Structural biology of the proteasome

Annual Review of Biophysics

Volumn 42, Issue 1, 2013, Pages 29-49

  Kish Trier, Erik ^a   Hill, Christopher P ^a  

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

Author keywords

conformational changes; intracellular proteolysis; macromolecule assembly; regulated degradation proteasome structure

Indexed keywords

ADENOSINE TRIPHOSPHATE; BLM10 PROTEIN; CORE PROTEIN; P200 PROTEIN; PROTEASOME; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CHANNEL GATING; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; EUBACTERIUM; EUKARYOTE; HISTOCOMPATIBILITY COMPLEX; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; UBIQUITINATION;

ANIMALS; ARCHAEA; BACTERIA; EUKARYOTA; HUMANS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS;

EID: 84876916040     PISSN: 1936122X     EISSN: 19361238     Source Type: Book Series    
DOI: 10.1146/annurev-biophys-083012-130417     Document Type: Article

References (104)

1. Barrault MB, Richet N, Godard C, Murciano B, Le Tallec B, et al. 2012. Dual functions of the Hsm33 protein in chaperoning and scaffolding regulatory particle subunits during the proteasome assembly. Proc. Natl. Acad. Sci. USA 109:E1001-100
2. Barthelme D, Sauer RT. 2012. Identification of the Cdc48*20S proteasome as an ancient AAA++ proteolytic machine. Science 337:843-466
3. Beck F, Unverdorben P, Bohn S, Schweitzer A, Pfeifer G, et al. 2012. Near-atomic resolution structural model of the yeast 26S proteasome. Proc. Natl. Acad. Sci. USA 109:14870-755
4. Benaroudj N, Zwickl P, Seemuller E, Baumeister W, Goldberg AL. 2003. ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation. Mol. Cell 11: 69-788
5. Besche HC, Haas W, Gygi SP, Goldberg AL. 2009. Isolation of mammalian 26S proteasomes and p97/VCP complexes using the ubiquitin-like domain fromHHR23Breveals novel proteasome-associated proteins. Biochemistry 48:2538-499
6. Boehringer J, Riedinger C, Paraskevopoulos K, Johnson EO, Lowe ED, et al. 2012. Structural and functional characterization of Rpn12 identifies residues required for Rpn10 proteasome incorporation. Biochem. J. 448:55-655
7. Bohn S, Beck F, Sakata E, WalzthoeniT, BeckM, et al. 2010. From the cover: Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc.Natl. Acad. Sci. USA107:20992-977
8. Burgie SE, Bingman CA, Soni AB, Phillips GN Jr. 2011. Structural characterization of human Uch37. Proteins. In press. doi: 10.1002/prot.231477
9. Chen X, Barton LF, Chi Y, Clurman BE, Roberts JM. 2007. Ubiquitin-independent degradation of cell-cycle inhibitors by the REGγproteasome. Mol. Cell 26:843-522
10. 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 38:404-155
11. da Fonseca PC, He J, Morris EP. 2012. Molecular model of the human 26S proteasome. Mol. Cell 46:54-666
12. Dange T, Smith D, Noy T, Rommel PC, Jurzitza L, et al. 2011. Blm10 protein promotes proteasomal substrate turnover by an active gating mechanism. J. Biol. Chem. 286:42830-399
13. Djuranovic S, Hartmann MD, HabeckM, Ursinus A, Zwickl P, et al. 2009. Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol. Cell 34:580-900
14. Elsasser S,Gali RR, SchwickartM, Larsen CN, Leggett DS, et al. 2002. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 4:725-300
15. Enemark EJ, Joshua-Tor L. 2006. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442:270-755
16. Erzberger JP, Berger JM. 2006. Evolutionary relationships and structuralmechanisms of AAA+proteins. Annu. Rev. Biophys. Biomol. Struct. 35:93-1144
17. Finley D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78:477-5133
