Regulation of Endocytic Sorting by ESCRT-DUB-Mediated Deubiquitination

Cell Biochemistry and Biophysics

Volumn 60, Issue 1-2, 2011, Pages 39-46

  Wright, Michelle H ^a   Berlin, Ilana ^a   Nash, Piers D ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b GCIS   (United States)

Author keywords

Deubiquitylase; Endocytosis; Protease; Receptor; Ubiquitin

Indexed keywords

CELL SURFACE RECEPTOR; ESCRT PROTEIN; PROTEINASE; STAMBP PROTEIN, HUMAN; UBIQUITIN THIOLESTERASE; USP8 PROTEIN, HUMAN;

ARTICLE; BIOLOGICAL MODEL; ENDOCYTOSIS; HUMAN; METABOLISM; PROTEIN BINDING; PROTEIN TRANSPORT; UBIQUITINATION;

ENDOCYTOSIS; ENDOPEPTIDASES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HUMANS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE; UBIQUITIN THIOLESTERASE; UBIQUITINATION;

EID: 79955940965     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12013-011-9181-9     Document Type: Article

References (79)

1. Jovic, M., Sharma, M., Rahajeng, J., & Caplan, S. (2010). The early endosome: A busy sorting station for proteins at the crossroads. Histology and Histopathology, 25, 99-112.
2. Waterman, H., & Yarden, Y. (2001). Molecular mechanisms underlying endocytosis and sorting of ErbB receptor tyrosine kinases. FEBS Letters, 490, 142-152.
3. Duncan, L. M., Piper, S., Dodd, R. B., Saville, M. K., Sanderson, C. M., Luzio, J. P., et al. (2006). Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO Journal, 25, 1635-1645.
4. Galan, J. M., & Haguenauer-Tsapis, R. (1997). Ubiquitin lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO Journal, 16, 5847-5854.
5. Geetha, T., Jiang, J., & Wooten, M. W. (2005). Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling. Molecular Cell, 20, 301-312.
6. Hicke, L., & Dunn, R. (2003). Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annual Review of Cell and Developmental Biology, 19, 141-172.
7. Pickart, C. M., & Fushman, D. (2004). Polyubiquitin chains: Polymeric protein signals. Current Opinion Chemical Biology, 8, 610-616.
8. Kirisako, T., Ichimura, Y., Okada, H., Kabeya, Y., Mizushima, N., Yoshimori, T., et al. (2000). The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. Journal of Cell Biology, 151, 263-276.
9. Urbe, S., McCullough, J., Row, P., Prior, I. A., Welchman, R., & Clague, M. J. (2006). Control of growth factor receptor dynamics by reversible ubiquitination. Biochemical Society Transactions, 34, 754-756.
10. Dikic, I., Wakatsuki, S., & Walters, K. J. (2009). Ubiquitin-binding domains-from structures to functions. Nature Reviews Molecular Cell Biology, 10, 659-671.
11. Ardley, H. C., & Robinson, P. A. (2005). E3 ubiquitin ligases. Essays in Biochemistry, 41, 15-30.
12. Deshaies, R. J., & Joazeiro, C. A. (2009). RING domain E3 ubiquitin ligases. Annual Review of Biochemistry, 78, 399-434.
13. Magnifico, A., Ettenberg, S., Yang, C., Mariano, J., Tiwari, S., Fang, S., et al. (2003). WW domain HECT E3s target Cbl RING finger E3s for proteasomal degradation. Journal of Biological Chemistry, 278, 43169-43177.
14. Wang, J., & Pantopoulos, K. (2005). The pathway for IRP2 degradation involving 2-oxoglutarate-dependent oxygenase(s) does not require the E3 ubiquitin ligase activity of pVHL. Biochimica et Biophysica Acta, 1743, 79-85.
15. Amerik, A. Y., & Hochstrasser, M. (2004). Mechanism and function of deubiquitinating enzymes. Biochimica et Biophysica Acta, 1695, 189-207.
16. Nijman, S. M., Huang, T. T., Dirac, A. M., Brummelkamp, T. R., Kerkhoven, R. M., D'Andrea, A. D., et al. (2005). The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Molecular Cell, 17, 331-339.
17. Nijman, S. M., Luna-Vargas, M. P., Velds, A., Brummelkamp, T. R., Dirac, A. M., Sixma, T. K., et al. (2005). A genomic and functional inventory of deubiquitinating enzymes. Cell, 123, 773-786.
