Ubiquitin-binding domains

Nature Reviews Molecular Cell Biology

Volumn 6, Issue 8, 2005, Pages 610-621

  Hicke, Linda ^a   Schubert, Heidi L ^b   Hill, Christopher P ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; POLYUBIQUITIN ASSOCIATED ZINC FINGER; PROTEASOME; PROTEIN COUPLING OF UBIQUITIN CONJUGATION TO ENDOPLASMIC RETICULUM DEGRADATION; PROTEIN GAT; PROTEIN GRAM LIKE UBIQUITIN BINDING IN EAP45; PROTEIN NPL4 ZINC FINGER; PROTEIN UBA; PROTEIN UBIQUITIN CONJUGATING ENZYME VARIANT; PROTEIN UBIQUITIN INTERACTING MOTIF; PROTEIN VHS; RECEPTOR; UBIQUITIN; UBIQUITIN RECEPTOR; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

BINDING AFFINITY; BINDING SITE; COVALENT BOND; ENDOCYTOSIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

CARRIER PROTEINS; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; UBIQUITIN;

EID: 23144452091     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1701     Document Type: Review

References (104)

1. Kuriyan, J. & Cowburn, D. Modular peptide recognition domains in eukaryotic signaling. Annu. Rev. Biophys. Biomol. Struct. 26, 259-288 (1997).
2. Pawson, T. & Nash, P. Assembly of cell regulatory systems through protein interaction domains. Science 300, 445-452 (2003).
3. Weissman, A. Themes and variations on ubiquitylation. Nature Rev. Mol. Cell Biol. 2, 169-178 (2001).
4. Pickart, C. M. & Eddins, M. J. Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 1695, 55-72 (2004).
5. Hershko, A. & Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 67, 425-479 (1998).
6. Hicke, L. & Dunn, R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172 (2003).
7. DiAntonio, A. & Hicke, L. Ubiquitin-dependent regulation of the synapse. Annu. Rev. Neurosci. 27, 223-246 (2004).
8. Liu, Y. C. Ubiquitin ligases and the immune response. Annu. Rev. Immunol. 22, 81-127 (2004).
9. Muratani, M. & Tansey, W. P. How the ubiquitin-proteasome system controls transcription. Nature Rev. Mol. Cell Biol. 4, 192-201 (2003).
10. Sun, L. & Chen, Z. J. The novel functions of ubiquitination in signaling. Curr. Opin. Cell Biol. 16, 119-126 (2004).
11. Young, P., Deveraux, Q., Seal, R. E., Pickart, C. M. & Rechsteiner, M. Characterization of two polyubiquitin binding sites in the 26 S protease subunit 5a. J. Biol. Chem. 273, 5461-5467 (1998). Describes the first Identification and definition of a ubiquitin-binding domain, the sequence in the S5a subunit of the proteasome, which provided the basis for the UIM.
12. Hofmann, K. & Falquet, L. A ubiquitin-interacting motif conserved in components of the proteasomal and tysosomal protein degradation systems. Trends Biochem. Sci. 26, 347-350 (2001). The results of a bioinformatics approach that was based on the proteasomal S5a ubiquitin-binding sequence and resulted in the identification of the UIM.
13. Donaldson, K. M. et al. Ubiquitin-mediated sequestration of normal cellular proteins into polyglutamine aggregates. Proc. Natl Acad. Sci. USA 100, 8892-8897 (2003).
14. Bilodeau, P. S., Urbanowski, J. L., Winistorfer, S. C. & Piper, R. C. The Vps27p-Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nature Cell Biol. 4, 534-539 (2002).
15. Polo, S. et al. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416, 451-455 (2002). Shows a link between UIMs and the monoubiquitylation of proteins that contain them.
16. Raiborg, C. et al. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nature Cell Biol. 4, 394-398 (2002).
17. Shih, S. C. et al. Epsins and Vps27/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nature Cell Biol. 4, 389-393 (2002).
18. Hofmann, K. & Bucher, P. The UBA domain: a sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends Biochem. Sci. 21, 172-173 (1996).
