Structural basis for the specificity of ubiquitin C-terminal hydrolases

EMBO Journal

Volumn 18, Issue 14, 1999, Pages 3877-3887

  Johnston, Steven C ^a   Riddle, Steven M ^b   Cohen, Robert E ^b   Hill, Christopher P ^a  

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

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Crystal structure; Cysteine protease; Deubiquitinating; Enzyme; Enzyme specificity; Ubiquitin

Indexed keywords

HYDROLASE; UBIQUITIN;

AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; YEAST;

AMINO ACID SEQUENCE; BINDING SITES; CATALYSIS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ENDOPEPTIDASES; FUNGAL PROTEINS; HYDROGEN BONDING; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY; THIOLESTER HYDROLASES; UBIQUITIN THIOLESTERASE; UBIQUITINS;

EID: 0033565867     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.14.3877     Document Type: Article

References (50)

1. Bacon, D. and Anderson, W.F. (1988) A fast algorithm for rendering space-filling molecule pictures. J. Mol. Graph., 6, 219-220.
2. Baker, R.T., Tobias, J.W. and Varshavsky, A. (1992) Ubiquitin-specific proteases of Saccharomyces cerevisiae: cloning of UBP2 and UBP3 and functional analysis of the UBP gene family. J. Biol. Chem., 267, 23364-23375.
3. Beal, R., Deveraux, Q., Xia, G., Rechsteiner, M. and Pickart, C. (1996) Surface hydrophobic residues of multiubiquitin chains essential for proteolytic targeting. Proc. Natl Acad. Sci. USA, 93, 861-866.
4. Beal, R.E., Toscano-Cantaffa, D., Young, P., Rechsteiner, M. and Pickart, C.M. (1998) The hydrophobic effect contributes to polyubiquitin chain recognition. Biochemistry, 37, 2925-2934.
5. Brünger, A.T. (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature, 355, 472-475.
6. Brünger, A.T. (1996) X-PLOR Version 3.843, A System for X-ray Crystallography and NMR. Yale University, New Haven, CT.
7. Burch, T. and Haas, A. (1994) Site-directed mutagenesis of ubiquitin. Differential roles for arginine in the interaction with ubiquitin-activating enzyme. Biochemistry, 33, 7300-7308.
8. (1994) The CCP4 suite: programs for protein crystallography. Acta Cryst., D50, 760-763.
9. Chau, V., Tobias, J.W., Bachmair, A., Marriott, D., Ecker, D.J., Gonda, D.K. and Varshavsky, A. (1989) A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science, 243, 1576-1583.
10. Ciechanover, A. and Schwartz, A.L. (1998) The ubiquitin-proteasome pathway: the complexity and myriad functions of proteins death. Proc. Natl Acad. Sci. USA, 95, 2727-2730.
11. Cowtan, K.D. (1994) 'dm': an automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography, 31, 34-38.
12. Dang, L.C., Melandri, F.D. and Stein, R.L. (1998) Kinetic and mechanistic studies on the hydrolysis of ubiquitin C-terminal 7-amido-4-methylcoumarin by deubiquitinating enzymes. Biochemistry, 37, 1868-1879.
13. DeKoster, G.T. and Robertson, A.D. (1997) Thermodynamics of unfolding for Kazal-type serine protease inhibitors: entropie stabilization of ovomucoid first domain by glycosylation. Biochemistry, 36, 2323-2331.
14. Dunten, R.L. and Cohen, R.E. (1989) Recognition of modified forms of ribonuclease A by the ubiquitin system. J. Biol. Chem., 264, 16739-16747.
15. Gill, S.C. and vonHippel, P.H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem., 182, 319-326.
16. Hegde, A.N., Inokuchi, K., Pei, W., Casadio, A., Ghirardi, M., Chain, D.G., Martin, K.C., Kandel, E.R. and Schwartz, J.H. (1997) Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell, 89, 115-126.
17. Hershko, A. and Rose, I.A. (1987) Ubiquitin-aldehyde: a general inhibitor of ubiquitin-recycling processes. Proc. Natl Acad. Sci. USA, 84, 1829-1833.
18. Hutchinson, E.G. and Thornton, J.M. (1996) PROMOTIF - a program to identify and analyze structural motifs in proteins. Protein Sci., 5, 212-220.
19. Jensen, D.E. 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.
20. Johnston, S.C., Larsen, C.N., Cook, W., Wilkinson, K.D. and Hill, C.P. (1997) Crystal structure of a deubiquitinating enzyme (human UCHL3) at 1.8 Å resolution. EMBO J., 16, 3787-3796.
21. Jones, T.A., Zou, J.-Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and location of errors in these models. Acta Crystallogr., A47, 110-119.
22. Kleywegt, G.J. and Jones, T.A. (1994a) Halloween . . . masks and bones. In Bailey, S., Hubbard, R. and Waller, D. (eds), From First Map to Final Model. Daresbury Laboratory, Warrington, UK, pp. 59-66.