18. Komander, D., Clague, M. J., & Urbe, S. (2009). Breaking the chains: Structure and function of the deubiquitinases. Nature Reviews Molecular Cell Biology, 10, 550-563.
19. Wilkinson, K. D., Tashayev, V. L., O'Connor, L. B., Larsen, C. N., Kasperek, E., & Pickart, C. M. (1995). Metabolism of the polyubiquitin degradation signal: Structure, mechanism, and role of isopeptidase T. Biochemistry, 34, 14535-14546.
20. Reyes-Turcu, F. E., Ventii, K. H., & Wilkinson, K. D. (2009). Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annual Review of Biochemistry, 78, 363-397.
21. Ren, J., Kee, Y., Huibregtse, J. M., & Piper, R. C. (2007). Hse1, a component of the yeast Hrs-STAM ubiquitin-sorting complex, associates with ubiquitin peptidases and a ligase to control sorting efficiency into multivesicular bodies. Molecular Biology of the Cell, 18, 324-335.
22. Ren, X., Kloer, D. P., Kim, Y. C., Ghirlando, R., Saidi, L. F., Hummer, G., et al. (2009). Hybrid structural model of the complete human ESCRT-0 complex. Structure, 17, 406-416.
23. Pawson, T., & Nash, P. (2003). Assembly of cell regulatory systems through protein interaction domains. Science, 300, 445-452.
24. Katz, E. J., Isasa, M., & Crosas, B. (2010). A new map to understand deubiquitination. Biochemical Society Transactions, 38, 21-28.
25. Coornaert, B., Baens, M., Heyninck, K., Bekaert, T., Haegman, M., Staal, J., et al. (2008). T cell antigen receptor stimulation induces MALT1 paracaspase-mediated cleavage of the NF-kappaB inhibitor A20. Nature Immunology, 9, 263-271.
26. Wertz, I. E., O'Rourke, K. M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S., et al. (2004). De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature, 430, 694-699.
27. Boone, D. L., Turer, E. E., Lee, E. G., Ahmad, R. C., Wheeler, M. T., Tsui, C., et al. (2004). The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nature Immunology, 5, 1052-1060.
28. Lee, E. G., Boone, D. L., Chai, S., Libby, S. L., Chien, M., Lodolce, J. P., et al. (2000). Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science, 289, 2350-2354.
29. Kato, M., Sanada, M., Kato, I., Sato, Y., Takita, J., Takeuchi, K., et al. (2009). Frequent inactivation of A20 in B-cell lymphomas. Nature, 459, 712-716.
30. Lefkowitz, R. J. (1998). G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. Journal of Biological Chemistry, 273, 18677-18680.
31. Sorkin, A., & Von Zastrow, M. (2002). Signal transduction and endocytosis: Close encounters of many kinds. Nature Reviews Molecular Cell Biology, 3, 600-614.
32. Zastrow, O., Seidel, B., Kiess, W., Thiery, J., Keller, E., Bottner, A., et al. (2003). The soluble leptin receptor is crucial for leptin action: Evidence from clinical and experimental data. International Journal of Obesity and Related Metabolic Disorders, 27, 1472-1478.
33. Alwan, H. A., van Zoelen, E. J., & van Leeuwen, J. E. (2003). Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. Journal of Biological Chemistry, 278, 35781-35790.
34. Berlin, I., Higginbotham, K. M., Dise, R. S., Sierra, M. I., & Nash, P. D. (2010). The deubiquitinating enzyme USP8 promotes trafficking and degradation of the chemokine receptor CXCR4 at the sorting endosome. Journal of Biological Chemistry, 285, 37895-37908.
35. Berlin, I., Schwartz, H., & Nash, P. D. (2010) Regulation of the epidermal growth factor receptor ubiquitination and trafficking by the USP8/STAM complex. Journal of Biological Chemistry, 285, 34909-34921.
36. de Melker, A. A., van der Horst, G., Calafat, J., Jansen, H., & Borst, J. (2001). c-Cbl ubiquitinates the EGF receptor at the plasma membrane and remains receptor associated throughout the endocytic route. Journal of Cell Science, 114, 2167-2178.
37. Marchese, A., & Benovic, J. L. (2001). Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. Journal of Biological Chemistry, 276, 45509-45512.