19. Bertolaet, B. L. et al. UBA domains of DNA damage-inducible proteins interact with ubiquitin. Nature Struct. Biol. 8, 417-422 (2001).
20. Wilkinson, C. R. et al. Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nature Cell Biol. 3, 939-943 (2001).
21. Donaldson, K. M., Yin, H., Gekakis, N., Supek, F. & Joazeiro, C. A. Ubiquitin signals protein trafficking via interaction with a novel ubiquitin binding domain in the membrane fusion regulator, Vps9p. Curr. Biol. 13, 258-262 (2003).
22. Shih, S. C. et al. A ubiquitin-binding motif required for intramolecular ubiquitylation, the CUE domain. EMBO J. 22, 1273-1281 (2003).
23. Hook, S. S., Orian, A., Cowley, S. M. & Eisenman, R. N. Histone deacetylase 6 binds polyubiquitin through its zinc finger (PAZ domain) and copurifies with deubiquitinating enzymes. Proc. Natl Acad. Sci. USA 99, 13425-13430 (2002).
24. Yamakami, M., Yoshimori, T. & Yokosawa, H. Tom1, a VHS domain-containing protein, interacts with Tollip, ubiquitin, and clathrin. J. Biol. Chem. 278, 52865-52872 (2003).
25. Scott, P. M. et al. GGA proteins bind ubiquitin to facilitate sorting at the trans-Golgi network. Nature Cell Biol. 6, 252-259 (2004).
26. Shiba, Y. et al. GAT (GGA and Tom1) domain responsible for ubiquitin binding and ubiquitination. J. Biol. Chem. 279, 7105-7111 (2004).
27. Seigneurin-Berny, D. et al. Identification of components of the murine histone deacetylase 6 complex: link between acetylation and ubiquitination signaling pathways. Mol. Cell. Biol. 21, 8035-8044 (2001).
28. Meyer, H. H., Wang, Y. & Warren, G. Direct binding of ubiquitin conjugates by the mammalian p97 adaptor complexes, p47 and Ufd1-Npl4. EMBO J. 21, 5645-5652 (2002).
29. Kanayama, A. et al. TAB2 and TAB3 activate the NF-κB pathway through binding to polyubiquitin chains. Mol. Cell 15, 535-548 (2004).
30. Mizuno, E., Kawahata, K., Kato, M., Kitamura, N. & Komada, M. STAM proteins bind ubiquitinated proteins on the early endosome via the VHS domain and ubiquitin-interacting motif. Mol. Biol. Cell 14, 3675-3689 (2003).
31. Slagsvold, T. et al. Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J. Biol. Chem. 280, 19600-19606 (2005).
32. Fisher, R. D. et al. Structure and ubiquitin binding of the ubiquitin-interacting motif. J. Biol. Chem. 278, 28976-28984 (2003).
33. Alam, S. L. et al. Ubiquitin interactions of NZF zinc fingers. EMBO J. 23, 1411-1421 (2004).
34. Davies, G. C. et al. Cbl-b interacts with ubiquitinated proteins; differential functions of the UBA domains of c-Cbl and Cbl-b. Oncogene 23, 7104-7115 (2004).
35. Miller, S. L., Malotky, E. & O'Bryan, J. P. Analysis of the role of ubiquitin-interacting motifs (UIMs) in ubiquitin binding and ubiquitylation. J. Biol. Chem. 279, 33528-33537 (2004).
36. Walters, K. J., Lech, P. J., Goh, A. M., Wang, Q. & Howley, P. M. DNA-repair protein hHR23a alters its protein structure upon binding proteasomal subunit S5a. Proc. Natl Acad. Sci. USA 100, 12694-12699 (2003).
37. Tanaka, T., Kawashima, H., Yeh, E. T. & Kamitani, T. Regulation of the NEDD8 conjugation system by a splicing variant, NUB1L J. Biol. Chem. 278, 32905-32913 (2003).