18. Forster A,Masters EI,Whitby FG, Robinson H, Hill CP. 2005. The 1.9 ̊A structure of a proteasome-11S activator complex and implications for proteasome-PAN/PA700 interactions. Mol. Cell 18:589-999
19. Forster A, Whitby FG, Hill CP. 2003. The pore of activated 20S proteasomes has an ordered 7-fold symmetric conformation. EMBO J. 22:4356-644
20. Forster F, Lasker K, Beck F,Nickell S, Sali A, Baumeister W. 2009. An atomic model AAA-ATPase/20S core particle sub-complex of the 26S proteasome. Biochem. Biophys. Res. Commun. 388:228-333
21. Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, et al. 1998. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94:615-233
22. Glynn SE, Martin A, Nager AR, Baker TA, Sauer RT. 2009. Structures of asymmetric ClpX hexamers reveal nucleotide-dependent motions in a AAA+ protein-unfolding machine. Cell 139:744-566
23. Goh AM, Walters KJ, Elsasser S, Verma R, Deshaies RJ, et al. 2008. Components of the ubiquitinproteasome pathway compete for surfaces on Rad23 family proteins. BMC Biochem. 9:44
24. GrollM, Ditzel L, Lowe J, Stock D, Bochtler M, et al. 1997. Structure of 20S proteasome from yeast at 2.4 ̊A resolution. Nature 386:463-711
25. Hamazaki J, Iemura S, Natsume T, Yashiroda H, Tanaka K, Murata S. 2006. A novel proteasome interacting protein recruits the deubiquitinating enzymeUCH37to 26S proteasomes.EMBOJ. 25:4524- 366
26. Hanna J, Hathaway NA, Tone Y, Crosas B, Elsasser S, et al. 2006. Deubiquitinating enzyme Ubp66 functions noncatalytically to delay proteasomal degradation. Cell 127:99-1111
27. He J, Kulkarni K, da Fonseca PC, Krutauz D, Glickman MH, et al. 2012. The structure of the 26S proteasome subunit Rpn2 reveals its PC repeat domain as a closed toroid of two concentric α-helical rings. Structure 20:513-211
28. Horwitz AA, Navon A, Groll M, Smith DM, Reis C, Goldberg AL. 2007. ATP-induced structural transitions in PAN, the proteasome-regulatory ATPase complex in Archaea. J. Biol. Chem. 282:22921- 299
29. Hu M, Li P, Song L, Jeffrey PD, Chenova TA, et al. 2005. Structure and mechanisms of the proteasomeassociated deubiquitinating enzyme USP14. EMBO J. 24:3747-566
30. Huber EM, Basler M, Schwab R, Heinemeyer W, Kirk CJ, et al. 2012. Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell 148:727-388
31. Huber EM, GrollM. 2012. Inhibitors for the immuno- and constitutive proteasome: Current and future trends in drug development. Angew. Chem. Int. Ed. Engl. 51:8708-200
32. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, et al. 2008. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481-888
33. Inobe T, Fishbain S, Prakash S, Matouschek A. 2011. Defining the geometry of the two-component proteasome degron. Nat. Chem. Biol. 7:161-677
34. Iwanczyk J, Sadre-Bazzaz K, Ferrell K, Kondrashkina E, Formosa T, et al. 2006. Structure of the Blm10- 20 S proteasome complex by cryo-electron microscopy. Insights into the mechanism of activation of mature yeast proteasomes. J. Mol. Biol. 363:648-599
35. Kay LE. 2011. SolutionNMRspectroscopy of supra-molecular systems, why bother? Amethyl-TROSY view. J. Magn. Reson. 210:159-700
36. Kim S, Saeki Y, Fukunaga K, Suzuki A, Takagi K, et al. 2010. Crystal structure of yeast Rpn14, a chaperone of the 19 S regulatory particle of the proteasome. J. Biol. Chem. 285:15159-666
37. Knowlton JR, Johnston SC, Whitby FG, Realini C, Zhang Z, et al. 1997. Structure of the proteasome activator REGα(PA28α). Nature 390:639-433
38. Kusmierczyk AR, Kunjappu MJ, Funakoshi M, Hochstrasser M. 2008. A multimeric assembly factor controls the formation of alternative 20S proteasomes. Nat. Struct. Mol. Biol. 15:237-444
