Crystal structure of the catalytic domain of UCHL5, a proteasome-associated human deubiquitinating enzyme, reveals an unproductive form of the enzyme

FEBS Journal

Volumn 278, Issue 24, 2011, Pages 4917-4926

  Maiti, Tushar K ^a   Permaul, Michelle ^a   Boudreaux, David A ^a   Mahanic, Christina ^a   Mauney, Sarah ^a   Das, Chittaranjan ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

deubiquitination; proteasome associated deubiquitinases; ubiquitin hydrolase; UCHL5; unproductive active site

Indexed keywords

ALANINE; CYSTEINE; CYSTEINE PROTEINASE; MUTANT PROTEIN; PROTEASOME; PROTEIN UCHL5; UBIQUITIN CARBOXY TERMINAL HYDROLASE L5 PROTEIN; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; UBIQUITINATION;

CARBOXYPEPTIDASES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; POLYUBIQUITIN; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN CONFORMATION;

EID: 82755187438     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08393.x     Document Type: Article

References (41)

1. Finley D, (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78, 477-513.
2. Goldberg AL, (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426, 895-899. (Pubitemid 38056882)
3. Glickman MH, &, Ciechanover A, (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82, 373-428. (Pubitemid 34654457)
4. Yao T, Song L, Xu W, DeMartino GN, Florens L, Swanson SK, Washburn MP, Conaway RC, Conaway JW, &, Cohen RE, (2006) Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat Cell Biol 8, 994-1002. (Pubitemid 44314731)
5. Stone M, Hartmann-Petersen R, Seeger M, Bech-Otschir D, Wallace M, &, Gordon C, (2004) Uch2/Uch37 is the major deubiquitinating enzyme associated with the 26S proteasome in fission yeast. J Mol Biol 344, 697-706. (Pubitemid 39469214)
6. Lee MJ, Lee BH, Hanna J, King RW, &, Finley D, (2011) Trimming of ubiquitin chains by proteasome-associated deubiquitinating enzymes. Mol Cell Proteomics 10, R110.003871.
7. Qiu XB, Ouyang SY, Li CJ, Miao S, Wang L, &, Goldberg AL, (2006) hRpn13/ADRM1/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37. EMBO J 25, 5742-5753. (Pubitemid 44967758)
8. Hamazaki J, Iemura S, Natsume T, Yashiroda H, Tanaka K, &, Murata S, (2006) A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J 25, 4524-4536. (Pubitemid 44498126)
9. Lam YA, Xu W, DeMartino GN, &, Cohen RE, (1997) Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385, 737-740. (Pubitemid 27098096)
10. Verma R, Aravind L, Oania R, McDonald WH, Yates JR III, Koonin EV, &, Deshaies RJ, (2002) Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611-615. (Pubitemid 35215317)
11. Koulich E, Li X, &, DeMartino GN, (2008) Relative structural and functional roles of multiple deubiquitylating proteins associated with mammalian 26S proteasome. Mol Biol Cell 19, 1072-1082. (Pubitemid 351481820)
12. Borodovsky A, Kessler BM, Casagrande R, Overkleeft HS, Wilkinson KD, &, Ploegh HL, (2001) A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14. EMBO J 20, 5187-5196. (Pubitemid 32910913)
13. Hu M, Li P, Song L, Jeffrey PD, Chenova TA, Wilkinson KD, Cohen RE, &, Shi Y, (2005) Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. EMBO J 24, 3747-3756. (Pubitemid 41581691)
14. Yao T, &, Cohen RE, (2002) A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419, 403-407.
15. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK, &, Bernards R, (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786. (Pubitemid 41721026)
16. Komander D, (2010) Mechanism, specificity and structure of the deubiquitinases. Subcell Biochem 54, 69-87.
17. Love KR, Catic A, Schlieker C, &, Ploegh HL, (2007) Mechanisms, biology and inhibitors of deubiquitinating enzymes. Nat Chem Biol 3, 697-705. (Pubitemid 47609116)
