Domain analysis reveals that a deubiquitinating enzyme usp13 performs non-activating catalysis for lys63-linked polyubiquitin

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Zhang, Yu Hang ^a   Zhou, Chen Jie ^a   Zhou, Zi Ren ^a   Song, Ai Xin ^a   Hu, Hong Yu ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

POLYUBIQUITIN; PROTEINASE; UBIQUITIN SPECIFIC PROTEASE 13; UBIQUITIN SPECIFIC PROTEASE 5; UNCLASSIFIED DRUG; LYSINE; USP13 PROTEIN, HUMAN;

ARTICLE; CATALYSIS; CONTROLLED STUDY; DEUBIQUITINATION; ENZYME ACTIVITY; ENZYME BINDING; HYDROLYSIS; NUCLEAR MAGNETIC RESONANCE; PROTEIN DOMAIN; PROTEIN MODIFICATION; UBIQUITIN BINDING DOMAIN; ZINC FINGER MOTIF; AMINO ACID SEQUENCE; BINDING SITE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BINDING SITES; BIOCATALYSIS; ENDOPEPTIDASES; HUMANS; HYDROLYSIS; LYSINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; POLYUBIQUITIN; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84555203316     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029362     Document Type: Article

References (50)

1. Hochstrasser M, (2009) Origin and function of ubiquitin-like proteins. Nature 458: 422-429.
2. Hershko A, Ciechanover A, (1998) The ubiquitin system. Annu Rev Biochem 67: 425-479.
3. Pickart CM, (2004) Back to the future with ubiquitin. Cell 116: 181-190.
4. Hochstrasser M, (1996) Protein degradation or regulation: Ub the judge. Cell 84: 813-815.
5. Xu P, Duong DM, Seyfried NT, Cheng D, Xie Y, et al. (2009) Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137: 133-145.
6. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, et al. (2003) A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21: 921-926.
7. Amerik AY, Hochstrasser M, (2004) Mechanism and function of deubiquitinating enzymes. Biochim Biophys Acta 1695: 189-207.
8. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, et al. (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123: 773-786.
9. Komander D, Clague MJ, Urbe S, (2009) Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10: 550-563.
10. Reyes-Turcu FE, Ventii KH, Wilkinson KD, (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78: 363-397.
11. Wilkinson KD, (2009) DUBs at a glance. J Cell Sci 122: 2325-2329.
12. Ye Y, Scheel H, Hofmann K, Komander D, (2009) Dissection of USP catalytic domains reveals five common insertion points. Mol Biosyst 5: 1797-1808.
13. Dikic I, Wakatsuki S, Walters KJ, (2009) Ubiquitin-binding domains- from structures to functions. Nat Rev Mol Cell Biol 10: 659-671.
14. Bonnet J, Romier C, Tora L, Devys D, (2008) Zinc-finger UBPs: regulators of deubiquitylation. Trends Biochem Sci 33: 369-375.
15. Hadari T, Warms JV, Rose IA, Hershko A, (1992) A ubiquitin C-terminal isopeptidase that acts on polyubiquitin chains. Role in protein degradation. J Biol Chem 267: 719-727.
16. Wilkinson KD, Tashayev VL, O'Connor LB, Larsen CN, Kasperek E, et al. (1995) Metabolism of the polyubiquitin degradation signal: structure, mechanism, and role of isopeptidase T. Biochemistry 34: 14535-14546.
17. Stein RL, Chen Z, Melandri F, (1995) Kinetic studies of isopeptidase T: modulation of peptidase activity by ubiquitin. Biochemistry 34: 12616-12623.
18. Reyes-Turcu FE, Shanks JR, Komander D, Wilkinson KD, (2008) Recognition of polyubiquitin isoforms by the multiple ubiquitin binding modules of isopeptidase T. J Biol Chem 283: 19581-19592.
19. Reyes-Turcu FE, Horton JR, Mullally JE, Heroux A, Cheng X, et al. (2006) The ubiquitin binding domain ZnF UBP recognizes the C-terminal diglycine motif of unanchored ubiquitin. Cell 124: 1197-1208.
20. Gabriel JM, Lacombe T, Carobbio S, Paquet N, Bisig R, et al. (2002) Zinc is required for the catalytic activity of the human deubiquitinating isopeptidase T. Biochemistry 41: 13755-13766.
21. Dayal S, Sparks A, Jacob J, Allende-Vega N, Lane DP, et al. (2009) Suppression of the deubiquitinating enzyme USP5 causes the accumulation of unanchored polyubiquitin and the activation of p53. J Biol Chem 284: 5030-5041.
22. Cooper EM, Cutcliffe C, Kristiansen TZ, Pandey A, Pickart CM, et al. (2009) K63-specific deubiquitination by two JAMM/MPN+ complexes: BRISC-associated Brcc36 and proteasomal Poh1. Embo J 28: 621-631.
23. Raasi S, Varadan R, Fushman D, Pickart CM, (2005) Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat Struct Mol Biol 12: 708-714.
24. Timms KM, Ansari-Lari MA, Morris W, Brown SN, Gibbs RA, (1998) The genomic organization of Isopeptidase T-3 (ISOT-3), a new member of the ubiquitin specific protease family (UBP). Gene 217: 101-106.
