The life cycle of the 26S proteasome: From birth, through regulation and function, and onto its death

Cell Research

Volumn 26, Issue 8, 2016, Pages 869-885

  Livneh, Ido ^a   Cohen Kaplan, Victoria ^a   Cohen Rosenzweig, Chen ^a   Avni, Noa ^a   Ciechanover, Aaron ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

proteasome; ubiquitin

Indexed keywords

ATP DEPENDENT 26S PROTEASE; PROTEASOME;

ANIMAL; CHEMISTRY; ENZYME SPECIFICITY; HUMAN; METABOLISM; PROTEIN DEGRADATION; PROTEIN PROCESSING;

ANIMALS; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; SUBSTRATE SPECIFICITY;

EID: 84979306721     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2016.86     Document Type: Review

References (217)

1. Tomko RJ, Hochstrasser M. Molecular architecture and assembly of the eukaryotic proteasome. Annu Rev Biochem 2013; 82: 415-445.
2. Groll M, Bajorek M, Köhler A, et al. A gated channel into the proteasome core particle. Nat Struct Biol 2000; 7: 1062-1067.
3. Rabl J, Smith DM, Yu Y, Chang SC, Goldberg AL, Cheng Y. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol Cell 2008; 30: 360-368.
4. Smith DM, Chang SC, Park S, Finley D, Cheng Y, Goldberg AL. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's ring opens the gate for substrate entry. Mol Cell 2007; 27: 731-744.
5. Pickart CM, Cohen RE. Proteasomes and their kin: proteases in the machine age. Nat Rev Mol Cell Biol 2004; 5: 177-187.
6. Groll M, Ditzel L, Löwe J, et al. Structure of 20S proteasome from yeast at 2. 4 A resolution. Nature 1997; 386: 463-471.
7. Nederlof PM, Wang HR, Baumeister W. Nuclear localization signals of human and Thermoplasma proteasomal subunits are functional in vitro. Proc Natl Acad Sci USA 1995; 92: 12060-12064.
8. Tanaka K, Yoshimura T, Tamura T, Fujiwara T, Kumatori A, Ichihara A. Possible mechanism of nuclear translocation of proteasomes. FEBS Lett 1990; 271: 41-46.
9. Ogiso Y, Tomida A, Tsuruo T. Nuclear localization of proteasomes participates in stress-inducible resistance of solid tumor cells to topoisomerase II-directed drugs. Cancer Res 2002; 62: 5008-5012.
10. Dick TP, Nussbauma K, Deeg M, et al. Contribution of proteasomal subunits to the cleavage of peptide substrates analyzed with yeast mutants. J Biol Chem 1998; 273: 25637-25646.
11. Dahlmann B. Mammalian proteasome subtypes: Their diversity in structure and function. Arch Biochem Biophys 2016; 591: 132-140.
12. Díaz-Villanueva JF, Díaz-Molina R, García-González V. Protein folding and mechanisms of proteostasis. Int J Mol Sci 2015; 16: 17193-17230.
13. Heinemeyer W, Ramos PC, Dohmen RJ. Ubiquitin-proteasome system. Cell Mol Life Sci 2004; 61: 1562-1578.
14. Husnjak K, Elsasser S, Zhang N, et al. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 2008; 453: 481-488.
15. Shi Y, Chen X, Elsasser S, et al. Rpn1 provides adjacent receptor sites for substrate binding and deubiquitination by the proteasome. Science 2016; 351: aad9421. 1-10.
16. Fu H, Sadis S, Rubin DM, et al. Multiubiquitin chain binding and protein degradation are mediated by distinct domains within the 26 S proteasome subunit Mcb1. J Biol Chem 1998; 273: 1970-1981.
17. Verma R, Aravind L, Oania R, et al. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 2002; 298: 611-615.
18. Yao T, Cohen RE. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 2002; 419: 403-407.
19. Lam YA, Xu W, DeMartino GN, Cohen RE. Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 1997; 385: 737-740.
20. Leggett DS, Hanna J, Borodovsky A, et al. Multiple associated proteins regulate proteasome structure and function. Mol Cell 2002; 10: 495-507.
21. Maytal-Kivity V, Reis N, Hofmann K, Glickman MH. MPN+, a putative catalytic motif found in a subset of MPN domain proteins from eukaryotes and prokaryotes, is critical for Rpn11 function. BMC Biochem 2002; 3: 28.
22. Kleijnen MF, Roelofs J, Park S, et al. Stability of the proteasome can be regulated allosterically through engagement of its proteolytic active sites. Nat Struct Mol Biol 2007; 14: 1180-1188.
23. Li X, Demartino GN, Craiu A, et al. Variably modulated gating of the 26S proteasome by ATP and polyubiquitin. Biochem J 2009; 421: 397-404.
24. Gallastegui N, Groll M. The 26S proteasome: assembly and function of a destructive machine. Trends Biochem Sci 2010; 35: 634-642.
25. Finley D, Chen X, Walters KJ. Gates, channels, and switches: elements of the proteasome machine. Trends Biochem Sci 2015; 41: 77-93.
26. Hirano Y, Hendil KB, Yashiroda H, et al. A heterodimeric complex that promotes the assembly of mammalian 20S proteasomes. Nature 2005; 437: 1381-1385.