38. Sierra, M. I., Wright, M. H., & Nash, P. D. (2010). AMSH interacts with ESCRT-0 to regulate the stability and trafficking of CXCR4. Journal of Biological Chemistry, 285, 13990-14004.
39. Fader, C. M., & Colombo, M. I. (2009). Autophagy and multivesicular bodies: Two closely related partners. Cell Death and Differentiation, 16, 70-78.
40. Im, Y. J., Wollert, T., Boura, E., & Hurley, J. H. (2009). Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis. Developmental Cell, 17, 234-243.
41. Katzmann, D. J. (2006). No ESCRT to the melanosome: MVB sorting without ubiquitin. Developmental Cell, 10, 278-280.
42. Raiborg, C., & Stenmark, H. (2009). The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature, 458, 445-452.
43. Saksena, S., Sun, J., Chu, T., & Emr, S. D. (2007). ESCRTing proteins in the endocytic pathway. Trends in Biochemical Sciences, 32, 561-573.
44. McCullough, J., Row, P. E., Lorenzo, O., Doherty, M., Beynon, R., Clague, M. J., et al. (2006). Activation of the endosome-associated ubiquitin isopeptidase AMSH by STAM, a component of the multivesicular body-sorting machinery. Current Biology, 16, 160-165.
45. Row, P. E., Liu, H., Hayes, S., Welchman, R., Charalabous, P., Hofmann, K., et al. (2007). The MIT domain of UBPY constitutes a CHMP binding and endosomal localisation signal required for efficient EGF receptor degradation. Journal of Biological Chemistry, 282, 30929-30937.
46. Tsang, H. T., Connell, J. W., Brown, S. E., Thompson, A., Reid, E., & Sanderson, C. M. (2006). A systematic analysis of human CHMP protein interactions: Additional MIT domain-containing proteins bind to multiple components of the human ESCRT III complex. Genomics, 88, 333-346.
47. McCullough, J., Clague, M. J., & Urbe, S. (2004). AMSH is an endosome-associated ubiquitin isopeptidase. Journal of Cell Biology, 166, 487-492.
48. Jin, L., Williamson, A., Banerjee, S., Philipp, I., & Rape, M. (2008). Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell, 133, 653-665.
49. Kerscher, O., Felberbaum, R., & Hochstrasser, M. (2006). Modification of proteins by ubiquitin and ubiquitin-like proteins. Annual Review of Cell and Developmental Biology, 22, 159-180.
50. Komada, M. (2008). Controlling receptor downregulation by ubiquitination and deubiquitination. Current Drug Discovery Technologies, 5, 78-84.
51. Song, L., & Rape, M. (2008). Reverse the curse-the role of deubiquitination in cell cycle control. Current Opinion in Cell Biology, 20, 156-163.
52. Williams, R. L., & Urbe, S. (2007). The emerging shape of the ESCRT machinery. Nature Reviews Molecular Cell Biology, 8, 355-368.
53. Naviglio, S., Mattecucci, C., Matoskova, B., Nagase, T., Nomura, N., Di Fiore, P. P., et al. (1998). UBPY: A growth-regulated human ubiquitin isopeptidase. EMBO Journal, 17, 3241-3250.
54. Niendorf, S., Oksche, A., Kisser, A., Lohler, J., Prinz, M., Schorle, H., et al. (2007). Essential role of ubiquitin-specific protease 8 for receptor tyrosine kinase stability and endocytic trafficking in vivo. Molecular and Cellular Biology, 27, 5029-5039.
55. Hasdemir, B., Murphy, J. E., Cottrell, G. S., & Bunnett, N. W. (2009). Endosomal deubiquitinating enzymes control ubiquitination and down-regulation of protease-activated receptor 2. Journal of Biological Chemistry, 284, 28453-28466.
56. Hislop, J. N., Henry, A. G., Marchese, A., & von Zastrow, M. (2009). Ubiquitination regulates proteolytic processing of G protein-coupled receptors after their sorting to lysosomes. Journal of Biological Chemistry, 284, 19361-19370.
57. Alwan, H. A., & van Leeuwen, J. E. (2007). UBPY-mediated epidermal growth factor receptor (EGFR) de-ubiquitination promotes EGFR degradation. Journal of Biological Chemistry, 282, 1658-1669.
58. Sierra, M. I., Wright, M. H., & Nash, P. (2010). AMSH interacts with ESCRT-0 to regulate the stability and trafficking of CXCR4. Journal of Biological Chemistry, 285(18), 13990-14004.
