Mechanism of the Rpn13-induced activation of Uch37
详细信息 查看全文
- 作者：Lianying Jiao (1)
Songying Ouyang (1)
Neil Shaw (1)
Gaojie Song (2)
Yingang Feng (3)
Fengfeng Niu (1)
Weicheng Qiu (1)
Hongtao Zhu (1)
Li-Wei Hung (4)
Xiaobing Zuo (5)
V. Eleonora Shtykova (6)
Ping Zhu (1)
Yu-Hui Dong (7)
Ruxiang Xu (8)
Zhi-Jie Liu (1) (3) - 关键词：Uch37 ; Rpn13 complex ; de ; ubiquitination ; SAXS analysis ; oligomerization ; iso ; peptidase
- 刊名：Protein & Cell
- 出版年：2014
- 出版时间：August 2014
- 年：2014
- 卷：5
- 期：8
- 页码：616-630
- 全文大小：1,746 KB
- 参考文献：1. Armstrong CT, Vincent TL, Green PJ, Woolfson DN (2011) SCORER 2.0: an algorithm for distinguishing parallel dimeric and trimeric coiled-coil sequences. Bioinformatics 27:1908-914 CrossRef
2. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewski J, Nilges M, Pannu NS et al (1998) Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr Sect D 54:905-21 CrossRef
3. Burgie SE, Bingman CA, Soni AB, Phillips GN Jr (2011) Structural characterization of human Uch37. Proteins 80:649-54 CrossRef
4. Chen X, Lee BH, Finley D, Walters KJ (2010) Structure of proteasome ubiquitin receptor hRpn13 and its activation by the scaffolding protein hRpn2. Mol Cell 38:404-15 CrossRef
5. 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 103:4675-680 CrossRef
6. Duggan B, Legge G, Dyson HJ, Wright P (2001) SANE (Structure Assisted NOE Evaluation): an automated model-based approach for NOE assignment. J Biomol NMR 19:321-29 CrossRef
7. Fischer H, de Oliveira Neto M, Napolitano HB, Polikarpov I, Craievich AF (2010) Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale. J Appl Crystallogr 43:101-09 CrossRef
8. Glickman MH, Zhang DN, Chen T, Ziv I, Rosenzweig R, Matiuhin Y, Bronner V, Fushman D (2009) Together, Rpn10 and Dsk2 can serve as a polyubiquitin chain-length sensor. Mol Cell 36:1018-033 CrossRef
9. Groll M, Schreiner P, Chen X, Husnjak K, Randles L, Zhang NX, Elsasser S, Finley D, Dikic I, Walters KJ (2008) Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 453:548-52 CrossRef
10. Güntert P, Mumenthaler C, Wüthrich K (1997) Torsion angle dynamics for NMR structure calculation with the new program Dyana. J Mol Biol 273:283-98 CrossRef
11. 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 25:4524-536 CrossRef
12. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I (2008) Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481-88 CrossRef
13. Johnson B, Blevins R (1994) NMR view: acomputer program for the visualization and analysis of NMR data. J Biomol NMR 4:603-14 CrossRef
14. Johnston SC, Larsen CN, Cook WJ, Wilkinson KD, Hill CP (1997) Crystal structure of a deubiquitinating enzyme (human UCH-L3) at 1.8 angstrom resolution. EMBO J 16:3787-796 CrossRef
15. Johnston SC, Riddle SM, Cohen RE, Hill CP (1999) Structural basis for the specificity of ubiquitin C-terminal hydrolases. EMBO J 18:3877-887 CrossRef
16. Konarev PV, Petoukhov MV, Svergun DI (2001) MASSHA—a graphics system for rigid-body modelling of macromolecular complexes against solution scattering data. J Appl Crystallogr 34:527-32 CrossRef
17. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J Appl Crystallogr 36:1277-282 CrossRef
18. Koradi R, Billeter M, Wüthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph?14:51-5 CrossRef
19. Koulich E, Li X, DeMartino GN (2008) Relative structural and functional roles of multiple deubiquitylating proteins associated with mammalian 26S proteasome. Mol Biol Cell 19:1072-082 CrossRef
20. Kozin MB, Svergun DI (2001) Automated matching of high- and low-resolution structural models. J Appl Crystallogr 34:33-1 CrossRef
21. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774-97 CrossRef
22. Lam YA, Xu W, DeMartino GN, Cohen RE (1997) Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385:737-40 CrossRef
23. Larzabal M, Mercado EC, Vilte DA, Salazar-Gonzalez H, Cataldi A, Navarro-Garcia F (2010) Designed coiled-coil peptides inhibit the type three secretion system of enteropathogenic / Escherichia coli. PLoS One 5:e9046 CrossRef
24. Laskowski R, Rullmann JA, MacArthur M, Kaptein R, Thornton J (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477-86 CrossRef
25. Liu CW, Li X, Thompson D, Wooding K, Chang TL, Tang Z, Yu H, Thomas PJ, DeMartino GN (2006) ATP binding and ATP hydrolysis play distinct roles in the function of 26S proteasome. Mol Cell 24:39-0 CrossRef
26. Maiti TK, Permaul M, Boudreaux DA, Mahanic C, Mauney S, Das C (2011) Crystal structure of the catalytic domain of UCHL5, a proteasome-associated human deubiquitinating enzyme, reveals an unproductive form of the enzyme. FEBS J 278:4917-926 CrossRef
27. Markley JL, Bax A, Arata Y, Hilbers CW, Kaptein R, Sykes BD, Wright PE, Wuthrich K (1998) Recommendations for the presentation of NMR structures of proteins and nucleic acids-IUPAC Recommendations 1998). Pure Appl Chem 70:117-42 CrossRef
28. 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 280:1512-520 CrossRef
29. Nederveen AJ, Doreleijers JF, Vranken W, Miller Z, Spronk CAEM, Nabuurs SB, Güntert P, Livny M, Markley JL, Nilges M et al (2005) RECOORD: a recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank. Proteins 59:662-72 CrossRef
30. 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 390:855-60 CrossRef
31. Niu F, Shaw N, Wang YE, Jiao L, Ding W, Li X, Zhu P, Upur H, Ouyang S, Cheng G et al (2013) Structure of the Leanyer orthobunyavirus nucleoprotein-RNA complex reveals unique architecture for RNA encapsidation. Proc Natl Acad Sci USA 110:9054-059 CrossRef
32. 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 284:3593-602 CrossRef
33. 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 25:5742-753 CrossRef
34. Reyes-Turcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78:363-97 CrossRef
35. Schuck P (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78:1606-619 CrossRef
36. Shen Y, Delaglio F, Cornilescu G, Bax A (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol NMR 44:213-23 CrossRef
37. Svergun D (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Crystallogr 25:495-03 CrossRef
38. Svergun DI, Petoukhov MV, Koch MH (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys J 80:2946-953 CrossRef
39. Ventii KH, Wilkinson KD (2008) Protein partners of deubiquitinating enzymes. Biochem J 414:161-75 CrossRef
40. Voges D, Zwickl P, Baumeister W (1999) The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem 68:1015-068 CrossRef
41. Wicks SJ, Haros K, Maillard M, Song L, Cohen RE, Dijke PT, Chantry A (2005) The deubiquitinating enzyme UCH37 interacts with Smads and regulates TGF-beta signalling. Oncogene 24:8080-084 CrossRef
42. 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 8:994-002 CrossRef
43. Yao T, Song L, Jin J, Cai Y, Takahashi H, Swanson SK, Washburn MP, Florens L, Conaway RC, Cohen RE et al (2008) Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the Ino80 chromatin-remodeling complex. Mol Cell 31:909-17 CrossRef
44. Yin ST, Huang H, Zhang YH, Zhou ZR, Song AX, Hong FS, Hu HY (2011) A fluorescence assay for elucidating the substrate specificities of deubiquitinating enzymes. Biochem Biophys Res Commun 416:76-9 CrossRef