27. Stadtmueller BM, Kish-Trier E, Ferrell K, et al. Structure of a proteasome Pba1-Pba2 complex implications for proteasome assembly, activation, and biological function. J Biol Chem 2012; 287: 37371-37382.
28. Hirano Y, Hayashi H, Iemura S, et al. Cooperation of multiple chaperones required for the assembly of mammalian 20S proteasomes. Mol Cell 2006; 24: 977-984.
29. Murata S, Yashiroda H, Tanaka K. Molecular mechanisms of proteasome assembly. Nat Rev Mol Cell Biol 2009; 10: 104-115.
30. Fricke B, Heink S, Steffen J, Kloetzel P-M, Krüger E. The proteasome maturation protein POMP facilitates major steps of 20S proteasome formation at the endoplasmic reticulum. EMBO Rep 2007; 8: 1170-1175.
31. Ramos PC, Höckendorff J, Johnson ES, Varshavsky A, Dohmen RJ. Ump1p is required for proper maturation of the 20S proteasome and becomes its substrate upon completion of the assembly. Cell 1998; 92: 489-499.
32. Bar-Nun S, Glickman MH. Proteasomal AAA-ATPases: structure and function. Biochim Biophys Acta 2012; 1823: 67-82.
33. Hanssum A, Zhong Z, Rousseau A, Krzyzosiak A, Sigurdardottir A, Bertolotti A. An inducible chaperone adapts proteasome assembly to stress. Mol Cell 2014; 55: 566-577.
34. Saeki Y, Toh-E A, Kudo T, Kawamura H, Tanaka K. Multiple proteasome-interacting proteins assist the assembly of the yeast 19S regulatory particle. Cell 2009; 137: 900-913.
35. Tomko RJ, Taylor DW, Chen ZA, Wang H-W, Rappsilber J, Hochstrasser M. A single helix drives extensive remodeling of the proteasome lid and completion of regulatory particle assembly. Cell 2015; 163: 432-444.
36. Imai J, Maruya M, Yashiroda H, Yahara I, Tanaka K. The molecular chaperone Hsp90 plays a role in the assembly and maintenance of the 26S proteasome. EMBO J 2003; 22: 3557-3567.
37. Piterman R, Braunstein I, Isakov E, et al. Vwa Domain of S5a restricts the ability to bind ubiquitin and Ubl to the 26S proteasome. Mol Biol Cell 2014; 25: 3988-3998.
38. Hendil KB, Hartmann-Petersen R, Tanaka K. 26 S proteasomes function as stable entities. J Mol Biol 2002; 315: 627-636.
39. Peters LZ, Karmon O, David-Kadoch G, et al. The protein quality control machinery regulates its misassembled proteasome subunits. PLoS Genet 2015; 11: e1005178.
40. Meiners S, Heyken D, Weller A, et al. Inhibition of proteasome activity induces concerted expression of proteasome genes and de novo formation of mammalian proteasomes. J Biol Chem 2003; 278: 21517-21525.
41. Zhang Y, Manning BD. mTORC1 signaling activates NRF1 to increase cellular proteasome levels. Cell Cycle 2015; 14: 2011-2017.
42. Sha Z, Goldberg AL. Proteasome-mediated processing of Nrf1 is essential for coordinate induction of all proteasome subunits and p97. Curr Biol 2014; 24: 1573-1583.
43. Mitsiades N, Mitsiades CS, Poulaki V, et al. Molecular sequelae of proteasome inhibition in human multiple myeloma cells. Proc Natl Acad Sci USA 2002; 99: 14374-14379.
44. Lundgren J, Masson P, Mirzaei Z, Young P. Identification and characterization of a Drosophila proteasome regulatory network. Mol Cell Biol 2005; 25: 4662-4675.
45. Li X, Matilainen O, Jin C, Glover-Cutter KM, Holmberg CI, Blackwell TK. Specific SKN-1/NrF stress responses to perturbations in translation elongation and proteasome activity. PLoS Genet 2011; 7: 9-11.
46. London MK, Keck BI, Ramos PC, Dohmen RJ. Regulatory mechanisms controlling biogenesis of ubiquitin and the proteasome. FEBS Lett 2004; 567: 259-264.
47. Radhakrishnan SK, Lee CS, Young P, Beskow A, Chan JY, Deshaies RJ. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol Cell 2010; 38: 17-28.
48. Steffen J, Seeger M, Koch A, Krüger E. Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol Cell 2010; 40: 147-158.
49. Malloy MT, McIntosh DJ, Walters TS, Flores A, Goodwin JS, Arinze IJ. Trafficking of the transcription factor Nrf2 to promyelocytic leukemia-nuclear bodies: Implications for degradation of nrf2 in the nucleus. J Biol Chem 2013; 288: 14569-14583.
50. Kwak MK, Wakabayashi N, Greenlaw JL, Yamamoto M, Kensler TW. Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol Cell Biol 2003; 23: 8786-8794.
51. Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 2004; 10: 549-557.
52. Pickering AM, Staab TA., Tower J, Sieburth DS, Davies KJ. A conserved role for the 20S proteasome and Nrf2 transcription factor in oxidative-stress adaptation in mammals, C. elegans and D. melanogaster. J Exp Biol 2013; 216: 543-553.
53. Choe KP, Przybysz AJ, Strange K. The WD40 repeat protein WDR-23 functions with the CUL4/DDB1 ubiquitin ligase to regulate nuclear abundance and activity of SKN-1 in Caenorhabditis elegans. Mol Cell Biol 2009; 29: 2704-2715.