38. Raasi, S., Orlov, I., Fleming, K. G. & Pickart, C. M. Binding of polyubiquitin chains to ubiquitin-associated (UBA) domains of HHR23A. J. Mol. Biol. 341, 1367-1379 (2004).
39. Seibenhener, M. L. et al. Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol. Cell. Biol. 24, 8055-8068 (2004).
40. Elsasser, S. & Finley, D. Delivery of ubiquitin conjugates to protein-unfolding machines. Nature Cell Biol. (in the press).
41. Katoh, Y. et al. Tollip and Tom1 form a complex and recruit ubiquitin-conjugated proteins onto early endosomes. J. Biol. Chem. 279, 24435-24443 (2004).
42. Kang, R. S. et al. Solution structure of a CUE-ubiquitin complex reveals a conserved mode of ubiquitin-binding. Cell 113, 621-630 (2003).
43. Swanson, K. A., Kang, R. S., Stamenova, S. D., Hicke, L. & Radhakrishnan, I. Solution structure of Vps27 UIM-ubiquitin complex important for endosomal sorting and receptor downregulation. EMBO J. 22, 4597-4606 (2003).
44. de Beer, T., Carter, R. E., Lobel-Rice, K. E., Sorkin, A. & Overduin, M. Structure and Asn-Pro-Phe binding pocket of the Eps15 homology domain. Science 281, 1357-1360 (1998).
45. Yamabhai, M. et al. Intersectin, a novel adaptor protein with two Eps15 homology and five Src homology 3 domains. J. Biol. Chem. 273, 31401-31407 (1998).
46. Miele, A. E., Watson, P. J., Evans, P. R., Traub, L. M. & Owen, D. J. Two distinct interaction motifs in amphiphysin bind two independent sites on the clathrin terminal domain β-propeller. Nature Struct. Mol. Biol. 11, 242-248 (2004).
47. Praefcke, G. J. et al. Evolving nature of the AP2 α-appendage hub during clathrin-coated vesicle endocytosis. EMBO J. 23, 4371-4383 (2004).
48. Katzmann, D. J., Babst, M. & Emr, S. D. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal sorting complex, ESCRT-I. Cell 106, 145-155 (2001).
49. Lim, W. A. The modular logic of signaling proteins: building allosteric switches from simple binding domains. Curr. Opin. Struct. Biol. 12, 61-68 (2002).
50. Haas, A. L. & Bright, P. M. The immunochemical detection and quantitation of intracellular ubiquitin-protein conjugates. J. Biol. Chem. 260, 12464-12473 (1985).
51. Pomillos, O. et al. Structure and functional interactions of the Tsg101 UEV domain. EMBO J. 21, 2397-2406 (2002).
52. Hu, M. et al. Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 111, 1041-1054 (2002).
53. Yuan, X. et al. Structure, dynamics and interactions of p47, a major adaptor of the AAA ATPase, p97. EMBO J. 23, 1463-1473 (2004).
54. Withers-Ward, E. S., Mueller, T. D., Chen, I. S. & Feigon, J. Biochemical and structural analysis of the interaction between the UBA(2) domain of the DNA repair protein HHR23A and HIV-1 Vpr. Biochemistry 39, 14103-14112 (2000).
55. Bertolaet, B. L. et al. UBA domains mediate protein-protein interactions between two DNA damage-inducible proteins. J. Mol. Biol. 313, 955-963 (2001).
56. Ohno, A. et al. Structure of the UBA domain of Dsk2p in complex with ubiquitin: molecular determinants for ubiquitin recognition. Structure 13, 521-532 (2005).
57. Prag, G. et al. Mechanism of ubiquitin recognition by the CUE domain of Vps9p. Cell 113, 609-620 (2003).
58. Mueller, T. D., Kamionka, M. & Feigon, J. Specificity of the interaction between ubiquitin-associated domains and ubiquitin. J. Biol. Chem. 279, 11926-11936 (2004).
59. Sundquist, W. I. et al. Ubiquitin recognition by the human TSG101 protein. Mol. Cell 13, 783-789 (2004).
60. Teo, H., Veprintsev, D. B. & Williams, R. L. Structural insights into endosomal sorting complex required for transport (ESCRT-I) recognition of ubiquitinated proteins. J. Biol. Chem. 279, 28689-28696 (2004).