45. Young P, Deveraux Q, Beal RE, Pickart CM, Rechsteiner M (1998) Characterization of two polyubiquitin binding sites in the 26 S protease subunit 5a. J Biol Chem 273:5461-467 CrossRef
46. Zhang H, Chen J, Wang Y, Peng L, Dong X, Lu Y, Keating AE, Jiang T (2009) A computationally guided protein-interaction screen uncovers coiled-coil interactions involved in vesicular trafficking. J Mol Biol 392:228-41 CrossRef
47. Zhou ZR, Zhang YH, Liu S, Song AX, Hu HY (2012) Length of the active-site crossover loop defines the substrate specificity of ubiquitin C-terminal hydrolases for ubiquitin chains. Biochem J 441:143-49 CrossRef
48. Zhu QZ, Wani G, Wang QE, El-mahdy M, Snapka RM, Wani AA (2005) Deubiquitination by proteasome is coordinated with substrate translocation for proteolysis in vivo. Exp Cell Res 307:436-51 CrossRef - 作者单位：Lianying Jiao (1)
Songying Ouyang (1)
Neil Shaw (1)
Gaojie Song (2)
Yingang Feng (3)
Fengfeng Niu (1)
Weicheng Qiu (1)
Hongtao Zhu (1)
Li-Wei Hung (4)
Xiaobing Zuo (5)
V. Eleonora Shtykova (6)
Ping Zhu (1)
Yu-Hui Dong (7)
Ruxiang Xu (8)
Zhi-Jie Liu (1) (3)
1. National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
2. iHuman Institute, ShanghaiTech University, Shanghai, 201210, China
3. Shandong Provincial Key Laboratory of Energy Genetics, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, 266101, China
4. Physics Division, Los Alamos National Laboratory, Los Alamos, NM, 87545, USA
5. X-ray Science Division, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, IL, 60439, USA
6. Institute of Crystallography, Russian Academy of Sciences, 59 Leninsky Pr., 117333, Moscow, Russian Federation
7. Center for Multi-disciplinary Research, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China
8. Department of Nerosurgery, The Military General Hospital of Beijing PLA, Beijing, 100700, China - ISSN：1674-8018
文摘
Uch37 is a de-ubiquitinating enzyme that is activated by Rpn13 and involved in the proteasomal degradation of proteins. The full-length Uch37 was shown to exhibit low iso-peptidase activity and is thought to be auto-inhibited. Structural comparisons revealed that within a homo-dimer of Uch37, each of the catalytic domains was blocking the other’s ubiquitin (Ub)-binding site. This blockage likely prevented Ub from entering the active site of Uch37 and might form the basis of auto-inhibition. To understand the mode of auto-inhibition clearly and shed light on the activation mechanism of Uch37 by Rpn13, we investigated the Uch37-Rpn13 complex using a combination of mutagenesis, biochemical, NMR, and small-angle X-ray scattering (SAXS) techniques. Our results also proved that Uch37 oligomerized in solution and had very low activity against the fluorogenic substrate ubiquitin-7-amino-4-methylcoumarin (Ub-AMC) of de-ubiquitinating enzymes. Uch37ΔHb,Hc,KEKE, a truncation removal of the C-terminal extension region (residues 256-29) converted oligomeric Uch37 into a monomeric form that exhibited iso-peptidase activity comparable to that of a truncation-containing the Uch37 catalytic domain only. We also demonstrated that Rpn13C (Rpn13 residues 270-07) could disrupt the oligomerization of Uch37 by sequestering Uch37 and forming a Uch37-Rpn13 complex. Uch37 was activated in such a complex, exhibiting 12-fold-higher activity than Uch37 alone. Time-resolved SAXS (TR-SAXS) and FRET experiments supported the proposed mode of auto-inhibition and the activation mechanism of Uch37 by Rpn13. Rpn13 activated Uch37 by forming a 1:1 stoichiometric complex in which the active site of Uch37 was accessible to Ub.