59. Nakamura, M., Tanaka, N., Kitamura, N., & Komada, M. (2006). Clathrin anchors deubiquitinating enzymes, AMSH and AMSH-like protein, on early endosomes. Genes Cells, 11, 593-606.
60. Row, P. E., Prior, I. A., McCullough, J., Clague, M. J., & Urbe, S. (2006). The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. Journal of Biological Chemistry, 281, 12618-12624.
61. Raiborg, C., Bache, K. G., Mehlum, A., Stang, E., & Stenmark, H. (2001). Hrs recruits clathrin to early endosomes. EMBO Journal, 20, 5008-5021.
62. Berry, D. M., Nash, P., Liu, S. K., Pawson, T., & McGlade, C. J. (2002). A high-affinity Arg-X-X-Lys SH3 binding motif confers specificity for the interaction between Gads and SLP-76 in T cell signaling. Current Biology, 12, 1336-1341.
63. Bjorkoy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., et al. (2005). p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. Journal of Cell Biology, 171, 603-614.
64. Nixon, R. A., & Cataldo, A. M. (2006). Lysosomal system pathways: Genes to neurodegeneration in Alzheimer's disease. J Alzheimers Dis, 9, 277-289.
65. Mizuno, E., Kobayashi, K., Yamamoto, A., Kitamura, N., & Komada, M. (2006). A deubiquitinating enzyme UBPY regulates the level of protein ubiquitination on endosomes. Traffic, 7, 1017-1031.
66. Agromayor, M., & Martin-Serrano, J. (2006). Interaction of AMSH with ESCRT-III and deubiquitination of endosomal cargo. Journal of Biological Chemistry, 281, 23083-23091.
67. Lata, S., Roessle, M., Solomons, J., Jamin, M., Gottlinger, H. G., Svergun, D. I., et al. (2008). Structural basis for autoinhibition of ESCRT-III CHMP3. Journal of Molecular Biology, 378, 818-827.
68. Avvakumov, G. V., Walker, J. R., Xue, S., Finerty, P. J., Jr., Mackenzie, F., Newman, E. M., et al. (2006). Amino-terminal dimerization, NRDP1-rhodanese interaction, and inhibited catalytic domain conformation of the ubiquitin-specific protease 8 (USP8). Journal of Biological Chemistry, 281, 38061-38070.
69. Clague, M. J., & Urbe, S. (2006). Endocytosis: The DUB version. Trends in Cell Biology, 16, 551-559.
70. Carlton, J. G., & Martin-Serrano, J. (2007). Parallels between cytokinesis and retroviral budding: A role for the ESCRT machinery. Science, 316, 1908-1912.
71. Morita, E., Sandrin, V., Chung, H. Y., Morham, S. G., Gygi, S. P., Rodesch, C. K., et al. (2007). Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO Journal, 26, 4215-4227.
72. Mukai, A., Mizuno, E., Kobayashi, K., Matsumoto, M., Nakayama, K. I., Kitamura, N., et al. (2008). Dynamic regulation of ubiquitylation and deubiquitylation at the central spindle during cytokinesis. Journal of Cell Science, 121, 1325-1333.
73. Tanaka, N., Kaneko, K., Asao, H., Kasai, H., Endo, Y., Fujita, T., et al. (1999). Possible involvement of a novel STAM-associated molecule "AMSH" in intracellular signal transduction mediated by cytokines. Journal of Biological Chemistry, 274, 19129-19135.
74. Mizuno, E., Kitamura, N., & Komada, M. (2007). 14-3-3-dependent inhibition of the deubiquitinating activity of UBPY and its cancellation in the M phase. Experimental Cell Research, 313, 3624-3634.
75. Meijer, I. M., & van Leeuwen, J. E. (2011). ERBB2 is a target for USP8-mediated deubiquitination. Cellular Signalling, 23, 458-467.
76. Rusten, T. E., Filimonenko, M., Rodahl, L. M., Stenmark, H., & Simonsen, A. (2007). ESCRTing autophagic clearance of aggregating proteins. Autophagy, 2007, 4.
77. Levine, B., Sinha, S., & Kroemer, G. (2008). Bcl-2 family members: Dual regulators of apoptosis and autophagy. Autophagy, 4, 600-606.
78. Filimonenko, M., Stuffers, S., Raiborg, C., Yamamoto, A., Malerod, L., Fisher, E. M., et al. (2007). Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. Journal of Cell Biology, 179, 485-500.
79. Lee, J. A., Beigneux, A., Ahmad, S. T., Young, S. G., & Gao, F. B. (2007). ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Current Biology, 17, 1561-1567.