Specific and Covalent Targeting of Conjugating and Deconjugating Enzymes of Ubiquitin-Like Proteins

Molecular and Cellular Biology

Volumn 24, Issue 1, 2004, Pages 84-95

  Hemelaar, Joris ^a   Borodovsky, Anna ^a   Kessler, Benedikt M ^a   Reverter, David ^b   Cook, Julie ^a   Kolli, Nagamallesawari ^c   Gan Erdene, Tudev ^c   Wilkinson, Keith D ^c   Gill, Grace ^a   Lima, Christopher D ^b   Ploegh, Hidde L ^a   Ovaa, Huib ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROLASE; POLYPEPTIDE; SUMO 1 PROTEIN; UBIQUITIN;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; CONJUGATION; COVALENT BOND; ENZYME MODIFICATION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME SUBUNIT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; STEM CELL; TISSUE SPECIFICITY;

ANIMALS; ENDOPEPTIDASES; ENZYMES; MICE; MOLECULAR PROBES; SULFONES; SUMO-1 PROTEIN; UBIQUITINS;

ANIMALIA; ESCHERICHIA COLI;

EID: 10744227299     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.1.84-95.2004     Document Type: Article

References (74)

1. Amerik, A., S. Swaminathan, B. A. Krantz, K. D. Wilkinson, and M. Hochstrasser. 1997. In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome. EMBO J. 16:4826-4838.
2. Balakirev, M. Y., S. O. Tcherniuk, M. Jaquinod, and J. Chroboczek. 2003. Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep. 4:517-522.
3. Bayer, P., A. Arndt, S. Metzger, R. Mahajan, F. Melchior, R. Jaenicke, and J. Becker. 1998. Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 280:275-286.
4. Bernier-Villamor, V., D. A. Sampson, M. J. Matunis, and C. D. Lima. 2002. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108:345-356.
5. Best, J. L., S. Ganiatsas, S. Agarwal, A. Changou, P. Salomoni, O. Shirihai, P. B. Meluh, P. P. Pandolfi, and L. I. Zon. 2002. SUMO-1 protease-1 regulates gene transcription through PML. Mol. Cell 10:843-855.
6. Bogyo, M., S. Shin, J. S. McMaster, and H. L. Ploegh. 1998. Substrate binding and sequence preference of the proteasome revealed by active-site-directed affinity probes. Chem. Biol. 5:307-320.
7. Borodovsky, A., B. M. Kessler, R. Casagrande, H. S. Overkleeft, K. D. Wilkinson, and H. L. Ploegh. 2001. A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14. EMBO J. 20:5187-5196.
8. Borodovsky, A., H. Ovaa, N. Kolli, T. Gan-Erdene, K. D. Wilkinson, H. L. Ploegh, and B. M. Kessler. 2002. Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 9:1149-1159.
9. Cope, G. A., G. S. Suh, L. Aravind, S. E. Schwarz, S. L. Zipursky, E. V. Koonin, and R. J. Deshaies. 2002. Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 298:608-611.
10. Desterro, J. M., M. S. Rodriguez, and R. T. Hay. 1998. SUMO-I modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell 2:233-239.
11. Desterro, J. M., M. S. Rodriguez, G. D. Kemp, and R. T. Hay. 1999. Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem. 274:10618-10624.
12. Dohmen, R. J., R. Stappen, J. P. McGrath, H. Forrova, J. Kolarov, A. Goffeau, and A. Varshavsky. 1995. An essential yeast gene encoding a homolog of ubiquitin-activating enzyme. J. Biol. Chem. 270:18099-18109.
13. Evans, P. C., T. S. Smith, M. J. Lai, M. G. Williams, D. F. Burke, K. Heyninck, M. M. Kreike, R. Beyaert, T. L. Blundell, and P. J. Kilshaw. 2003. A novel type of deubiquitinating enzyme. J. Biol. Chem. 278:23180-23186.
14. Gan-Erdene, T., N. Kolli, L. Yin, K. Wu, Z. Q. Pan, and K. D. Wilkinson. 2003. Identification and characterization of DEN1, a deneddylase of the ULP family. J. Biol. Chem. 278:28892-28900.