39. Kusmierczyk AR, Kunjappu MJ, Kim RY,HochstrasserM. 2011. A conserved 20S proteasome assembly factor requires a C-terminal HbYX motif for proteasomal precursor binding. Nat. Struct. Mol. Biol. 18:622-299
40. Kwon YD, Nagy I, Adams PD, Baumeister W, Jap BK. 2004. Crystal structures of the Rhodococcus proteasome with and without its pro-peptides: Implications for the role of the pro-peptide in proteasome assembly. J. Mol. Biol. 335:233-455
41. Lam YA, DeMartino GN, Pickart CM, Cohen RE. 1997. Specificity of the ubiquitin isopeptidase in the PA700 regulatory complex of 26 S proteasomes. J. Biol. Chem. 272:28438-466
42. Lam YA, Xu W, DeMartino GN, Cohen RE. 1997. Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385:737-400
43. Lander GC, Estrin E,MatyskielaME, Bashore C, Nogales E,Martin A. 2012. Complete subunit architecture of the proteasome regulatory particle. Nature 482:186-911
44. Lasker K, Forster F, Bohn S, Walzthoeni T, Villa E, et al. 2012. Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc. Natl. Acad. Sci. USA 109:1380- 877
45. 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 467:179-844
46. Leggett DS, Hanna J, Borodovsky A, Crosas B, Schmidt M, et al. 2002. Multiple associated proteins regulate proteasome structure and function. Mol. Cell 10:495-5077
47. Li D, Li H, Wang T, PanH, Lin G. 2010. Structural basis for the assembly and gate closure mechanisms of the Mycobacterium tuberculosis 20S proteasome. EMBO J. 29:2037-477
48. Li X, Amazit L, Long W, Lonard DM, Monaco JJ, O'Malley BW. 2007. Ubiquitin- and ATPindependent proteolytic turnover of p21 by the REGγ-proteasome pathway. Mol. Cell 26:831-422
49. Lin G, Li D, de Carvalho LP, Deng H, Tao H, et al. 2009. Inhibitors selective for mycobacterial versus human proteasomes. Nature 461:621-266
50. Liu CW, Corboy MJ, DeMartino GN, Thomas PJ. 2003. Endoproteolytic activity of the proteasome. Science 299:408-111
51. Lowe J, Stock D, Jap B, Zwickl P, BaumeisterW,HuberR. 1995. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 ̊A resolution. Science 268:533-399
52. Matias AC, Ramos PC,Dohmen RJ. 2010. Chaperone-assisted assembly of the proteasome core particle. Biochem. Soc. Trans. 38:29-333
53. Murata S, Yashiroda H, Tanaka K. 2009. Molecular mechanisms of proteasome assembly. Nat. Rev. Mol. Cell Biol. 10:104-155
54. Nakamura Y, Nakano K, Umehara T, Kimura M, Hayashizaki Y, et al. 2007. Structure of the oncoprotein gankyrin in complex with S6 ATPase of the 26S proteasome. Structure 15:179-899
55. Park S, Tian G, Roelofs J, Finley D. 2010. Assembly manual for the proteasome regulatory particle: The first draft. Biochem. Soc. Trans. 38:6-133
56. Pathare GR, Nagy I, Bohn S, Unverdorben P, Hubert A, et al. 2012. The proteasomal subunit Rpn66 is a molecular clamp holding the core and regulatory subcomplexes together. Proc. Natl. Acad. Sci. USA 109:149-544
57. Peth A, Uchiki T, Goldberg AL. 2010. ATP-dependent steps in the binding of ubiquitin conjugates to the 26S proteasome that commit to degradation. Mol. Cell 40:671-811
58. Prakash S, Inobe T, Hatch AJ, Matouschek A. 2009. Substrate selection by the proteasome during degradation of protein complexes. Nat. Chem. Biol. 5:29-366
59. Prakash S, Tian L, Ratliff KS, Lehotzky RE, Matouschek A. 2004. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 11:830-377
60. 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. 25:5742-533
61. Rabl J, Smith DM, Yu Y, Chang SC, Goldberg AL, Cheng Y. 2008. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 30:360-688
