Gates, Channels, and Switches: Elements of the Proteasome Machine

Trends in Biochemical Sciences

Volumn 41, Issue 1, 2016, Pages 77-93

  Finley, Daniel ^a   Chen, Xiang ^b   Walters, Kylie J ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

ATPase; Proteasome; Protein degradation; Ubiquitin

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HOLOENZYME; PROTEASOME; UBIQUITIN; ADENOSINE TRIPHOSPHATE; ION CHANNEL; PROTEIN;

CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; ENZYME ACTIVE SITE; HYDROLYSIS KINETICS; MOLECULAR MODEL; MOLECULAR RECOGNITION; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN HYDROLYSIS; PROTEIN UNFOLDING; REVIEW; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; UBIQUITINATION; CHANNEL GATING; HUMAN; METABOLISM; THERMODYNAMICS;

ADENOSINE TRIPHOSPHATE; HUMANS; ION CHANNEL GATING; ION CHANNELS; MODELS, MOLECULAR; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEINS; THERMODYNAMICS;

EID: 84952639230     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2015.10.009     Document Type: Review

References (158)

1. Groll M., et al. Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 1997, 386:463-471.
2. Whitby F.G., et al. Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 2000, 408:115-120.
3. Groll M., et al. A gated channel into the proteasome core particle. Nat. Struct. Biol. 2000, 7:1062-1067.
4. Weber-Ban E.U., et al. Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature 1999, 401:90-93.
5. Leev C. ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell 2001, 7:627-637.
6. Sauer R.T., Baker T.A. AAA+ proteases: ATP-fueled machines of protein destruction. Annu. Rev. Biochem. 2011, 80:587-612.
7. Nyquist K., Martin A. Marching to the beat of the ring: polypeptide translocation by AAA+ proteases. Trends Biochem. Sci. 2014, 39:53-60.
8. Lasker K., et al. Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:1380-1387.
9. Beck F., et al. Near-atomic resolution structural model of the yeast 26S proteasome. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:14870-14875.
10. Lander G.C., et al. Complete subunit architecture of the proteasome regulatory particle. Nature 2012, 482:186-191.
11. da Fonseca P.C., et al. Molecular model of the human 26S proteasome. Mol. Cell 2012, 46:54-66.
12. Glickman M.H., et al. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 1998, 94:615-623.
13. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 2009, 78:477-513.
14. Tomko R.J., Hochstrasser M. Molecular architecture and assembly of the eukaryotic proteasome. Annu. Rev. Biochem. 2013, 82:415-445.
15. Verma R., et al. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 2002, 298:611-615.
16. Yao T., Cohen R.E. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 2002, 419:403-407.
17. Worden E.J., et al. Structure of the Rpn11-Rpn8 dimer reveals mechanisms of substrate deubiquitination during proteasomal degradation. Nat. Struct. Mol. Biol. 2014, 21:220-227.
18. Pathare G.R., et al. Crystal structure of the proteasomal deubiquitylation module Rpn8-Rpn11. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:2984-2989.
19. Husnjak K., et al. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 2008, 453:481-488.
20. Schreiner P., et al. Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 2008, 453:548-552.
21. Hamazaki J., et al. Redundant roles of Rpn10 and Rpn13 in recognition of ubiquitinated proteins and cellular homeostasis. PLoS Genet. 2015, 11:e1005401.
22. Elsasser S., Finley D. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat. Cell Biol. 2005, 7:742-749.
23. Hiyama H., et al. Interaction of hHR23 with S5a. The ubiquitin-like domain of hHR23 mediates interaction with S5a subunit of 26 S proteasome. J. Biol. Chem. 1999, 274:28019-28025.
24. Walters K.J., et al. Structural studies of the interaction between ubiquitin family proteins and proteasome subunit S5a. Biochemistry 2002, 41:1767-1777.