23. Kleywegt, G.J. and Jones, T.A. (1994b) A super position. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography, 31, 9-14.
24. Kraulis, P.J. (1991) Molscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
25. Lam, Y.A., DeMartino, G.N., Pickart, C.M. and Cohen, R.E. (1997a) Specificity of the ubiquitin isopeptidase in the PA700 regulatory complex of 26 S proteasomes. J. Biol. Chem., 272, 28438-28446.
26. Lam, Y.A., Xu, W., DeMartino, G.N. and Cohen, R.E. (1997b) Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature, 385, 737-740.
27. 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.
28. Larsen, C.N., Krantz, B.A. and Wilkinson, K.D. (1998) Substrate specificity of deubiquitinating enzymes: ubiquitin C-terminal hydrolases. Biochemistry, 37, 3358-3368.
29. 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.
30. Leroy, E. et al. (1998) The ubiquitin pathway in Parkinson's disease. Nature, 395, 450-451.
31. Miller, H.I., Henzel, W.J., Ridgmay, J.B., Kuang, W.-J., Chisholm, V. and Liu, C.-C. (1989) Cloning and expression of a yeast ubiquitin-protein cleaving activity in Escherichia coli. Biotechnology, 7, 698-704.
32. Otwinowski, Z. (1991) Maximum likelihood refinement of heavy atom parameters. In Wolf, W., Evans, P.R. and Leslie, A.G.W. (eds), Isomorphous Replacement and Anomalous Scattering. Daresbury Laboratory, Warrington, UK, pp. 80-86.
33. Otwinowski, Z. (1993) Oscillation data reduction program. In Sawyer. L., Isaacs, N. and Bailey, S. (eds), Data Collection and Processing. SERC Daresbury Laboratory, Warrington, UK, pp. 56-62.
34. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 176, 307-326.
35. Özkaynak, E., Finley, D., Solomon, M.J. and Varshavsky, A. (1987) The yeast ubiquitin genes: a family of natural gene fusions. EMBO J., 6, 1429-1439.
36. Pickart, C.M. (1997) Targeting of substrates to the 26S proteasome. FASEB J., 11, 1055-1066.
37. Pickart, C.M. and Rose, I.A. (1985) Ubiquitin carboxyl-terminal hydrolase acts on ubiquitin carboxyl-terminal amides. J. Biol. Chem., 260, 7903-7910.
38. Pickart, C.M. and Rose, I.A. (1986) Mechanism of ubiquitin carboxyl-terminal hydrolase: borohydride and hydroxylamine inactivate in the presence of ubiquitin. J. Biol. Chem., 261, 10210-10217.
39. Piotrowski, J., Beal, R., Hoffman, L., Wilkinson, K.D., Cohen, R.E. and Pickart, C.M. (1997) Inhibition of the 26 S proteasome by polyubiquitin chains synthesized to have defined lengths. J. Biol. Chem., 272, 23712-23721.
40. Ramakrishnan, V. and Biou, V. (1997) Treatment of multiwavelength anomalous diffraction as a special case of multiple isomorphous replacement. Methods Enzymol., 276, 538-557.
41. Rose, I.A. and Warms, J.V.M. (1983) An enzyme with ubiquitin carboxy-terminal esterase activity from reticulocytes. Biochemistry, 22, 4234-4237.
42. Storer, A.C. and Ménard, R. (1994) Catalytic mechanism in papain family of cysteine peptidases. Methods Enzymol., 244, 486-500.
43. Studier, F.W. and Moffatt, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol., 189, 113-130.
44. Tobias, J.W. and Varshavsky, A. (1991) Cloning and functional analysis of the ubiquitin-specific protease gene Ubp1 of Saccharomyces cerevisiae. J. Biol. Chem., 266, 12021-12028.
45. Vijay-Kumar, S., Bugg, C.E. and Cook, W.J. (1987) Structure of ubiquitin refined at 1.8Å resolution. J. Mol. Biol., 194, 531-544.
46. Whitby, F.G., Xia, G., Pickart, C.M. and Hill, C.P. (1998) Crystal structure of the human ubiquitin-like protein NEDD8 and inteactions with ubiquitin pathway enzymes. J. Biol. Chem., 273, 34983-34991.
47. Wilkinson, K.D. and Hochstrasser, M. (1998) The deubiquitinating enzymes. In Pettrs, J.M., Harris, J.R. and Finley, D. (eds), Ubiquitin and the Biology of the Cell. Plenum Press, New York, NY, pp. 99-125.
48. Wilkinson, K.D., Lee, K., Deshpande, S., Duerksen-Hughes, P., Boss, J.M. and Pohl, J. (1989) The neuron-specific protein PGP9.5 is a ubiquitin carboxyl-terminal hydrolase. Science, 246, 670-673.
49. Wilkinson, K.D., Deshpande, S. and Larsen, C.N. (1992) Comparisons of neuronal (PGP 9.5) and non-neuronal ubiquitin C-terminal hydrolases. Biochem. Soc. Trans., 20, 631-637.
50. Wintrode, P.L., Makhatadze, G.I. and Privalov, P.L. (1994) Thermodynamics of ubiquitin unfolding. Proteins, 18, 246-253.