62. Rape M, Jentsch S. 2002. Taking a bite: Proteasomal protein processing. Nat. Cell Biol. 4:E113-166
63. Rechsteiner M, Hill CP. 2005. Mobilizing the proteolytic machine: Cell biological roles of proteasome activators and inhibitors. Trends Cell Biol. 15:27-333
64. Religa TL, Sprangers R, Kay LE. 2010. Dynamic regulation of archaeal proteasome gate opening as studied by TROSY NMR. Science 328:98-1022
65. Riedinger C, Boehringer J, Trempe JF, Lowe ED, Brown NR, et al. 2010. Structure of Rpn10 and its interactions with polyubiquitin chains and the proteasome subunit Rpn12. J. Biol. Chem. 285:33992-40033
66. Rosenzweig R, Bronner V, Zhang D, Fushman D, Glickman MH. 2012. Rpn1 and Rpn2 coordinate ubiquitin processing factors at proteasome. J. Biol. Chem. 287:14659-711
67. Ruschak AM, Religa TL, Breuer S, Witt S, Kay LE. 2010. The proteasome antechamber maintains substrates in an unfolded state. Nature 467:868-711
68. Sadre-Bazzaz K, Whitby FG, Robinson H, Formosa T, Hill CP. 2010. Structure of a Blm10 complex reveals common mechanisms for proteasome binding and gate opening. Mol. Cell 37:728-355
69. Sakata E, Bohn S, Mihalache O, Kiss P, Beck F, et al. 2012. Localization of the proteasomal ubiquitin receptors Rpn10 and Rpn13 by electron cryomicroscopy. Proc. Natl. Acad. Sci. USA 109:1479-844
70. Sanches M, Alves BS, Zanchin NI, Guimaraes BG. 2007. The crystal structure of the human Mov344 MPN domain reveals a metal-free dimer. J. Mol. Biol. 370:846-555
71. Sato Y, Yoshikawa A, Yamagata A, Mimura H, Yamashita M, et al. 2008. Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains. Nature 455:358-622
72. Savulescu AF, Glickman MH. 2011. Proteasome activator 200: The heat is on. Mol. Cell. Proteomics 10:R110.0068900
73. SchmidtM, Haas W, Crosas B, Santamaria PG, Gygi SP, et al. 2005. The HEAT repeat protein Blm100 regulates the yeast proteasome by capping the core particle. Nat. Struct. Mol. Biol. 12:294-3033
74. Schreiner P, Chen X, Husnjak K, Randles L, Zhang N, et al. 2008. Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 453:548-522
75. Seemuller E, Lupas A, Stock D, Lowe J,Huber R, BaumeisterW. 1995. Proteasome from Thermoplasma acidophilum: A threonine protease. Science 268:579-822
76. Sijts EJ, Kloetzel PM. 2011. The role of the proteasome in the generation of MHC class I ligands and immune responses. Cell Mol. Life Sci. 68:1491-5022
77. Smith DM, Chang SC, Park S, Finley D, Cheng Y, Goldberg AL. 2007. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's αring opens the gate for substrate entry. Mol. Cell 27:731-444
78. Smith DM, Fraga H, Reis C, Kafri G, Goldberg AL. 2011. ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 144:526-388
79. Sprangers R, Kay LE. 2007. Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature 445:618-222
80. Sprangers R, Li X,Mao X, Rubinstein JL, Schimmer AD, Kay LE. 2008. TROSY-basedNMR evidence for a novel class of 20S proteasome inhibitors. Biochemistry 47:6727-344
81. Stadtmueller BM, Ferrell K, Whitby FG, Heroux A, Robinson H, et al. 2010. Structural models for interactions between the 20S proteasome and its PAN/19S activators. J. Biol. Chem. 285:13-177
82. Stadtmueller BM, Hill CP. 2011. Proteasome activators. Mol. Cell 41:8-199
83. Stadtmueller BM, Kish-Trier E, Ferrell K, Petersen CN, Robinson H, et al. 2012. Structure of a proteasome-Pba1-Pba2 complex: Implications for proteasome assembly, activation, and biological function. J. Biol. Chem. 287:37371-822
