Length of the active-site crossover loop defines the substrate specificity of ubiquitin C-terminal hydrolases for ubiquitin chains

Biochemical Journal

Volumn 441, Issue 1, 2012, Pages 143-149

  Zhou, Zi Ren ^a   Zhang, Yu Hang ^a   Liu, Shuai ^a   Song, Ai Xin ^a   Hu, Hong Yu ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

Active site crossover loop; BRCA1 (breast cancer early onset 1) associated protein 1 (BAP1); Ubiquitin C terminal hydrolase (UCH)

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; UBIQUITIN THIOLESTERASE;

ARTICLE; ATOM; CATALYSIS; CHEMICAL BOND; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SPECIFICITY; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

CATALYSIS; CATALYTIC DOMAIN; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; HYDROLYSIS; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN; UBIQUITIN THIOLESTERASE;

EID: 84055178186     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110699     Document Type: Article

References (44)

1. Hershko, A. and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479 (Pubitemid 28411135)
2. Ikeda, F. and Dikic, I. (2008) Atypical ubiquitin chains: new molecular signals. EMBO Rep. 9, 536-542
3. Clague, M. J. and Urbe, S. (2010) Ubiquitin: same molecule, different degradation pathways. Cell 143, 682-685
4. 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 (Pubitemid 41721026)
5. Katz, E. J., Isasa, M. and Crosas, B. (2010) A new map to understand deubiquitination. Biochem. Soc. Trans. 38, 21-28
6. Komander, D., Clague, M. J. and Urbé, S. (2009) Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550-563
7. Reyes-Turcu, F. E., Ventii, K. H. and Wilkinson, K. D. (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 78, 363-397
8. Amerik, A. Y. and Hochstrasser, M. (2004) Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695, 189-207 (Pubitemid 39574973)
9. Lam, Y. A., Xu, W., DeMartino, G. N. and Cohen, R. E. (1997) Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385, 737-740 (Pubitemid 27098096)
10. Larsen, C. N., Krantz, B. A. and Wilkinson, K. D. (1998) Substrate specificity of deubiquitinating enzymes: ubiquitin C-terminal hydrolases. Biochemistry 37, 3358-3368 (Pubitemid 28125563)
11. Doran, J. F., Jackson, P., Kynoch, P. A. and Thompson, R. J. (1983) Isolation of PGP 9.5, a new human neurone-specific protein detected by high-resolution two-dimensional electrophoresis. J. Neurochem. 40, 1542-1547 (Pubitemid 13106931)
12. Wilkinson, K. D., Lee, K. M., Deshpande, S., Duerksen-Hughes, P., Boss, J. M. and Pohl, J. (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246, 670-673 (Pubitemid 19283361)
13. Jensen, D. E., Proctor, M., Marquis, S. T., Gardner, H. P., Ha, S. I., Chodosh, L. A., Ishov, A. M., Tommerup, N., Vissing, H., Sekido, Y. et al. (1998) BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene 16, 1097-1112 (Pubitemid 28127509)
14. Luchansky, S. J., Lansbury, Jr, P. T. and Stein, R. L. (2006) Substrate recognition and catalysis by UCH-L1. Biochemistry 45, 14717-14725 (Pubitemid 44906987)
15. Case, A. and Stein, R. L. (2006) Mechanistic studies of ubiquitin C-terminal hydrolase L1. Biochemistry 45, 2443-2452 (Pubitemid 43271345)
16. Li, T., Naqvi, N. I., Yang, H. and Teo, T. S. (2000) Identification of a 26S proteasome-associated UCH in fission yeast. Biochem. Biophys. Res. Commun. 272, 270-275 (Pubitemid 30444933)
17. Yao, T., Song, L., Xu, W., DeMartino, G. N., Florens, L., Swanson, S. K., Washburn, M. P., Conaway, R. C., Conaway, J. W. and Cohen, R. E. (2006) Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat. Cell Biol. 8, 994-1002 (Pubitemid 44314731)
18. DeMartino, G. N. and Slaughter, C. A. (1993) Regulatory proteins of the proteasome. Enzyme Protein 47, 314-324
19. Nishikawa, H., Wu, W., Koike, A., Kojima, R., Gomi, H., Fukuda, M. and Ohta, T. (2009) BRCA1-associated protein 1 interferes with BRCA1/BARD1 RING heterodimer activity. Cancer Res. 69, 111-119
20. Misaghi, S., Ottosen, S., Izrael-Tomasevic, A., Arnott, D., Lamkanfi, M., Lee, J., Liu, J., O'Rourke, K., Dixit, V. M. and Wilson, A. C. (2009) Association of C-terminal ubiquitin hydrolase BRCA1-associated protein 1 with cell cycle regulator host cell factor 1. Mol. Cell. Biol. 29, 2181-2192
21. Scheuermann, J. C., de Ayala Alonso, A. G., Oktaba, K., Ly-Hartig, N., McGinty, R. K., Fraterman, S., Wilm, M., Muir, T. W. and Muller, J. (2010) Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature 465, 243-247