15. Gong, L., T. Kamitani, S. Millas, and E. T. Yeh. 2000. Identification of a novel isopeptidase with dual specificity for ubiquitin- and NEDD8-conjugated proteins. J. Biol. Chem. 275:14212-14216.
16. Gong, L., B. Li, S. Millas, and E. T. Yeh. 1999. Molecular cloning and characterization of human AOS1 and UBA2, components of the sentrin-activating enzyme complex. FEBS Lett. 448:185-189.
17. Gong, L., S. Millas, G. G. Maul, and E. T. Yeh. 2000. Differential regulation of sentrinized proteins by a novel sentrin-specific protease. J. Biol. Chem. 275:3355-3359.
18. Gong, L., and E. T. Yeh. 1999. Identification of the activating and conjugating enzymes of the NEDD8 conjugation pathway. J. Biol. Chem. 274:12036-12042.
19. Haas, A. L., P. Ahrens, P. M. Bright, and H. Ankel. 1987. Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J. Biol. Chem. 262:11315-11323.
20. Hadari, T., J. V. Warms, I. A. Rose, and A. Hershko. 1992. A ubiquitin C-terminal isopeptidase that acts on polyubiquitin chains. Role in protein degradation. J. Biol. Chem. 267:719-727.
21. Hamerman, J. A., F. Hayashi, L. A. Schroeder, S. P. Gygi, A. L. Haas, L. Hampson, P. Coughlin, R. Aebersold, and A. Aderem. 2002. Serpin 2a is induced in activated macrophages and conjugates to a ubiquitin homolog. J. Immunol. 168:2415-2423.
22. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
23. Hoege, C., B. Pfander, G. L. Moldovan, G. Pyrowolakis, and S. Jentsch. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141.
24. Hori, T., F. Osaka, T. Chiba, C. Miyamoto, K. Okabayashi, N. Shimbara, S. Kato, and K. Tanaka. 1999. Covalent modification of all members of human cullin family proteins by NEDD8. Oncogene 18:6829-6834.
25. Hu, M., P. Li, M. Li, W. Li, T. Yao, J. W. Wu, W. Gu, R. E. Cohen, and Y. Shi. 2002. Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 111:1041-1054.
26. Jentsch, S., and G. Pyrowolakis. 2000. Ubiquitin and its kin: how close are the family ties? Trends Cell Biol. 10:335-342.
27. Johnson, E. S., and G. Blobel. 1997. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 272:26799-26802.
28. Johnson, E. S., and A. A. Gupta. 2001. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106:735-744.
29. Johnson, E. S., I. Schwienhorst, R. J. Dohmen, and G. Blobel. 1997. The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J. 16:5509-5519.
30. Johnston, S. C., S. M. Riddle, R. E. Cohen, and C. P. Hill. 1999. Structural basis for the specificity of ubiquitin C-terminal hydrolases. EMBO J. 18:3877-3887.
31. Kadoya, T., H. Yamamoto, T. Suzuki, A. Yukita, A. Fukui, T. Michiue, T. Asahara, K. Tanaka, M. Asashima, and A. Kikuchi. 2002. Desumoylation activity of axam, a novel axin-binding protein, is involved in downregulation of beta-catenin. Mol. Cell. Biol. 22:3803-3819.
32. Kamura, T., M. N. Conrad, Q. Yan, R. C. Conaway, and J. W. Conaway. 1999. The Rbx1 subunit of SCF and VHL E3 ubiquitin ligase activates Rubl modification of cullins Cdc53 and Cul2. Genes Dev. 13:2928-2933.
33. Kawakami, T., T. Chiba, T. Suzuki, K. Iwai, K. Yamanaka, N. Minato, H. Suzuki, N. Shimbara, Y. Hidaka, F. Osaka, M. Omata, and K. Tanaka. 2001. NEDD8 recruits E2-ubiquitin to SCF E3 ligase. EMBO J. 20:4003-4012.
34. Kim, K. I., S. H. Baek, Y. J. Jeon, S. Nishimori, T. Suzuki, S. Uchida, N. Shimbara, H. Saitoh, K. Tanaka, and C. H. Chung. 2000. A new SUMO-1-specific protease, SUSP1, that is highly expressed in reproductive organs. J. Biol. Chem. 275:14102-14106.