84. Takagi K, Kim S, Yukii H, Ueno M, Morishita R, et al. 2012. Structural basis for specific recognition of Rpt1p, an ATPase subunit of 26 S proteasome, by proteasome-dedicated chaperone Hsm3p. J. Biol. Chem. 287:12172-822
85. Takeuchi J, Chen H, Coffino P. 2007. Proteasome substrate degradation requires association plus extended peptide. EMBO J. 26:123-311
86. Thomsen ND, Berger JM. 2009. Running in reverse: The structural basis for translocation polarity in hexameric helicases. Cell 139:523-344
87. Tian G, Park S, Lee MJ, Huck B, McAllister F, et al. 2011. An asymmetric interface between the regulatory and core particles of the proteasome. Nat. Struct. Mol. Biol. 18:1259-677
88. Tian L, Holmgren RA, Matouschek A. 2005. A conserved processing mechanism regulates the activity of transcription factors Cubitus interruptus and NF-κB. Nat. Struct. Mol. Biol. 12:1045-533
89. Tomko RJ Jr, Funakoshi M, Schneider K, Wang J, Hochstrasser M. 2010. Heterohexameric ring arrangement of the eukaryotic proteasomal ATPases: Implications for proteasome structure and assembly. Mol. Cell 38:393-4033
90. UnnoM,MizushimaT,MorimotoY,Tomisugi Y, Tanaka K, et al. 2002. The structure of themammalian 20S proteasome at 2.75 ̊A resolution. Structure 10:609-188
91. Verma R, Chen S, Feldman R, Schieltz D, Yates J, et al. 2000. Proteasomal proteomics: Identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes. Mol. Biol. Cell 11:3425-399
92. Vilchez D, Morantte I, Liu Z, Douglas PM, Merkwirth C, et al. 2012. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 489:263-688
93. Walters KJ, Lech PJ, Goh AM, Wang Q, Howley PM. 2003. DNA-repair protein hHR23a alters its protein structure upon binding proteasomal subunit S5a. Proc. Natl. Acad. Sci. USA 100:12694-999
94. Wang T, Darwin KH, Li H. 2010. Binding-induced folding of prokaryotic ubiquitin-like protein on the Mycobacterium proteasomal ATPase targets substrates for degradation. Nat. Struct. Mol. Biol. 17:1352-577
95. Wang T, Li H, Lin G, Tang C, Li D, et al. 2009. Structural insights on the Mycobacterium tuberculosis proteasomal ATPase Mpa. Structure 17:1377-855
96. Wenzel T, Baumeister W. 1995. Conformational constraints in protein degradation by the 20S proteasome. Nat. Struct. Biol. 2:199-2044
97. Whitby FG, Masters EI, Kramer L, Knowlton JR, Yao Y, et al. 2000. Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 408:115-200
98. Witt S, Kwon YD, SharonM, Felderer K, Beuttler M, et al. 2006. Proteasome assembly triggers a switch required for active-site maturation. Structure 14:1179-888
99. Yao T, Song L, XuW, DeMartino GN, Florens L, et al. 2006. Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat. Cell Biol. 8:994-10022
100. Yashiroda H, Mizushima T, Okamoto K, Kameyama T, Hayashi H, et al. 2008. Crystal structure of a chaperone complex that contributes to the assembly of yeast 20S proteasomes. Nat. Struct. Mol. Biol. 15:228-366
101. Yu Y, SmithDM, KimHM, RodriguezV,Goldberg AL,Cheng Y. 2010. Interactions of PAN's C-termini with archaeal 20S proteasome and implications for the eukaryotic proteasome-ATPase interactions. EMBO J. 29:692-7022
102. Zhang F, Hu M, Tian G, Zhang P, Finley D, et al. 2009. Structural insights into the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol. Cell 34:473-844
103. Zhang F, Wu Z, Zhang P, Tian G, Finley D, Shi Y. 2009. Mechanism of substrate unfolding and translocation by the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol. Cell 34:485-966
104. Zhang N, Wang Q, Ehlinger A, Randles L, Lary JW, et al. 2009. Structure of the S5a:K48-linked diubiquitin complex and its interactions with Rpn13. Mol. Cell 35:280-900