25. Bertolaet B.L., et al. UBA domains of DNA damage-inducible proteins interact with ubiquitin. Nat. Struct. Biol. 2001, 8:417-422.
26. Chen L., et al. Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition of multi-ubiquitin chain assembly. EMBO Rep. 2001, 2:933-938.
27. Benaroudj N., et al. ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation. Mol. Cell 2003, 11:69-78.
28. Smith D.M., et al. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol. Cell 2007, 27:731-744.
29. Zhang F., et al. Structural insights into the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol. Cell 2009, 34:473-484.
30. Djuranovic S., et al. Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol. Cell 2009, 34:580-590.
31. Rubin D.M., et al. Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 1998, 17:4909-4919.
32. Erales J., et al. Functional asymmetries of proteasome translocase pore. J. Biol. Chem. 2012, 287:18535-18543.
33. Beckwith R., et al. Reconstitution of the 26S proteasome reveals functional asymmetries in its AAA+ unfoldase. Nat. Struct. Mol. Biol. 2013, 20:1164-1172.
34. Peth A., et al. The ATP costs and time required to degrade ubiquitinated proteins by the 26 S proteasome. J. Biol. Chem. 2013, 288:29215-29222.
35. Pathare G.R., et al. The proteasomal subunit Rpn6 is a molecular clamp holding the core and regulatory subcomplexes together. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:149-154.
36. Tian G., et al. An asymmetric interface between the regulatory and core particles of the proteasome. Nat. Struct. Mol. Biol. 2011, 18:1259-1267.
37. Park S., et al. Reconfiguration of the proteasome during chaperone-mediated assembly. Nature 2013, 497:512-516.
38. Sokolova V., et al. Proteasome activation is mediated via a functional switch of the Rpt6 C-terminal tail following chaperone-dependent assembly. Sci. Rep. 2015, 5:14909.
39. Sledz P., et al. Structure of the 26S proteasome with ATP-gammaS bound provides insights into the mechanism of nucleotide-dependent substrate translocation. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:7264-7269.
40. Inobe T., Genmei R. N-Terminal coiled-coil structure of ATPase subunits of 26S proteasome Is crucial for proteasome function. PLoS ONE 2015, 10:e0134056.
41. Prakash S., et al. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 2004, 11:830-837.
42. Fishbain S., et al. Sequence composition of disordered regions fine-tunes protein half-life. Nat. Struct. Mol. Biol. 2015, 22:214-221.
43. van der Lee R., et al. Intrinsically disordered segments affect protein half-life in the cell and during evolution. Cell Rep. 2014, 8:1832-1844.
44. Fishbain S., et al. Rad23 escapes degradation because it lacks a proteasome initiation region. Nat. Commun. 2011, 2:192.
45. Inobe T., et al. Defining the geometry of the two-component proteasome degron. Nat. Chem. Biol. 2011, 7:161-167.
46. Palombella V.J., et al. The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 1994, 78:773-785.
47. Tian L., et al. A conserved processing mechanism regulates the activity of transcription factors Cubitus interruptus and NF-kappaB. Nat. Struct. Mol. Biol. 2005, 12:1045-1053.
48. Schrader E.K., et al. A three-part signal governs differential processing of Gli1 and Gli3 proteins by the proteasome. J. Biol. Chem. 2011, 286:39051-39058.
49. Hoppe T., et al. Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 2000, 102:577-586.
50. Rape M., et al. Mobilization of processed, membrane-tethered SPT23 transcription factor by CDC48(UFD1/NPL4), a ubiquitin-selective chaperone. Cell 2001, 107:667-677.
51. Rape M., Jentsch S. Productive RUPture: activation of transcription factors by proteasomal processing. Biochim. Biophys. Acta 2004, 1695:209-213.
52. Zanet J., et al. Pri sORF peptides induce selective proteasome-mediated protein processing. Science 2015, 349:1356-1358.
