Traffic 2, 612-621
7. Bache, K. G., Brech, A., Mehlum, A., and Stenmark, H. (2003) Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162, 435-442
8. Saksena, S., Sun, J., Chu, T., and Emr, S. D. (2007) ESCRTing proteins in the endocytic pathway. Trends Biochem. Sci. 32, 561-573
9. 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
10. Marmor, M. D., and Yarden, Y. (2004) Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23, 2057-2070
11. Bache, K. G., Raiborg, C., Mehlum, A., and Stenmark, H. (2003) STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521
12. Mizuno, E., Iura, T., Mukai, A., Yoshimori, T., Kitamura, N., and Komada, M. (2005) Regulation of epidermal growth factor receptor down-regulation by UBPY-mediated deubiquitination at endosomes. Mol. Biol. Cell 16, 5163-5174
13. Eden, E. R., Huang, F., Sorkin, A., and Futter, C. E. (2012) The role of EGF receptor ubiquitination in regulating its intracellular traffic. Traffic 13, 329-337
14. MacDonald, C., Buchkovich, N. J., Stringer, D. K., Emr, S. D., and Piper, R. C. (2012) Cargo ubiquitination is essential for multivesicular body intralumenal vesicle formation. EMBO Rep. 13, 331-338
15. Hurley, J. H., and Hanson, P. I. (2010) Membrane budding and scission by the ESCRT machinery. It's all in the neck. Nat. Rev. Mol. Cell Biol. 11, 556-566
16. Williams, R. L., and Urbé, S. (2007) The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368
17. Wollert, T., Wunder, C., Lippincott-Schwartz, J., and Hurley, J. H. (2009) Membrane scission by the ESCRT-III complex. Nature 458, 172-177
18. Haglund, K., and Dikic, I. (2012) The role of ubiquitylation in receptor endocytosis and endosomal sorting. J. Cell Sci. 125, 265-275
19. Schlessinger, J. (2000) Cell signalingbyreceptor tyrosine kinases. Cell 103, 211-225
20. Alexander, A. (1998) Endocytosis and intracellular sorting of receptor tyrosine kinases. Front. Biosci. 3, d729-738
21. 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
22. Huang, F., Goh, L. K., and Sorkin, A. (2007) EGF receptor ubiquitination is not necessary for its internalization. Proc. Natl. Acad. Sci. U. S. A. 104, 16904-16909
23. Li, W., Bengtson, M. H., Ulbrich, A., Matsuda, A., Reddy, V. A., Orth, A., Chanda, S. K., Batalov, S., and Joazeiro, C. A. (2008) Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. PLoS ONE 3, e1487
24. Nijman, S. M., Luna-Vargas, M. P., Velds, A., Brummelkamp, T. R., Dirac, A. M., Sixma, T. K., and Bernards, R. (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786
25. Richter, C., West, M., and Odorizzi, G. (2007) Dual mechanisms specify Doa4-mediated deubiquitination at multivesicular bodies. EMBO J. 26, 2454-2464
26. Alwan, H. A., and Van Leeuwen, J. E. (2007) UBPY-mediated epidermal growth factor receptor (EGFR) de-ubiquitination promotes EGFR degradation. J. Biol. Chem. 282, 1658-1669
27. Berlin, I., Schwartz, H., and Nash, P. D. (2010) Regulation of epidermal growth factor receptor ubiquitination and trafficking by the USP8-STAM complex. J. Biol. Chem. 285, 34909-34921
28. Row, P. E., Liu, H., Hayes, S., Welchman, R., Charalabous, P., Hofmann, K., Clague, M. J., Sanderson, C. M., and Urbé, S. (2007) The MIT domain of UBPY constitutes a CHMP binding and endosomal localization signal required for efficient epidermal growth factor receptor degradation. J. Biol. Chem. 282, 30929-30937
29. Tsujimoto, S., Pelto-Huikko, M., Aitola, M., Meister, B., Vik-Mo, E. O., Davanger, S., Scheller, R. H., and Bean, A. J. (1999) The cellular and developmental expression of hrs-2 in rat. Eur. J. Neurosci. 11, 3047-3063
30. Sun, W., Vida, T. A., Sirisaengtaksin, N., Merrill, S. A., Hanson, P. I., and Bean, A. J. (2010) Cell-free reconstitution of multivesicular body formation and receptor sorting. Traffic 11, 867-876
31. Bean, A. J., Davanger, S., Chou, M. F., Gerhardt, B., Tsujimoto, S., and Chang, Y. (2000) Hrs-2 regulates receptor-mediated endocytosis via interactions with Eps15. J. Biol. Chem. 275, 15271-15278
32. Hatakeyama, S., Yada, M., Matsumoto, M., Ishida, N., and Nakayama, K. I. (2001) U box proteins as a new family of ubiquitin-protein ligases. J. Biol. Chem. 276, 33111-33120