54. Wang L, Mao X, Ju D, Xie Y. Rpn4 is a physiological substrate of the Ubr2 ubiquitin ligase. J Biol Chem 2004; 279: 55218-55223.
55. Ju D, Xie Y. Proteasomal degradation of RPN4 via two distinct mechanisms, ubiquitin-dependent and-independent. J Biol Chem 2004; 279: 23851-23854.
56. Xie Y, Varshavskya. RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc Natl Acad Sci USA 2001; 98: 3056-3061.
57. Mannhaupt G, Schnall R, Karpov V, Vetter I, Feldmann H. Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Lett 1999; 450: 27-34.
58. Ma M, Liu ZL. Comparative transcriptome profiling analyses during the lag phase uncover YAP1, PDR1, PDR3, RPN4, and HSF1 as key regulatory genes in genomic adaptation to the lignocellulose derived inhibitor HMF for Saccharomyces cerevisiae. BMC Genomics 2010; 11: 660.
59. Chondrogianni N, Tzavelas C, Pemberton AJ, Nezis IP, Rivett AJ, Gonos ES. Overexpression of proteasome 5 subunit increases the amount of assembled proteasome and confers ameliorated response to oxidative stress and higher survival rates. J Biol Chem 2005; 280: 11840-11850.
60. Vilchez D, Morantte I, Liu Z, et al. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 2012; 489: 263-268.
61. Vilchez D, Boyer L, Morantte I, et al. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature 2012; 489: 304-308.
62. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2013; 149: 274-293.
63. Zhang Y, Nicholatos J, Dreier JR, et al. Coordinated regulation of protein synthesis and degradation by mTORC1. Nature 2014; 513: 440-443.
64. Zhao J, Zhai B, Gygi SP, Goldberg AL. mTOR inhibition activates overall protein degradation by the ubiquitin proteasome system as well as by autophagy. Proc Natl Acad Sci USA 2015; 112: 15790-15797.
65. Zhao J, Garcia GA, Goldberg AL. Control of proteasomal proteolysis by mTOR. Nature 2016; 529: E1-E2.
66. Zhang Y, Manning BD. Zhang & Manning reply. Nature 2016; 529: E2-E3.
67. Hirano H, Kimura Y, Kimura A. Biological significance of coand post-translational modifications of the yeast 26S proteasome. J Proteomics 2015; 134: 37-46.
68. Zong N, Ping P, Lau E, et al. Lysine ubiquitination and acetylation of human cardiac 20S proteasomes. Proteomics Clin Appl 2014; 8: 590-594.
69. Guo X, Engel JL, Xiao J, et al. UBLCP1 is a 26S proteasome phosphatase that regulates nuclear proteasome activity. Proc Natl Acad Sci USA 2011; 108: 18649-18654.
70. van Deventer S, Menendez-Benito V, van Leeuwen F, Neefjes J. N-terminal acetylation and replicative age affect proteasome localization and cell fitness during aging. J Cell Sci 2015; 128: 109-117.
71. Marshall RS, Li F, Gemperline DC, Book AJ, Vierstra RD. Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol Cell 2015; 58: 1053-1066.
72. Iwafune Y, Kawasaki H, Hirano H. Electrophoretic analysis of phosphorylation of the yeast 20S proteasome. Electrophoresis 2002; 23: 329-338.
73. Bose S, Stratford FLL, Broadfoot KI, Mason GGF, Rivett AJ. Phosphorylation of 20S proteasome subunit C8 (7) stabilizes the 26S proteasome and plays a role in the regulation of proteasome complexes by-interferon. Biochem J 2004; 378: 177-184.
74. Kikuchi J, Iwafune Y, Akiyama T, et al. Co-and post-translational modifications of the 26S proteasome in yeast. Proteomics 2010; 10: 2769-2779.
75. Zhang F, Hu Y, Huang P, Toleman CA, Paterson AJ, Kudlow JE. Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of Rpt6. J Biol Chem 2007; 282: 22460-22471.
76. Satoh K, Sasajima H, Nyoumura K, Yokosawa H, Sawada H. Assembly of the 26S proteasome is regulated by phosphorylation of the p45/Rpt6 ATPase subunit. Biochemistry 2001; 40: 314-319.
77. Lu H, Zong C, Wang Y, et al. Revealing the dynamics of the 20S proteasome phosphoproteome: a combined CID and electron transfer dissociation approach. Mol Cell Proteomics 2008; 7: 2073-2089.
78. Ramnanan CJ, Allan ME, Groom AG, Storey KB. Regulation of global protein translation and protein degradation in aerobic dormancy. Mol Cell Biochem 2009; 323: 9-20.
79. Lee S-H, Park Y, Yoon SK, Yoon J-B. Osmotic stress inhibits proteasome by p38 MAPK-dependent phosphorylation. J Biol Chem 2010; 285: 41280-41289.
80. Liu X, Huang W, Li C, et al. Interaction between c-Abl and Arg tyrosine kinases and proteasome subunit PSMA7 regulates proteasome degradation. Mol Cell 2006; 22: 317-327.
81. Lokireddy S, Kukushkin NV, Goldberg AL. cAMP-induced phosphorylation of 26S proteasomes on Rpn6/PSMD11 enhances their activity and the degradation of misfolded proteins. Proc Natl Acad Sci USA 2015; 112: E7176-7185.