61. VanDemark, A. P., Hofmann, R. M., Tsui, C., Pickart, C. M. & Wolberger, C. Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer. Cell 105, 711-720 (2001).
62. McKenna, S. et al. An NMR-based model of the ubiquitin-bound human ubiquitin conjugation complex Mms2-Ubc13: the structural basis for lysine 63 chain catalysis. J. Biol. Chem. 278, 13151-13158 (2003).
63. Miura, T., Klaus, W., Gsell, B., Miyamoto, C. & Senn, H. Characterization of the binding interface between ubiquitin and class I human ubiquitin-conjugating enzyme 2b by multidimensional heteronuclear NMR spectroscopy in solution. J. Mol. Biol. 290, 213-228 (1999).
64. Hamilton, K. S. et al. Structure of a conjugating enzyme-ubiquitin thiolester intermediate reveals a novel role for the ubiquitin tail. Structure 9, 897-904 (2001).
65. Bilodeau, P. S., Winistorfer, S. C., Kearney, W. R., Robertson, A. D. & Piper, R. C. Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J. Cell Biol. 163, 237-243 (2003).
66. Johnston, S. C., Riddle, S. M., Cohen, R. E. & Hill, C. P. Structural basis for the specificity of ubiquitin C-terminal hydrolases. EMBO J. 18, 3877-3887 (1999).
67. Walden, H., Podgorski, M. S. & Schulman, B. A. Insights into the ubiquitin transfer cascade from the structure of the activating enzyme for NEDD8. Nature 422, 330-334 (2003).
68. Klapisz, E. et al. A ubiquitin-interacting motif (UIM) is essential for Eps15 and Eps15R ubiquitination. J. Biol. Chem. 277, 30746-30753 (2002).
69. Oldham, C. E., Mohney, R. P., Miller, S. L., Hanes, R. N. & O'Bryan, J. P. The ubiquitin-interacting motifs target the endocytic adaptor protein epsin for ubiquitination. Curr. Biol. 12, 1112-1116 (2002).
70. Davies, B. A. et al. Vps9p CUE domain ubiquitin binding is required for efficient endocytic protein traffic. J. Biol. Chem. 278, 19826-19833 (2003).
71. Katz, M. et al. Ligand-independent degradation of epidermal growth factor receptor involves receptor ubiquitylation and Hgs, an adaptor whose ubiquitin-interacting motif targets ubiquitylation by Nedd4. Traffic 3, 740-751 (2002).
72. Saito, T., Mitsui, K., Hamada, Y. & Tsurugi, K. Regulation of the Gts1p level by the ubiquitination system to maintain metabolic oscillations in the continuous culture of yeast. J. Biol. Chem. 277, 33624-33631 (2002).
73. Peng, J. et al. A proteomics approach to understanding protein ubiquitination. Nature Biotechnol. 21, 921-926 (2003).
74. Amit, I et al. Tal, a Tsg101 -specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding. Genes Dev. 18, 1737-1752 (2004).
75. Cdc4 complex. Genes Dev. 12, 914-926 (1998).
76. Magnifico, A. et al. WW domain HECT E3s target Cbl RING finger E3s for proteasomal degradation. J. Biol. Chem. 278, 43169-43177 (2003).
77. 2+-dependent decrease of protein ubiquitination at synapses. Proc. Natl Acad. Sci. USA 100, 14908-14913 (2003).
78. Chen, X., Zhang, B. & Fischer, J. A. A specific protein substrate for a deubiquitinating enzyme: Liquid facets is the substrate of Fat facets. Genes Dev. 16, 289-294 (2002).
79. Di Fiore, P. P., Polo, S. & Hofmann, K. When ubiquitin meets ubiquitin receptors: a signalling connection. Nature Rev. Mol. Cell Biol. 4, 491-497 (2003).