35. Kurz, T., L. Pintard, J. H. Willis, D. R. Hamill, P. Gonczy, M. Peter, and B. Bowerman. 2002. Cytoskeletal regulation by the Nedd8 ubiquitin-like protein modification pathway. Science 295:1294-1298.
36. Larsen, C. N., J. S. Price, and K. D. Wilkinson. 1996. Substrate binding and catalysis by ubiquitin C-terminal hydrolases: identification of two active site residues. Biochemistry 35:6735-6744.
37. Li, S. J., and M. Hochstrasser. 1999. A new protease required for cell-cycle progression in yeast. Nature 398:246-251.
38. Liakopoulos, D., G. Doenges, K. Matuschewski, and S. Jentsch. 1998. A novel protein modification pathway related to the ubiquitin system. EMBO J. 17:2208-2214.
39. Loeb, K. R., and A. L. Haas. 1994. Conjugates of ubiquitin cross-reactive protein distribute in a cytoskeletal pattern. Mol. Cell. Biol. 14:8408-8419.
40. Malakhov, M. P., K. I. Kim, O. A. Malakhova, B. S. Jacobs, E. C. Borden, and D. E. Zhang. 2003. High-throughput immunoblotting. Ubiquitin-like protein ISG15 modifies key regulators of signal transduction. J. Biol. Chem. 278:16608-16613.
41. Malakhov, M. P., O. A. Malakhova, K. I. Kim, K. J. Ritchie, and D. E. Zhang. 2002. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J. Biol. Chem. 277:9976-9981.
42. Malakhova, O. A., M. Yan, M. P. Malakhov, Y. Yuan, K. J. Ritchie, K. I. Kim, L. F. Peterson, K. Shuai, and D. E. Zhang. 2003. Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev. 17:455-460.
43. Mendoza, H. M., L. N. Shen, C. Botting, A. Lewis, J. Chen, B. Ink, and R. T. Hay. 2003. NEDP1, a highly conserved cysteine protease that deNEDDylates Cullins. J. Biol. Chem. 278:25637-25643.
44. Miyauchi, Y., S. Yogosawa, R. Honda, T. Nishida, and H. Yasuda. 2002. Sumoylation of Mdm2 by protein inhibitor of activated STAT (PIAS) and RanBP2 enzymes. J. Biol. Chem. 277:50131-50136.
45. Mizushima, N., T. Yoshimori, and Y. Ohsumi. 2002. Mouse Apg10 as an Apg12-conjugating enzyme: analysis by the conjugation-mediated yeast two-hybrid method. FEBS Lett. 532:450-454.
46. Mossessova, E., and C. D. Lima. 2000. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5:865-876.
47. Muller, S., C. Hoege, G. Pyrowolakis, and S. Jentsch. 2001. SUMO, ubiquitin's mysterious cousin. Nat. Rev. Mol. Cell. Biol. 2:202-210.
48. Nakagawa, K., and H. Yokosawa. 2002. PIAS3 induces SUMO-1 modification and transcriptional repression of IRF-1. FEBS Lett. 530:204-208.
49. Nishida, T., F. Kaneko, M. Kitagawa, and H. Yasuda. 2001. Characterization of a novel mammalian SUMO-1/Smt3-specific isopeptidase, a homologue of rat axam, which is an axin-binding protein promoting beta-catenin degradation. J. Biol. Chem. 276:39060-39066.
50. Nishida, T., H. Tanaka, and H. Yasuda. 2000. A novel mammalian Smt3-specific isopeptidase 1 (SMT3IP1) localized in the nucleolus at interphase. Eur. J. Biochem. 267:6423-6427.
51. Pichler, A., A. Gast, J. S. Seeler, A. Dejean, and F. Melchior. 2002. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108:109-120.
52. Potter, J. L., J. Narasimhan, L. Mende-Mueller, and A. L. Haas. 1999. Precursor processing of pro-ISG15/UCRP, an interferon-beta-induced ubiquitin-like protein. J. Biol. Chem. 274:25061-25068.
53. Pru, J. K., K. J. Austin, A. L. Haas, and T. R. Hansen. 2001. Pregnancy and interferon-tau upregulate gene expression of members of the 1-8 family in the bovine uterus. Biol. Reprod. 65:1471-1480.
54. Raasi, S., G. Schmidtke, and M. Groettrup. 2001. The ubiquitin-like protein FAT10 forms covalent conjugates and induces apoptosis. J. Biol. Chem. 276:35334-35343.