82. Isasa M, Katz EJ, Kim W, et al. Monoubiquitination of RPN10 regulates substrate recruitment to the proteasome. Mol Cell 2010; 38: 733-745.
83. Besche HC, Sha Z, Kukushkin N V, et al. Autoubiquitination of the 26S proteasome on Rpn13 regulates breakdown of ubiquitin conjugates. EMBO J 2014; 33: 1159-1176.
84. Wang D, Fang C, Zong NC, et al. Regulation of acetylation restores proteolytic function of diseased myocardium in mouse and human. Mol Cell Proteomics 2013; 12: 3793-3802.
85. Silva GM, Netto LES, Simes V, et al. Redox control of 20S proteasome gating. Antioxid Redox Signal 2012; 16: 1183-1194.
86. Kimura A, Kurata Y, Nakabayashi J, Kagawa H, Hirano H. N-myristoylation of the Rpt2 subunit of the yeast 26S proteasome is implicated in the subcellular compartment-specific protein quality control system. J Proteomics 2016; 130: 33-41.
87. Zhang F, Su K, Yang X, Bowe DB, Paterson AJ, Kudlow JE. O-GlcNAc modification is an endogenous inhibitor of the proteasome. Cell 2003; 115: 715-725.
88. Ullrich O, Reinheckel T, Sitte N, Hass R, Grune T, Davies KJ. Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc Natl Acad Sci USA 1999; 96: 6223-6228.
89. Lam YA, Lawson TG, Velayutham M, Zweier JL, Pickart CM. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 2002; 416: 763-767.
90. Paraskevopoulos K, Kriegenburg F, Tatham MH, et al. Dss1 is a 26S proteasome ubiquitin receptor. Mol Cell 2014; 56: 453-461.
91. Schreiner P, Chen X, Husnjak K, et al. Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 2008; 453: 548-552.
92. Yao T, Song L, Xu W, et al. Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat Cell Biol 2006; 8: 994-1002.
93. Hamazaki J, Iemura S-I, Natsume T, Yashiroda H, Tanaka K, Murata S. A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J 2006; 25: 4524-4536.
94. Rosenzweig R, Bronner V, Zhang D, Fushman D, Glickman MH. Rpn1 and Rpn2 coordinate ubiquitin processing factors at proteasome. J Biol Chem 2012; 287: 14659-14671.
95. Elsasser S, Gali RR, Schwickart M, et al. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat Cell Biol 2002; 4: 725-730.
96. Gomez TA, Kolawa N, Gee M, Sweredoski MJ, Deshaies RJ. Identification of a functional docking site in the Rpn1 LRR domain for the UBA-UBL domain protein Ddi1. BMC Biol 2011; 9: 33.
97. Haracska L, Udvardy A. Mapping the ubiquitin-binding domains in the p54 regulatory complex subunit of the Drosophila 26S protease. FEBS Lett 1997; 412: 331-336.
98. van Nocker S, Sadis S, Rubin DM, et al. The multiubiquitin-chain-binding protein Mcb1 is a component of the 26S proteasome in Saccharomyces cerevisiae and plays a nonessential, substrate-specific role in protein turnover. Mol Cell Biol 1996; 16: 6020-6028.
99. van Nocker S, Deveraux Q, Rechsteiner M, Vierstra RD. Arabidopsis MBP1 gene encodes a conserved ubiquitin recognition component of the 26S proteasome. Proc Natl Acad Sci USA 1996; 93: 856-860.
100. Lipinszki Z, Kiss P, Pál M, et al. Developmental-stage-specific regulation of the polyubiquitin receptors in Drosophila melanogaster. J Cell Sci 2009; 122: 3083-3092.
101. Verma R, Oania R, Graumann J, Deshaies RJ. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 2004; 118: 99-110.
102. Woelk T, Oldrini B, Maspero E, et al. Molecular mechanisms of coupled monoubiquitination. Nat Cell Biol 2006; 8: 1246-1254.
103. Di Fiore PP, Polo S, Hofmann K. When ubiquitin meets ubiquitin receptors: a signaling connection. Nat Rev Mol Cell Biol 2003; 4: 491-497.
104. Hofmann K, Bucher P. The UBA domain: A sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends Biochem Sci 1996; 21: 172-173.
105. Wilkinson CR, Seeger M, Hartmann-Petersen R, et al. Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nat Cell Biol 2001; 3: 939-943.
106. Elsasser S, Chandler-Mitilello D, Müller B, Hanna J, Finley D. Rad23 and Rpn10 serve as alternate ubiquitin receptors for the proteasome. J Biol Chem 2004; 279: 26817-26822.
107. Schauber C, Chen L, Tongaonkar P, et al. Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature 1998; 391: 715-718.
108. Hiyama H, Yokoi M, Masutani C, et al. Interaction of hHR23 with S5a. The ubiquitin-like domain of hHR23 mediates interaction with S5a subunit of 26S proteasome. J Biol Chem 1999; 274: 28019-28025.
109. Walters KJ, Kleijnen MF, Goh AM, Wagner G, Howley PM. Structural studies of the interaction between ubiquitin family proteins and proteasome subunit S5a. Biochemistry 2002; 41: 1767-1777.