33. Tsujimoto, S., and Bean, A. J. (2000) Distinct protein domains are responsible for the interaction of Hrs-2 with SNAP-25. The role of Hrs-2 in 7 S complex formation. J. Biol. Chem. 275, 2938-2942
34. Sun, W., Yan, Q., Vida, T. A., and Bean, A. J. (2003) Hrs regulates early endosome fusion by inhibiting formation of an endosomal SNARE complex. J. Cell Biol. 162, 125-137
35. Rezvani, K., Teng, Y., Shim, D., and De Biasi, M. (2007) Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity. J. Neurosci. 27, 10508-10519
36. Krall, J. A., Beyer, E. M., and MacBeath, G. (2011) High- and low-affinity epidermal growth factor receptor-ligand interactions activate distinct signaling pathways. PLoS ONE 6, e15945
37. Alwan, H. A., Van Zoelen, E. J., and Van Leeuwen, J. E. (2003) Ligandinduced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. J. Biol. Chem. 278, 35781-35790
38. 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
39. Balut, C. M., Loch, C. M., and Devor, D. C. (2011) Role of ubiquitylation and USP8-dependent deubiquitylation in the endocytosis and lysosomal targeting of plasma membrane KCa3. 1. FASEB J. 25, 3938-3948
40. Babst, M., Odorizzi, G., Estepa, E. J., and Emr, S. D. (2000) Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1, 248-258
41. Bache, K. G., Stuffers, S., Malerød, L., Slagsvold, T., Raiborg, C., Lechardeur, D., Wälchli, S., Lukacs, G. L., Brech, A., and Stenmark, H. (2006) The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol. Biol. Cell 17, 2513-2523
42. 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
43. Zage, P. E., Sirisaengtaksin, N., Liu, Y., Gireud, M., Brown, B. S., Palla, S., Richards, K. N., Hughes, D. P., and Bean, A. J. (2013) UBE4B levels are correlated with clinical outcomes in neuroblastoma patients and with altered neuroblastoma cell proliferation and sensitivity to epidermal growth factor receptor inhibitors. Cancer 119, 915-923
44. Wang, Y., Pennock, S., Chen, X., and Wang, Z. (2002) Endosomal signaling of epidermal growth factor receptor stimulates signal transduction pathways leading to cell survival. Mol. Cell. Biol. 22, 7279-7290
45. Krona, C., Ejeskär, K., Abel, F., Kogner, P., Bjelke, J., Björk, E., Sjöberg, R. M., and Martinsson, T. (2003) Screening for gene mutations in a 500 kb neuroblastoma tumor suppressor candidate region in chromosome 1p. Mutation and stage-specific expression in UBE4B/UFD2. Oncogene 22, 2343-2351
46. Marchese, A., Raiborg, C., Santini, F., Keen, J. H., Stenmark, H., and Benovic, J. L. (2003) The E3 ubiquitin ligase AIP4 mediates ubiquitination and sorting of the G protein-coupled receptor CXCR4. Dev. Cell 5, 709-722
47. Nakamura, N., Fukuda, H., Kato, A., and Hirose, S. (2005) MARCH-II is a syntaxin-6-binding protein involved in endosomal trafficking. Mol. Biol. Cell 16, 1696-1710
48. Fukuda, H., Nakamura, N., and Hirose, S. (2006) MARCH-III Is a novel component of endosomes with properties similar to those of MARCH-II. J. Biochem. 139, 137-145
49. Hassink, G., Slotman, J., Oorschot, V., Van Der Reijden, B. A., Monteferrario, D., Noordermeer, S. M., Van Kerkhof, P., Klumperman, J., and Strous, G. J. (2012) Identification of the ubiquitin ligase Triad1 as a regulator of endosomal transport. Biol. Open 1, 607-614
50. Bocock, J. P., Carmicle, S., Madamba, E., and Erickson, A. H. (2010) Nuclear targeting of an endosomal E3 ubiquitin ligase. Traffic 11, 756-766
51. Starita, L. M., Pruneda, J. N., Lo, R. S., Fowler, D. M., Kim, H. J., Hiatt, J. B., Shendure, J., Brzovic, P. S., Fields, S., and Klevit, R. E. (2013) Activityenhancing mutations in an E3 ubiquitin ligase identified by high-throughput mutagenesis. Proc. Natl. Acad. Sci. U. S. A. 110, E1263-1272
52. 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
53. Luhtala, N., and Odorizzi, G. (2004) Bro1 coordinates deubiquitination in the multivesicular body pathway by recruiting Doa4 to endosomes. J. Cell Biol. 166, 717-729
54. Berruti, G., Ripolone, M., and Ceriani, M. (2010) USP8, a regulator of endosomal sorting, is involved in mouse acrosome biogenesis through interaction with the spermatid ESCRT-0 complex and microtubules. Biol. Reprod. 82, 930-939