22. Das, C., Hoang, Q. Q., Kreinbring, C. A., Luchansky, S. J., Meray, R. K., Ray, S. S., Lansbury, P. T., Ringe, D. and Petsko, G. A. (2006) Structural basis for conformational plasticity of the Parkinson's disease-associated ubiquitin hydrolase UCH-L1. Proc. Natl. Acad. Sci. U.S.A. 103, 4675-4680
23. Johnston, S. C., Larsen, C. N., Cook, W. J., Wilkinson, K. D. and Hill, C. P. (1997) Crystal structure of a deubiquitinating enzyme (human UCH-L3) at 1.8 Å resolution. EMBO J. 16, 3787-3796 (Pubitemid 27280994)
24. Nishio, K., Kim, S. W., Kawai, K., Mizushima, T., Yamane, T., Hamazaki, J., Murata, S., Tanaka, K. and Morimoto, Y. (2009) Crystal structure of the de-ubiquitinating enzyme UCH37 (human UCH-L5) catalytic domain. Biochem. Biophys. Res. Commun. 390, 855-860
25. Johnston, S. C., Riddle, S. M., Cohen, R. E. and Hill, C. P. (1999) Structural basis for the specificity of ubiquitin C-terminal hydrolases. EMBO J. 18, 3877-3887 (Pubitemid 29335841)
26. Popp, M. W., Artavanis-Tsakonas, K. and Ploegh, H. L. (2009) Substrate filtering by the active site crossover loop in UCHL3 revealed by sortagging and gain-of-function mutations. J. Biol. Chem. 284, 3593-3602
27. Kabuta, T., Furuta, A., Aoki, S., Furuta, K. and Wada, K. (2008) Aberrant interaction between Parkinson disease-associated mutant UCH-L1 and the lysosomal receptor for chaperone-mediated autophagy. J. Biol. Chem. 283, 23731-23738
28. Larsen, C. N., Price, J. S. and Wilkinson, K. D. (1996) Substrate binding and catalysis by ubiquitin C-terminal hydrolases: identification of two active site residues. Biochemistry 35, 6735-6744 (Pubitemid 26172432)
29. Qiu, X. B., Ouyang, S. Y., Li, C. J., Miao, S., Wang, L. and Goldberg, A. L. (2006) hRpn13/ADRM1/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37. EMBO J. 25, 5742-5753 (Pubitemid 44967758)
30. Raasi, S. and Pickart, C. M. (2005) Ubiquitin chain synthesis. Methods Mol. Biol. 301, 47-55
31. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
32. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C. and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
33. Emsley, P., Lohkamp, B., Scott, W. G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 486-501
34. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 213-221
35. Laskowski, R. A., MacArthur, M. W., Moss, D. S. and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
36. Eswar, N., Eramian, D., Webb, B., Shen, M. Y. and Sali, A. (2008) Protein structure modeling with MODELLER. Methods Mol. Biol. 426, 145-159
37. Machida, Y. J., Machida, Y., Vashisht, A. A., Wohlschlegel, J. A. and Dutta, A. (2009) The deubiquitinating enzyme BAP1 regulates cell growth via interaction with HCF-1. J. Biol. Chem. 284, 34179-34188
38. Misaghi, S., Galardy, P. J., Meester, W. J., Ovaa, H., Ploegh, H. L. and Gaudet, R. (2005) Structure of the ubiquitin hydrolase UCH-L3 complexed with a suicide substrate. J. Biol. Chem. 280, 1512-1520
39. Boudreaux, D. A., Maiti, T. K., Davies, C. W. and Das, C. (2010) Ubiquitin vinyl methyl ester binding orients the misaligned active site of the ubiquitin hydrolase UCHL1 into productive conformation. Proc. Natl. Acad. Sci. U.S.A. 107, 9117-9122
40. Lam, Y. A., DeMartino, G. N., Pickart, C. M. and Cohen, R. E. (1997) Specificity of the ubiquitin isopeptidase in the PA700 regulatory complex of 26 S proteasomes. J. Biol. Chem. 272, 28438-28446 (Pubitemid 27517791)
41. Hamazaki, J., Iemura, S., Natsume, T., Yashiroda, H., Tanaka, K. and Murata, S. (2006) A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J. 25, 4524-4536 (Pubitemid 44498126)
42. Jorgensen, J. P., Lauridsen, A. M., Kristensen, P., Dissing, K., Johnsen, A. H., Hendil, K. B. and Hartmann-Petersen, R. (2006) Adrm1, a putative cell adhesion regulating protein, is a novel proteasome-associated factor. J. Mol. Biol. 360, 1043-1052 (Pubitemid 44062521)
43. Yao, T., Song, L., Jin, J., Cai, Y., Takahashi, H., Swanson, S. K., Washburn, M. P., Florens, L., Conaway, R. C., Cohen, R. E. and Conaway, J. W. (2008) Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the Ino80 chromatin-remodeling complex. Mol. Cell 31, 909-917
44. Chen, X., Lee, B. H., Finley, D. and Walters, K. J. (2010) Structure of proteasome ubiquitin receptor hRpn13 and its activation by the scaffolding protein hRpn2. Mol. Cell 38, 404-415