110. Funakoshi M, Sasaki T, Nishimoto T, Kobayashi H. Budding yeast Dsk2p is a polyubiquitin-binding protein that can interact with the proteasome. Proc Natl Acad Sci USA 2002; 99: 745-750.
111. Biggins S, Ivanovska I, Rose MD. Yeast ubiquitin-like genes are involved in duplication of the microtubule organizing center. J Cell Biol 1996; 133: 1331-1346.
112. Matiuhin Y, Kirkpatrick DS, Ziv I, et al. Extraproteasomal Rpn10 restricts access of the polyubiquitin-binding protein Dsk2 to proteasome. Mol Cell 2008; 32: 415-425.
113. Zuin A, Bichmann A, Isasa M, Puig-Sàrries P, Díaz LM, Crosas B. Rpn10 monoubiquitination orchestrates the association of the ubiquilin-type DSK2 receptor with the proteasome. Biochem J 2015; 472: 353-365.
114. Ko HS, Uehara T, Tsuruma K, Nomura Y. Ubiquilin interacts with ubiquitylated proteins and proteasome through its ubiquitin-associated and ubiquitin-like domains. FEBS Lett 2004; 566: 110-114.
115. Hamazaki J, Hirayama S, Murata S. Redundant roles of Rpn10 and Rpn13 in recognition of ubiquitinated proteins and cellular homeostasis. PLoS Genet 2015; 11: 1-20.
116. Liu Y, Lü L, Hettinger CL, et al. Ubiquilin-1 protects cells from oxidative stress and ischemic stroke caused tissue injury in mice. J Neurosci 2014; 34: 2813-2821.
117. Wang H, Monteiro MJ. Ubiquilin interacts and enhances the degradation of expanded-polyglutamine proteins. Biochem Biophys Res Commun 2007; 360: 423-427.
118. Wang H, Lim PJ, Yin C, Rieckher M, Vogel BE, Monteiro MJ. Suppression of polyglutamine-induced toxicity in cell and animal models of Huntington's disease by ubiquilin. Hum Mol Genet 2006; 15: 1025-1041.
119. Haapasalo A, Viswanathan J, Kurkinen KM, et al. Involvement of ubiquilin-1 transcript variants in protein degradation and accumulation. Commun Integr Biol 2011; 4: 428-432.
120. Raasi S, Varadan R, Fushman D, Pickart CM. Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat Struct Mol Biol 2005; 12: 708-714.
121. Rosenzweig R, Osmulski PA, Gaczynska M, Glickman MH. The central unit within the 19S regulatory particle of the proteasome. Nat Struct Mol Biol 2008; 15: 573-580.
122. Ishii T, Funakoshi M, Kobayashi H. Yeast Pth2 is a UBL domain-binding protein that participates in the ubiquitin-proteasome pathway. EMBO J 2006; 25: 5492-5503.
123. Liang RY, Chen L, Ko BT, et al. Rad23 interaction with the proteasome is regulated by phosphorylation of its ubiquitin-like (UbL) domain. J Mol Biol 2014; 426: 4049-4060.
124. Kim I, Mi K, Rao H. Multiple interactions of rad23 suggest a mechanism for ubiquitylated substrate delivery important in proteolysis. Mol Biol Cell 2004; 15: 3357-3365.
125. Ortolan TG, Tongaonkar P, Lambertson D, Chen L, Schauber C, Madura K. The DNA repair protein rad23 is a negative regulator of multi-ubiquitin chain assembly. Nat Cell Biol 2000; 2: 601-608.
126. Raasi S, Pickart CM. Rad23 ubiquitin-associated domains (UBA) inhibit 26S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J Biol Chem 2003; 278: 8951-8959.
127. Richly H, Rape M, Braun S, Rumpf S, Hoege C, Jentsch S. A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 2005; 120: 73-84.
128. Kim I, Ahn J, Liu C, et al. The Png1-Rad23 complex regulates glycoprotein turnover. J Cell Biol 2006; 172: 211-219.
129. Heessen S, Masucci MG, Dantuma NP. The UBA2 domain functions as an intrinsic stabilization signal that protects rad23 from proteasomal degradation. Mol Cell 2005; 18: 225-235
130. Heinen C, Acs K, Hoogstraten D, Dantuma NP. C-terminal UBA domains protect ubiquitin receptors by preventing initiation of protein degradation. Nat Commun 2011; 2: 191.
131. Meyer H, Bug M, Bremer S. Emerging functions of the VCP/ p97 AAA-ATPase in the ubiquitin system. Nat Cell Biol 2012; 14: 117-123.
132. Stolz A, Hilt W, Buchberger A, Wolf DH. Cdc48: a power machine in protein degradation. Trends Biochem Sci 2011; 36: 515-523.
133. Alexandru G, Graumann J, Smith GT, Kolawa NJ, Fang R, Deshaies RJ. UBXD7 binds multiple ubiquitin ligases and implicates p97 in HIF1 turnover. Cell 2008; 134: 804-816.
134. Jentsch S, Rumpf S. Cdc48 (p97): a "molecular gearbox" in the ubiquitin pathway Trends Biochem Sci 2007; 32: 6-11.
135. Vadlamudi RK, Joung I, Strominger JL, Shin J. p62, a phosphotyrosine-independent ligand of the SH2 domain of p56 lck, belongs to a new class of ubiquitin-binding proteins. J Biol Chem 1996; 271: 20235-20237.