80. Elsasser, S., Chandler-Militello, D., Muller, B., Hanna, J. & Finley, D. Rad23 and Rpn10 serve as alternative ubiquitin receptors for the proteasome. J. Biol. Chem. 279, 26817-26822 (2004).
81. Verma, R., Oania, R., Graumann, J. & Deshaies, R. J. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 118, 99-110 (2004).
82. Deveraux, Q., Ustrell, V., Pickart, C. & Rechsteiner, M. A 26S protease subunit that binds ubiquitin conjugates. J. Biol. Chem. 289, 7059-7061 (1994).
83. Lam, Y. A., Lawson, T. G., Velayutham, M., Zweier, J. L. & Pickart, C. M. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 416, 763-767 (2002).
84. Schauber, C. et al. Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature 391, 715-718 (1998).
85. Puertollano, R. & Bonifacino, J. S. Interactions of GGA3 with the ubiquitin sorting machinery. Nature Cell Biol. 6, 244-251 (2004).
86. Katzmann, D. J., Odorizzi, G. & Emr, S. D. Receptor downregulation and multivesicular-body sorting. Nature Rev. Mol. Cell Biol. 3, 893-905 (2002).
87. Raiborg, C., Rusten, T. E. & Stenmark, H. Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15, 446-455 (2003).
88. Reggiori, F. & Pelham, H. R. Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J. 20, 5176-5186 (2001).
89. Dai, R. M. & Li, C. C. Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nature Cell Biol. 3, 740-744 (2001).
90. UFD1/NPL4, a ubiquitin-selective chaperone. Cell 107, 667-677 (2001).
91. Ye, Y., Meyer, H. H. & Rapoport, T. A. Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol. 162, 71-84 (2003).
92. Hannich, J. T. et al. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280, 4102-4110 (2005).
93. Song, J., Durrin, L. K., Wilkinson, T. A., Krontiris, T. G. & Chen, Y. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl Acad. Sci. USA 101, 14373-14378 (2004).
94. Takahashi, H., Hatakeyama, S., Saitoh, H. & Nakayama, K. I. Noncovalent SUMO-1 binding activity of thymine DNA glycosylase (TDG) is required for its SUMO-1 modification and colocalization with the promyelocytic leukemia protein. J. Biol. Chem. 280, 5611-5621 (2005).
95. Amerik, A. Y. & Hochstrasser, M. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695, 189-207 (2004).
96. Prag, G. et al. Structural mechanism for ubiquitinated-cargo recognition by the Golgi-localized, γ-ear-containing, ADP-ribosylation-factor-binding proteins. Proc. Natl Acad. Sci. USA 102, 2334-2339 (2005).
97. Ponting, C. P. Proteins of the endoplasmic-reticulum-associated degradation pathway: domain detection and function prediction. Biochem. J. 351, 527-535 (2000).
98. Bilodeau, P. S. et al. The GAT domains of clathrin-associated GGA proteins have two ubiquitin binding motifs. J. Biol. Chem. 279, 54808-54816 (2004).
99. Wang, B. et al. Structure and ubiquitin interactions of the conserved zinc finger domain of Npl4. J. Biol. Chem. 278, 20225-20234 (2003).
100. Mueller, T. D. & Feigon, J. Solution structures of UBA domains reveal a conserved hydrophobic surface for protein-protein interactions. J. Mol. Biol. 319, 1243-1255 (2002).
101. Chim, N. et al. Solution structure of the ubiquitin-binding domain in Swa2p from Saccharomyces cerevisiae. Proteins 54, 784-793 (2004).
102. Merkley, N. & Shaw, G. S. Solution structure of the flexible class II ubiquitin-conjugating enzyme Ubc1 provides insights for polyubiquitin chain assembly. J. Biol. Chem. 279, 47139-47147 (2004).
103. Shekhtman, A. & Cowburn, D. A ubiquitin-interacting motif from Hrs binds to and occludes the ubiquitin surface necessary for polyubiquitination in monoubiquitinated proteins. Biochem. Biophys. Res. Commun. 296, 1222-1227 (2002).
104. Cadwell, K. & Coscoy, L. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309, 127-130 (2005).