53. Unverdorben P., et al. Deep classification of a large cryo-EM dataset defines the conformational landscape of the 26S proteasome. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:5544-5549.
54. Matyskiela M.E., et al. Conformational switching of the 26S proteasome enables substrate degradation. Nat. Struct. Mol. Biol. 2013, 20:781-788.
55. Peth A., et al. ATP-dependent steps in the binding of ubiquitin conjugates to the 26S proteasome that commit to degradation. Mol. Cell 2010, 40:671-681.
56. Asano S., et al. Proteasomes. A molecular census of 26S proteasomes in intact neurons. Science 2015, 347:439-442.
57. Iosefson O., et al. Coordinated gripping of substrate by subunits of a AAA+ proteolytic machine. Nat. Chem. Biol. 2015, 11:201-206.
58. Iosefson O., et al. Dissection of axial-pore loop function during unfolding and translocation by a AAA+ proteolytic machine. Cell Rep. 2015, 12:1032-1041.
59. Estrin E., et al. Formation of an intricate helical bundle dictates the assembly of the 26S proteasome lid. Structure 2013, 21:1624-1635.
60. Lu Y., et al. Substrate degradation by the proteasome: a single-molecule kinetic analysis. Science 2015, 348:1250834.
61. Wang Q., et al. Structure of S5a bound to monoubiquitin provides a model for polyubiquitin recognition. J. Mol. Biol. 2005, 348:727-739.
62. Zhang N., et al. Structure of the s5a:k48-linked diubiquitin complex and its interactions with rpn13. Mol. Cell 2009, 35:280-290.
63. Zhang D., et al. Together, Rpn10 and Dsk2 can serve as a polyubiquitin chain-length sensor. Mol. Cell 2009, 36:1018-1033.
64. Deveraux Q., et al. A 26 S protease subunit that binds ubiquitin conjugates. J. Biol. Chem. 1994, 269:7059-7061.
65. Elsasser S., et al. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 2002, 4:725-730.
66. Deng H.X., et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
67. Tomko R.J., Hochstrasser M. The intrinsically disordered Sem1 protein functions as a molecular tether during proteasome lid biogenesis. Mol. Cell 2014, 53:433-443.
68. Bohn S., et al. Localization of the regulatory particle subunit Sem1 in the 26S proteasome. Biochem. Biophys. Res. Commun. 2013, 435:250-254.
69. Paraskevopoulos K., et al. Dss1 is a 26S proteasome ubiquitin receptor. Mol. Cell 2014, 56:453-461.
70. Aufderheide A., et al. Structural disorder and its role in proteasomal degradation. FEBS Lett. 2015, 589:2552-2560.
71. Thrower J.S., et al. Recognition of the polyubiquitin proteolytic signal. EMBO J. 2000, 19:94-102.
72. Kravtsova-Ivantsiv Y., et al. Modification by single ubiquitin moieties rather than polyubiquitination is sufficient for proteasomal processing of the p105 NF-kappaB precursor. Adv. Exp. Med. Biol. 2011, 691:95-106.
73. Dimova N.V., et al. APC/C-mediated multiple monoubiquitylation provides an alternative degradation signal for cyclin B1. Nat. Cell Biol. 2012, 14:168-176.
74. Shabek N., et al. The size of the proteasomal substrate determines whether its degradation will be mediated by mono- or polyubiquitylation. Mol. Cell 2012, 48:87-97.
75. Kulathu Y., Komander D. Atypical ubiquitylation - the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 2012, 13:508-523.
76. Meyer H.J., Rape M. Enhanced protein degradation by branched ubiquitin chains. Cell 2014, 157:910-921.
77. Kirkpatrick D.S., et al. Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nat. Cell Biol. 2006, 8:700-710.
78. Jin L., et al. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 2008, 133:653-665.
79. Xu P., et al. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009, 137:133-145.
80. Hofmann R.M., Pickart C.M. In vitro assembly and recognition of Lys-63 polyubiquitin chains. J. Biol. Chem. 2001, 276:27936-27943.