136. Seibenhener M, Babu J. Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol Cell Biol 2004; 24: 8055-8068.
137. Babu JR, Geetha T, Wooten MW. Sequestosome 1/p62 shuttles polyubiquitinated tau for proteasomal degradation. J Neurochem 2005; 94: 192-203.
138. Pankiv S, Clausen TH, Lamark T, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282: 24131-24145.
139. Hanna J, Hathaway NA, Tone Y, et al. Deubiquitinating enzyme Ubp6 functions noncatalytically to delay proteasomal degradation. Cell 2006; 127: 99-111.
140. Lam YA, Demartino GN, Pickart CM, Cohen RE, Chem JB. Specificity of the ubiquitin isopeptidase in the PA700 regulatory complex of 26S proteasomes. J Biol Chem 1997; 272: 28438-28446.
141. Aufderheide A, Beck F, Stengel F, et al. Structural characterization of the interaction of Ubp6 with the 26S proteasome. Proc Natl Acad Sci USA 2015; 112: 8626-8631.
142. Hu M, Li P, Song L, et al. Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. EMBO J 2005; 24: 3747-3756.
143. Lee BH, Lu Y, Prado MA, et al. USP14 deubiquitinates proteasome-bound substrates that are ubiquitinated at multiple sites. Nature 2016; 532: 398-401.
144. Bashore C, Dambacher CM, Goodall EA, Matyskiela ME, Lander GC, Martin A. Ubp6 deubiquitinase controls conformational dynamics and substrate degradation of the 26S proteasome. Nat Struct Mol Biol 2015; 22: 712-719.
145. Verma R, Aravind L, Oania R, et al. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 2002; 298: 611-615.
146. Wilkinson KD, Tashayev VL, O'Connor LB, Larsen CN, Kasperek E, Pickart CM. Metabolism of the polyubiquitin degradation signal: structure, mechanism, and role of isopeptidase T. Biochemistry 1995; 34: 14535-14546.
147. Hadari T, Warms JVB, Rose IA, Hershko A. A ubiquitin C-terminal isopeptidase that acts on polyubiquitin chains: Role in protein degradation. J Biol Chem 1992; 267: 719-727.
148. Amerik Ay, Swaminathan S, Krantz BA, Wilkinson KD, Hochstrasser M. In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome. EMBO J 1997; 16: 4826-4838.
149. Reyes-Turcu FE, Horton JR, Mullally JE, Heroux A, Cheng X, Wilkinson KD. The ubiquitin binding domain ZnF UBP recognizes the C-terminal diglycine motif of unanchored ubiquitin. Cell 2006; 124: 1197-1208.
150. Dayal S, Sparks A, Jacob J, Allende-Vega N, Lane DP, Saville MK. Suppression of the deubiquitinating enzyme USP5 causes the accumulation of unanchored polyubiquitin and the activation of p53. J Biol Chem 2009; 284: 5030-5041.
151. Zaiss DMW, Standera S, Holzhütter H, Kloetzel PM, Sijts AJAM. The proteasome inhibitor PI31 competes with PA28 for binding to 20S proteasomes. FEBS Lett 1999; 457: 333-338.
152. McCutchen-Maloney SL, Matsuda K, Shimbara N, et al. cDNA cloning, expression, and functional characterization of PI31, a proline-rich inhibitor of the proteasome. J Biol Chem 2000; 275: 18557-18565.
153. Zaiss DMW, Standera S, Kloetzel PM, Sijts AJAM. PI31 is a modulator of proteasome formation and antigen processing. Proc Natl Acad Sci USA 2002; 99: 14344-14349.
154. Bader M, Benjamin S, Wapinski OL, Smith DM, Goldberg AL, Steller H. A conserved F box regulatory complex controls proteasome activity in Drosophila. Cell 2011; 145: 371-382.
155. Li X, Thompson D, Kumar B, DeMartino GN. Molecular and cellular roles of PI31 (PSMF1) protein in regulation of proteasome function. J Biol Chem 2014; 289: 17392-17405.
156. Lee SYC, De La Mota-Peynado A, Roelofs J. Loss of Rpt5 protein interactions with the core particle and Nas2 protein causes the formation of faulty proteasomes that are inhibited by Ecm29 protein. J Biol Chem 2011; 286: 36641-36651.
157. De La Mota-Peynado A, Lee SYC, Pierce BM, Wani P, Singh CR, Roelofs J. The proteasome-associated protein Ecm29 inhibits proteasomal ATPase activity and in vivo protein degradation by the proteasome. J Biol Chem 2013; 288: 29467-29481.
158. Lehmann A, Niewienda A, Jechow K, Janek K, Enenkel C. Ecm29 fulfils quality control functions in proteasome assembly. Mol Cell 2010; 38: 879-888.
159. Park S, Kim W, Tian G, Gygi SP, Finley D. Structural defects in the regulatory particle-core particle interface of the proteasome induce a novel proteasome stress response. J Biol Chem 2011; 286: 36652-36666.
160. Wang X, Yen J, Kaiser P, Huang L. Regulation of the 26S proteasome complex during oxidative stress. Sci Signal 2010; 3: ra88.
161. Davies KJ a. Degradation of oxidized proteins by the 20S proteasome. Biochimie 2001; 83: 301-310.
162. Breusing N, Grune T. Regulation of proteasome-mediated protein degradation during oxidative stress and aging. Biol Chem 2008; 389: 203-209.