18. Wilkinson KD, (2009) DUBs at a glance. J Cell Sci 122, 2325-2329.
19. Johnston SC, Larsen CN, Cook WJ, Wilkinson KD, &, Hill CP, (1997) Crystal structure of a deubiquitinating enzyme (human UCH-L3) at 1.8 A resolution. EMBO J 16, 3787-3796. (Pubitemid 27280994)
20. Misaghi S, Galardy PJ, Meester WJ, Ovaa H, Ploegh HL, &, Gaudet R, (2005) Structure of the ubiquitin hydrolase UCH-L3 complexed with a suicide substrate. J Biol Chem 280, 1512-1520.
21. Larsen CN, Price JS, &, Wilkinson KD, (1996) Substrate binding and catalysis by ubiquitin C-terminal hydrolases: identification of two active site residues. Biochemistry 35, 6735-6744. (Pubitemid 26172432)
22. Popp MW, Artavanis-Tsakonas K, &, Ploegh HL, (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.
23. Das C, Hoang QQ, Kreinbring CA, Luchansky SJ, Meray RK, Ray SS, Lansbury PT, Ringe D, &, Petsko GA, (2006) Structural basis for conformational plasticity of the Parkinson's disease-associated ubiquitin hydrolase UCH-L1. Proc Natl Acad Sci USA 103, 4675-4680.
24. Boudreaux DA, Maiti TK, Davies CW, &, 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 USA 107, 9117-9122.
25. Johnston SC, Riddle SM, Cohen RE, &, Hill CP, (1999) Structural basis for the specificity of ubiquitin C-terminal hydrolases. EMBO J 18, 3877-3887. (Pubitemid 29335841)
26. Nishio K, Kim SW, Kawai K, Mizushima T, Yamane T, Hamazaki J, Murata S, Tanaka K, &, Morimoto Y, (2009) Crystal structure of the de-ubiquitinating enzyme UCH37 (human UCH-L5) catalytic domain. Biochem Biophys Res Commun 390, 855-860.
27. Luchansky SJ, Lansbury PT Jr, &, Stein RL, (2006) Substrate recognition and catalysis by UCH-L1. Biochemistry 45, 14717-14725. (Pubitemid 44906987)
28. Laskowski RA, MacArthur MW, Moss DS, &, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26, 283-291.
29. Vagin A, &, Teplyakov A, (1997) MOLREP: an automated program for molecular replacement. J Appl Crystallogr 30, 1022-1025. (Pubitemid 127485985)
30. Storer AC, &, Menard R, (1994) Catalytic mechanism in papain family of cysteine peptidases. Methods Enzymol 244, 486-500.
31. Derewenda ZS, Lee L, &, Derewenda U, (1995) The occurrence of C-H···O hydrogen bonds in proteins. J Mol Biol 252, 248-262.
32. Madan Babu M, Kumar Singh S, &, Balaram P, (2002) A C-H triplebond O hydrogen bond stabilized polypeptide chain reversal motif at the C terminus of helices in proteins. J Mol Biol 322, 871-880.
33. Chakrabarti P, &, Chakrabarti S, (1998) C-H···O hydrogen bond involving proline residues in alpha-helices. J Mol Biol 284, 867-873. (Pubitemid 28558540)
34. Derewenda ZS, Derewenda U, &, Kobos PM, (1994) (His)C epsilon-H···O=C< hydrogen bond in the active sites of serine hydrolases. J Mol Biol 241, 83-93.
35. Rawlings ND, Barrett AJ, &, Bateman A, (2010) MEROPS: the peptidase database. Nucleic Acids Res 38, D227-D233.
36. Otwinowski Z, &, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. In Methods in Enzymology, Volume 276: Macromolecular Crystallography, part A (, Carter CW, &, Sweet RM, eds), pp. 307-326. (Pubitemid 27085611)
37. Kiefer F, Arnold K, Kunzli M, Bordoli L, &, Schwede T, (2009) The SWISS-MODEL repository and associated resources. Nucleic Acids Res 37, D387-D392.
38. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760-763.
39. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, &, Vagin AA, (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 67, 355-367.
40. Emsley P, Lohkamp B, Scott WG, &, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66, 486-501.
41. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. (2011) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213-221.