81. Saeki Y., et al. Lysine 63-linked polyubiquitin chain may serve as a targeting signal for the 26S proteasome. EMBO J. 2009, 28:359-371.
82. Jacobson A.D., et al. The lysine 48 and lysine 63 ubiquitin conjugates are processed differently by the 26 s proteasome. J. Biol. Chem. 2009, 284:35485-35494.
83. Nathan J.A., et al. Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes?. EMBO J. 2013, 32:552-565.
84. Schmidtke G., et al. FAT10ylation as a signal for proteasomal degradation. Biochim. Biophys. Acta 2014, 1843:97-102.
85. Godderz D., et al. The N-terminal unstructured domain of yeast ODC functions as a transplantable and replaceable ubiquitin-independent degron. J. Mol. Biol. 2011, 407:354-367.
86. Rani N., et al. FAT10 and NUB1L bind to the VWA domain of Rpn10 and Rpn1 to enable proteasome-mediated proteolysis. Nat. Commun. 2012, 3:749.
87. Tanji K., et al. Interaction of NUB1 with the proteasome subunit S5a. Biochem. Biophys. Res. Commun. 2005, 337:116-120.
88. Hanna J., et al. Deubiquitinating enzyme Ubp6 functions noncatalytically to delay proteasomal degradation. Cell 2006, 127:99-111.
89. Hanna J., et al. A ubiquitin stress response induces altered proteasome composition. Cell 2007, 129:747-759.
90. Lee B.H., et al. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 2010, 467:179-184.
91. Hanna J., et al. Ubiquitin depletion as a key mediator of toxicity by translational inhibitors. Mol. Cell. Biol. 2003, 23:9251-9261.
92. Hershko A., Rose I.A. Ubiquitin-aldehyde: a general inhibitor of ubiquitin-recycling processes. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:1829-1833.
93. Ekkebus R., et al. Catching a DUB in the act: novel ubiquitin-based active site directed probes. Curr. Opin. Chem. Biol. 2014, 23:63-70.
94. Peth A., et al. Ubiquitinated proteins activate the proteasome by binding to Usp14/Ubp6, which causes 20S gate opening. Mol. Cell 2009, 36:794-804.
95. Bashore C., et al. Ubp6 deubiquitinase controls conformational dynamics and substrate degradation of the 26S proteasome. Nat. Struct. Mol. Biol. 2015, 22:712-719.
96. Aufderheide A., et al. Structural characterization of the interaction of Ubp6 with the 26S proteasome. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:8626-8631.
97. Lam Y.A., et al. Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 1997, 385:737-740.
98. Yao T., et al. Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the Ino80 chromatin-remodeling complex. Mol. Cell 2008, 31:909-917.
99. Yao T., et al. Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat. Cell Biol. 2006, 8:994-1002.
100. Hamazaki J., et al. A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J. 2006, 25:4524-4536.
101. Qiu X.B., et al. hRpn13/ADRM1/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37. EMBO J. 2006, 25:5742-5753.
102. Chen X., et al. Structure of proteasome ubiquitin receptor hRpn13 and its activation by the scaffolding protein hRpn2. Mol. Cell 2010, 38:404-415.
103. Sahtoe D.D., et al. Mechanism of UCH-L5 activation and inhibition by DEUBAD domains in RPN13 and INO80G. Mol. Cell 2015, 57:887-900.
104. VanderLinden R.T., et al. Structural basis for the activation and inhibition of the UCH37 deubiquitylase. Mol. Cell 2015, 57:901-911.
105. Chen X., Walters K.J. Structural plasticity allows UCH37 to be primed by RPN13 or locked down by INO80G. Mol. Cell 2015, 57:767-768.