55. Ritchie, K. J., M. P. Malakhov, C. J. Hetherington, L. Zhou, M. T. Little, O. A. Malakhova, J. C. Sipe, S. H. Orkin, and D. E. Zhang. 2002. Dysregulation of protein modification by ISG15 results in brain cell injury. Genes Dev. 16:2207-2212.
56. Ross, S., J. L. Best, L. I. Zon, and G. Gill. 2002. SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol. Cell 10:831-842.
57. Sapetschnig, A., G. Rischitor, H. Braun, A. Doll, M. Schergaut, F. Melchior, and G. Suske. 2002. Transcription factor Sp3 is silenced through SUMO modification by PIAS1. EMBO J. 21:5206-5215.
58. Seufert, W., B. Futcher, and S. Jentsch. 1995. Role of a ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins. Nature 373:78-81.
59. Stein, R. L., Z. Chen, and F. Melandri. 1995. Kinetic studies of isopeptidase T: modulation of peptidase activity by ubiquitin. Biochemistry 34:12616-12623.
60. Suzuki, T., A. Ichiyama, H. Saitoh, T. Kawakami, M. Omata, C. H. Chung, M. Kimura, N. Shimbara, and K. Tanaka. 1999. A new 30-kDa ubiquitin-related SUMO-1 hydrolase from bovine brain. J. Biol. Chem. 274:31131-31134.
61. Tateishi, K., M. Omata, K. Tanaka, and T. Chiba. 2001. The NEDD8 system is essential for cell cycle progression and morphogenetic pathway in mice. J. Cell Biol. 155:571-579.
62. Tatham, M. H., E. Jaffray, O. A. Vaughan, J. M. Desterro, C. H. Botting, J. H. Naismith, and R. T. Hay. 2001. Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276:35368-35374.
63. Verma, R., L. Aravind, R. Oania, W. H. McDonald, J. R. Yates III, E. V. Koonin, and R. J. Deshaies. 2002. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298:611-615.
64. Wada, H., K. Kito, L. S. Caskey, E. T. Yeh, and T. Kamitani. 1998. Cleavage of the C-terminus of NEDD8 by UCH-L3. Biochem. Biophys. Res. Commun. 251:688-692.
65. Walden, H., M. S. Podgorski, and B. A. Schulman. 2003. Insights into the ubiquitin transfer cascade from the structure of the activating enzyme for NEDD8. Nature 422:330-334.
66. Whitby, F. G., G. Xia, C. M. Pickart, and C. P. Hill. 1998. Crystal structure of the human ubiquitin-like protein NEDD8 and interactions with ubiquitin pathway enzymes. J. Biol. Chem. 273:34983-34991.
67. Wilkinson, K. D. 1997. Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J. 11:1245-1256.
68. Wilkinson, K. D., K. M. Lee, S. Deshpande, P. Duerksen-Hughes, J. M. Boss, and J. Pohl. 1989. The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246:670-673.
69. Wilkinson, K. D., V. L. Tashayev, L. B. O'Connor, C. N. Larsen, E. Kasperek, and C. M. Pickart. 1995. Metabolism of the polyubiquitin degradation signal: structure, mechanism, and role of isopeptidase T. Biochemistry 34:14535-14546.
70. Wu, K., A. Chen, and Z. Q. Pan. 2000. Conjugation of Nedd8 to CUL1 enhances the ability of the ROC1-CUL1 complex to promote ubiquitin polymerization. J. Biol. Chem. 275:32317-32324.
71. Wu, K., K. Yamoah, G. Dolios, T. Gan-Erdene, P. Tan, A. Chen, C. G. Lee, N. Wei, K. D. Wilkinson, R. Wang, and Z. Q. Pan. 2003. DEN1 is a dual function protease capable of processing the C-terminus of Nedd8 deconjugating hyper-neddylated CUL1. J. Biol. Chem. 278:28882-28891.
72. Xu, M. Q., and T. C. Evans, Jr. 2001. Intein-mediated ligation and cyclization of expressed proteins. Methods 24:257-277.
73. Yeh, E. T., L. Gong, and T. Kamitani. 2000. Ubiquitin-like proteins: new wines in new bottles. Gene 248:1-14.
74. Zhang, H., H. Saitoh, and M. J. Matunis. 2002. Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex. Mol. Cell. Biol. 22:6498-6508.