163. Haratake K, Sato A, Tsuruta F, Chiba T. KIAA0368-deficiency affects disassembly of 26S proteasome under oxidative stress condition. J Biochem 2016; 159: 609-618.
164. Gorbea C, Goellner GM, Teter K, Holmes RK, Rechsteiner M. Characterization of mammalian Ecm29, a 26S proteasome-associated protein that localizes to the nucleus and membrane vesicles. J Biol Chem 2004; 279: 54849-54861.
165. Gorbea C, Pratt G, Ustrell V, et al. A protein interaction network for Ecm29 links the 26S proteasome to molecular motors and endosomal components. J Biol Chem 2010; 285: 31616-31633.
166. Kish-Trier E, Hill CP. Structural biology of the proteasome. Annu Rev Biophys 2013; 42: 29-49.
167. Li X, Lonard DM, Jung SY, et al. The SRC-3/AIB1 coactivator is degraded in a ubiquitin-and ATP-independent manner by the REG? proteasome. Cell 2006; 124: 381-392.
168. Li X, Amazit L, Long W, Lonard DM, Monaco JJ, O'Malley BW. Ubiquitin-and ATP-independent proteolytic turnover of p21 by the REG-proteasome pathway. Mol Cell 2007; 26: 831-842.
169. Chen X, Barton LF, Chi Y, Clurman BE, Roberts JM. Ubiquitin-independent degradation of cell-cycle inhibitors by the REG proteasome. Mol Cell 2007; 26: 843-852.
170. Fabre B, Lambour T, Garrigues L, et al. Deciphering preferential interactions within supramolecular protein complexes: the proteasome case. Mol Syst Biol 2015; 11: 771.
171. Fabre B, Lambour T, Garrigues L, et al. Label-free quantitative proteomics reveals the dynamics of proteasome complexes composition and stoichiometry in a wide range of human cell lines. J Proteome Res 2014; 13: 3027-3037.
172. Lander GC, Estrin E, Matyskiela ME, Bashore C, Nogales E, Martin A. Complete subunit architecture of the proteasome regulatory particle. Nature 2012; 482: 186-191.
173. Beck F, Unverdorben P, Bohn S, et al. Near-atomic resolution structural model of the yeast 26S proteasome. Proc Natl Acad Sci USA 2012; 109: 14870-14875.
174. Lasker K, Förster F, Bohn S, et al. Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci USA 2012; 109: 1380-1387.
175. Unverdorben P, Beck F, Sledz P, et al. Deep classification of a large cryo-EM dataset defines the conformational landscape of the 26S proteasome. Proc Natl Acad Sci USA 2014; 111: 5544-5549.
176. Matyskiela ME, Lander GC, Martin A. Conformational switching of the 26S proteasome enables substrate degradation. Nat Struct Mol Biol 2013; 20: 781-788.
177. led P, Unverdorben P, Beck F, et al. Structure of the 26S proteasome with ATP-S bound provides insights into the mechanism of nucleotide-dependent substrate translocation. Proc Natl Acad Sci USA 2013; 110: 7264-7269.
178. Asano S, Fukuda Y, Beck F, et al. Proteasomes. A molecular census of 26S proteasomes in intact neurons. Science 2015; 347: 439-442.
179. Luan B, Huang X, Wu J, et al. Structure of an endogenous yeast 26S proteasome reveals two major conformational states. Proc Natl Acad Sci USA 2016; 113: 2642-2647.
180. da Fonseca PCA, Morris EP. Structure of the human 26S proteasome: subunit radial displacements open the gate into the proteolytic core. J Biol Chem 2008; 283: 23305-23314.
181. Gillette TG, Kumar B, Thompson D, Slaughter CA, DeMartino GN. Differential roles of the COOH termini of AAA subunits of PA700 (19S regulator) in asymmetric assembly and activation of the 26S proteasome. J Biol Chem 2008; 283: 31813-31822.
182. Schmidt T, Lindenberg KS, Krebs A, et al. Protein surveillance machinery in brains with spinocerebellar ataxia type 3: redistribution and differential recruitment of 26S proteasome subunits and chaperones to neuronal intranuclear inclusions. Ann Neurol 2002; 51: 302-310.
183. Stenoien DL, Cummings CJ, Adams HP, et al. Polyglutamine-expanded androgen receptors form aggregates that sequester heat shock proteins, proteasome components and SRC-1, and are suppressed by the HDJ-2 chaperone. Hum Mol Genet 1999; 8: 731-741.
184. Schipper-Krom S, Juenemann K, Jansen AH, et al. Dynamic recruitment of active proteasomes into polyglutamine initiated inclusion bodies. FEBS Lett 2014; 588: 151-159.
185. Davies SW, Turmaine M, Cozens BA, et al. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 1997; 90: 537-548.
186. Rousseau E, Kojima R, Hoffner G, Djian P, Bertolotti A. Misfolding of proteins with a polyglutamine expansion is facilitated by proteasomal chaperones. J Biol Chem 2009; 284: 1917-1929.
187. Cummings CJ, Mancini MA, Antalffy B, DeFranco DB, Orr HT, Zoghbi HY. Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat Genet 1998; 19: 148-154.