106. Fort P., et al. Evolution of proteasome regulators in eukaryotes. Genome Biol. Evol. 2015, 7:1363-1379.
107. Kish-Trier E., Hill C.P. Structural biology of the proteasome. Annu. Rev. Biophys. 2013, 42:29-49.
108. Barthelme D., Sauer R.T. Identification of the Cdc48*20S proteasome as an ancient AAA+ proteolytic machine. Science 2012, 337:843-846.
109. Barthelme D., et al. An ALS disease mutation in Cdc48/p97 impairs 20S proteasome binding and proteolytic communication. Protein Sci. 2015, 24:1521-1527.
110. Tar K., et al. Proteasomes associated with the Blm10 activator protein antagonize mitochondrial fission through degradation of the fission protein Dnm1. J. Biol. Chem. 2014, 289:12145-12156.
111. Dange T., et al. Blm10 protein promotes proteasomal substrate turnover by an active gating mechanism. J. Biol. Chem. 2011, 286:42830-42839.
112. Li X., et al. Ubiquitin- and ATP-independent proteolytic turnover of p21 by the REGgamma-proteasome pathway. Mol. Cell 2007, 26:831-842.
113. Chen X., et al. Ubiquitin-independent degradation of cell-cycle inhibitors by the REGgamma proteasome. Mol. Cell 2007, 26:843-852.
114. Qian M.X., et al. Acetylation-mediated proteasomal degradation of core histones during DNA repair and spermatogenesis. Cell 2013, 153:1012-1024.
115. Li X., et al. The SRC-3/AIB1 coactivator is degraded in a ubiquitin- and ATP-independent manner by the REGgamma proteasome. Cell 2006, 124:381-392.
116. Moriishi K., et al. Proteasome activator PA28gamma-dependent nuclear retention and degradation of hepatitis C virus core protein. J. Virol. 2003, 77:10237-10249.
117. Lopez A.D., et al. Proteasomal degradation of Sfp1 contributes to the repression of ribosome biogenesis during starvation and is mediated by the proteasome activator Blm10. Mol. Biol. Cell 2011, 22:528-540.
118. Cascio P. PA28alphabeta: the enigmatic magic ring of the proteasome?. Biomolecules 2014, 4:566-584.
119. Tanahashi N., et al. Hybrid proteasomes. Induction by interferon-gamma and contribution to ATP-dependent proteolysis. J. Biol. Chem. 2000, 275:14336-14345.
120. Buchberger A., et al. Control of p97 function by cofactor binding. FEBS Lett. 2015, 589:2578-2589.
121. Richly H., et al. A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 2005, 120:73-84.
122. Kim I., et al. Multiple interactions of rad23 suggest a mechanism for ubiquitylated substrate delivery important in proteolysis. Mol. Biol. Cell 2004, 15:3357-3365.
123. Leggett D.S., et al. Multiple associated proteins regulate proteasome structure and function. Mol. Cell 2002, 10:495-507.
124. Crosas B., et al. Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities. Cell 2006, 127:1401-1413.
125. Besche H.C., et al. Autoubiquitination of the 26S proteasome on Rpn13 regulates breakdown of ubiquitin conjugates. EMBO J. 2014, 33:1159-1176.
126. Jacobson A.D., et al. Autoregulation of the 26S proteasome by in situ ubiquitination. Mol. Biol. Cell 2014, 25:1824-1835.
127. Park S., et al. 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.
128. Fang N.N., et al. Hul5 HECT ubiquitin ligase plays a major role in the ubiquitylation and turnover of cytosolic misfolded proteins. Nat. Cell. Biol. 2011, 13:1344-1352.
129. Kohlmann S., et al. Ubiquitin ligase Hul5 is required for fragment-specific substrate degradation in endoplasmic reticulum-associated degradation. J. Biol. Chem. 2008, 283:16374-16383.
130. Aviram S., Kornitzer D. The ubiquitin ligase Hul5 promotes proteasomal processivity. Mol. Cell Biol. 2010, 30:985-994.