25. Fontaine JF, Mirebeau-Prunier D, Raharijaona M, Franc B, Triau S, et al. (2009) Increasing the number of thyroid lesions classes in microarray analysis improves the relevance of diagnostic markers. PLoS One 4: e7632.
26. Ovaa H, Kessler BM, Rolen U, Galardy PJ, Ploegh HL, et al. (2004) Activity-based ubiquitin-specific protease (USP) profiling of virus-infected and malignant human cells. Proc Natl Acad Sci U S A 101: 2253-2258.
27. Catic A, Fiebiger E, Korbel GA, Blom D, Galardy PJ, et al. (2007) Screen for ISG15-crossreactive deubiquitinases. PLoS One 2: e679.
28. McElhinny AS, Kakinuma K, Sorimachi H, Labeit S, Gregorio CC, (2002) Muscle-specific RING finger-1 interacts with titin to regulate sarcomeric M-line and thick filament structure and may have nuclear functions via its interaction with glucocorticoid modulatory element binding protein-1. J Cell Biol 157: 125-136.
29. Sowa ME, Bennett EJ, Gygi SP, Harper JW, (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138: 389-403.
30. Dang LC, Melandri FD, Stein RL, (1998) Kinetic and mechanistic studies on the hydrolysis of ubiquitin C-terminal 7-amido-4-methylcoumarin by deubiquitinating enzymes. Biochemistry 37: 1868-1879.
31. Amerik A, Swaminathan S, Krantz BA, Wilkinson KD, Hochstrasser M, (1997) In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome. Embo J 16: 4826-4838.
32. Allen MD, Bycroft M, (2007) The solution structure of the ZnF UBP domain of USP33/VDU1. Protein Sci 16: 2072-2075.
33. Pai MT, Tzeng SR, Kovacs JJ, Keaton MA, Li SS, et al. (2007) Solution structure of the Ubp-M BUZ domain, a highly specific protein module that recognizes the C-terminal tail of free ubiquitin. J Mol Biol 370: 290-302.
34. Chang YG, Song AX, Gao YG, Shi YH, Lin XJ, et al. (2006) Solution structure of the ubiquitin-associated domain of human BMSC-UbP and its complex with ubiquitin. Protein Sci 15: 1248-1259.
35. Mueller TD, Feigon J, (2002) Solution structures of UBA domains reveal a conserved hydrophobic surface for protein-protein interactions. J Mol Biol 319: 1243-1255.
36. Mueller TD, Kamionka M, Feigon J, (2004) Specificity of the interaction between ubiquitin-associated domains and ubiquitin. J Biol Chem 279: 11926-11936.
37. Hirsch C, Gauss R, Horn SC, Neuber O, Sommer T, (2009) The ubiquitylation machinery of the endoplasmic reticulum. Nature 458: 453-460.
38. Yang M, Omura S, Bonifacino JS, Weissman AM, (1998) Novel aspects of degradation of T cell receptor subunits from the endoplasmic reticulum (ER) in T cells: importance of oligosaccharide processing, ubiquitination, and proteasome-dependent removal from ER membranes. J Exp Med 187: 835-846.
39. Zhong X, Pittman RN, (2006) Ataxin-3 binds VCP/p97 and regulates retrotranslocation of ERAD substrates. Hum Mol Genet 15: 2409-2420.
40. Gamsjaeger R, Liew CK, Loughlin FE, Crossley M, Mackay JP, (2007) Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem Sci 32: 63-70.
41. Boyault C, Gilquin B, Zhang Y, Rybin V, Garman E, et al. (2006) HDAC6-p97/VCP controlled polyubiquitin chain turnover. Embo J 25: 3357-3366.
42. Hurley JH, Lee S, Prag G, (2006) Ubiquitin-binding domains. Biochem J 399: 361-372.
43. Lee BH, Lee MJ, Park S, Oh DC, Elsasser S, et al. (2010) Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 467: 179-184.
44. Cohn MA, Kowal P, Yang K, Haas W, Huang TT, et al. (2007) A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol Cell 28: 786-797.
45. Luna-Vargas MP, Faesen AC, van Dijk WJ, Rape M, Fish A, et al. (2011) Ubiquitin-specific protease 4 is inhibited by its ubiquitin-like domain. EMBO Rep 12: 365-372.
46. Zhao X, Fiske B, Kawakami A, Li J, Fisher DE, (2011) Regulation of MITF stability by the USP13 deubiquitinase. Nat Commun 2: 414.
47. Scortegagna M, Subtil T, Qi J, Kim H, Zhao W, et al. (2011) USP13 enzyme regulates Siah2 ligase stability and activity via noncatalytic ubiquitin-binding domains. J Biol Chem 286: 27333-27341.
48. Liu J, Xia H, Kim M, Xu L, Li Y, et al. (2011) Beclin1 Controls the Levels of p53 by Regulating the Deubiquitination Activity of USP10 and USP13. Cell 147: 223-234.
49. Song AX, Zhou CJ, Guan X, Sze KH, Hu HY, (2010) Solution structure of the N-terminal domain of DC-UbP/UBTD2 and its interaction with ubiquitin. Protein Sci 19: 1104-1109.
50. Raasi S, Pickart CM, (2005) Ubiquitin chain synthesis. Methods Mol Biol 301: 47-55.