188. DiFiglia M. Aggregation of Huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997; 277: 1990-1993.
189. Jana NR. Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum Mol Genet 2001; 10: 1049-1059.
190. McCampbell A, Fischbeck KH. Polyglutamine and CBP: fatal attraction? Nat Med 2001; 7: 528-530.
191. Dantuma NP, Bott LC. The ubiquitin-proteasome system in neurodegenerative diseases: precipitating factor, yet part of the solution. Front Mol Neurosci 2014; 7: 70.
192. Maynard CJ, Böttcher C, Ortega Z, et al. Accumulation of ubiquitin conjugates in a polyglutamine disease model occurs without global ubiquitin/proteasome system impairment. Proc Natl Acad Sci USA 2009; 106: 13986-13991.
193. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001; 292: 1552-1555.
194. Hipp MS, Patel CN, Bersuker K, et al. Indirect inhibition of 26S proteasome activity in a cellular model of Huntington's disease. J Cell Biol 2012; 196: 573-587.
195. Myeku N, Clelland CL, Emrani S, et al. Tau-driven 26S proteasome impairment and cognitive dysfunction can be prevented early in disease by activating cAMP-PKA signaling. Nat Med 2015; 22: 46-53.
196. Hegde AN. Ubiquitin-proteasome-mediated local protein degradation and synaptic plasticity. Prog Neurobiol 2004; 73: 311-357.
197. Pinto MJ, Alves PL, Martins L, et al. The proteasome controls presynaptic differentiation through modulation of an onsite pool of polyubiquitinated conjugates. J Cell Biol 2016; 212: 789-801.
198. Tsai NP. Ubiquitin proteasome system-mediated degradation of synaptic proteins: An update from the postsynaptic side. Biochim Biophys Acta 2014; 1843: 2838-2842.
199. Ferreira JS, Schmidt J, Rio P, et al. GluN2B-containing NMDA receptors regulate AMPA receptor traffic through anchoring of the synaptic proteasome. J Neurosci 2015; 35: 8462-8479.
200. Lallemand-Breitenbach V, Zhu J, Chen Z, de Thé H. Curing APL through PML/RARA degradation by As2O3. Trends Mol Med 2012; 18: 36-42.
201. Ivanschitz L, Takahashi Y, Jollivet F, Ayrault O, Le Bras M, de Thé H. PML IV/ARF interaction enhances p53 SUMO-1 conjugation, activation, and senescence. Proc Natl Acad Sci USA 2015; 112: 14278-14283.
202. Lallemand-Breitenbach V, de Thé H. PML nuclear bodies. Cold Spring Harb Perspect Biol 2010; 2: a000661.
203. Fabunmi RP, Wigley WC, Thomas PJ, DeMartino GN. Interferon regulates accumulation of the proteasome activator PA28 and immunoproteasomes at nuclear PML bodies. J Cell Sci 2001; 114: 29-36.
204. Lallemand-Breitenbach V, Zhu J, Puvion F, et al. Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-induced PML or PML/retinoic acid receptor degradation. J Exp Med 2001; 193: 1361-1371.
205. Guo L, Giasson BI, Glavis-Bloom A, et al. A cellular system that degrades misfolded proteins and protects against neurodegeneration. Mol Cell 2014; 55: 15-30.
206. Wigley CW, Fabunmi RP, Lee MG, et al. Dynamic association of proteasomal machinery with the centrosome. J Cell Biol 1999; 145: 481-490.
207. Puram S V., Kim AH, Park HY, Anckar J, Bonni A. The ubiquitin receptor S5a/Rpn10 links centrosomal proteasomes with dendrite development in the mammalian brain. Cell Rep 2013; 4: 19-30.
208. Ng W, Sergeyenko T, Zeng N, Brown JD, Römisch K. Characterization of the proteasome interaction with the Sec61 channel in the endoplasmic reticulum. J Cell Sci 2007; 120: 682-691.
209. Kalies K-U, Allan S, Sergeyenko T, Kröger H, Römisch K. The protein translocation channel binds proteasomes to the endoplasmic reticulum membrane. EMBO J 2005; 24: 2284-2293.
210. Kaiser ML, Römisch K. Proteasome 19S RP binding to the Sec61 channel plays a key role in ERAD. PLoS One 2015; 10: 1-19.
211. Azzu V, Brand MD. Degradation of an intramitochondrial protein by the cytosolic proteasome. J Cell Sci 2010; 123: 578-585.
212. Chan NC, Salazar AM, Pham AH, et al. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet 2011; 20: 1726-1737.
213. Nakagawa T, Shirane M, Lemura SI, Natsume T, Nakayama KI. Anchoring of the 26S proteasome to the organellar membrane by FKBP38. Genes to Cells 2007; 12: 709-719.
214. Sun XM, Butterworth M, MacFarlane M, Dubiel W, Ciechanover A, Cohen GM. Caspase activation inhibits proteasome function during apoptosis. Mol Cell 2004; 14: 81-93.
215. Adrain C, Creagh EM, Cullen SP, Martin SJ. Caspase-dependent inactivation of proteasome function during programmed cell death in Drosophila and man. J Biol Chem 2004; 279: 36923-36930.
216. Cuervo AM, Palmer A, Rivett AJ, Knecht E. Degradation of proteasomes by lysosomes in rat liver. Eur J Biochem 1995; 227: 792-800.
217. Waite KA, De-La Mota-Peynado A, Vontz G, Roelofs J. Starvation induces proteasome autophagy with different pathways for core and regulatory particle. J Biol Chem 2015; 291: 3239-3253.