131. Martinez-Noel G., et al. Identification and proteomic analysis of distinct UBE3A/E6AP protein complexes. Mol. Cell Biol. 2012, 32:3095-3106.
132. Chu B.W., et al. The E3 ubiquitin ligase UBE3C enhances proteasome processivity by ubiquitinating partially proteolyzed substrates. J. Biol. Chem. 2013, 288:34575-34587.
133. De La Mota-Peynado A., et al. The proteasome-associated protein Ecm29 inhibits proteasomal ATPase activity and in vivo protein degradation by the proteasome. J. Biol. Chem. 2013, 288:29467-29481.
134. Wang X., et al. Regulation of the 26S proteasome complex during oxidative stress. Sci. Signal. 2010, 3:ra88.
135. Lee S.Y., et al. 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.
136. Livnat-Levanon N., et al. Reversible 26S proteasome disassembly upon mitochondrial stress. Cell Rep. 2014, 7:1371-1380.
137. Marshall R.S., et al. Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol. Cell 2015, 58:1053-1066.
138. Xie Y., Varshavsky A. RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:3056-3061.
139. Radhakrishnan S.K., et al. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 2010, 38:17-28.
140. Steffen J., et al. Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol. Cell 2010, 40:147-158.
141. Radhakrishnan S.K., et al. p97-dependent retrotranslocation and proteolytic processing govern formation of active Nrf1 upon proteasome inhibition. Elife 2014, 3:e01856.
142. Sha Z., Goldberg A.L. Proteasome-mediated processing of Nrf1 is essential for coordinate induction of all proteasome subunits and p97. Curr. Biol. 2014, 24:1573-1583.
143. Li X., et al. Specific SKN-1/Nrf stress responses to perturbations in translation elongation and proteasome activity. PLoS Genet. 2011, 7:e1002119.
144. Zhang Y., Manning B.D. mTORC1 signaling activates NRF1 to increase cellular proteasome levels. Cell Cycle 2015, 14:2011-2017.
145. Vilchez D., et al. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature 2012, 489:304-308.
146. Vilchez D., et al. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 2012, 489:263-268.
147. Cho-Park P.F., Steller H. Proteasome regulation by ADP-ribosylation. Cell 2013, 153:614-627.
148. Djakovic S.N., et al. Phosphorylation of Rpt6 regulates synaptic strength in hippocampal neurons. J. Neurosci. 2012, 32:5126-5131.
149. Guo X., et al. UBLCP1 is a 26S proteasome phosphatase that regulates nuclear proteasome activity. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:18649-18654.
150. Goldberg A.L. Development of proteasome inhibitors as research tools and cancer drugs. J. Cell Biol. 2012, 199:583-588.
151. Huber E.M., Groll M. Inhibitors for the immuno- and constitutive proteasome: current and future trends in drug development. Angew. Chem. Int. Ed. Engl. 2012, 51:8708-8720.
152. Schmidt M., Finley D. Regulation of proteasome activity in health and disease. Biochim. Biophys. Acta 2014, 1843:13-25.
153. Brehm A., et al. Additive loss-of-function proteasome subunit mutations in CANDLE/PRAAS patients promote type I IFN production. J. Clin. Invest. 2015, 125:4196-4211.
154. Sahara K., et al. The mechanism for molecular assembly of the proteasome. Adv. Biol. Regul. 2014, 54:51-58.
155. Kunjappu M.J., Hochstrasser M. Assembly of the 20S proteasome. Biochim. Biophys. Acta 2014, 1843:2-12.
156. Saeki Y., Tanaka K. Assembly and function of the proteasome. Methods Mol. Biol. 2012, 832:315-337.
157. Kniepert A., Groettrup M. The unique functions of tissue-specific proteasomes. Trends Biochem. Sci. 2014, 39:17-24.
158. Murata S., et al. Regulation of CD8+ T cell development by thymus-specific proteasomes. Science 2007, 316:1349-1353.