Cited by 1,764Ubiquitin and proteasome pathwaysHeat shock proteins researchProtein Degradation and Inhibitors

Recognition and Processing of Ubiquitin-Protein Conjugates by the Proteasome

Open access
Finley, Daniel·2009·Annual Review of Biochemistry

Abstract

The proteasome is an intricate molecular machine, which serves to degrade proteins following their conjugation to ubiquitin. Substrates dock onto the proteasome at its 19-subunit regulatory particle via a diverse set of ubiquitin receptors and are then translocated into an internal chamber within the 28-subunit proteolytic core particle (CP), where they are hydrolyzed. Substrate is threaded into the CP through a narrow gated channel, and thus translocation requires unfolding of the substrate. Six distinct ATPases in the regulatory particle appear to form a ring complex and to drive unfolding as well as translocation. ATP-dependent, degradation-coupled deubiquitination of the substrate is required both for efficient substrate degradation and for preventing the degradation of the ubiquitin tag. However, the proteasome also contains deubiquitinating enzymes (DUBs) that can remove ubiquitin before substrate degradation initiates, thus allowing some substrates to dissociate from the proteasome and escape degradation. Here we examine the key elements of this molecular machine and how they cooperate in the processing of proteolytic substrates.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1146/annurev.biochem.78.081507.101607

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 206

  1. [1]Coux O Tanaka K Goldberg AL 1996 Structure and functions of the 20S and 26S proteasomes Ann Rev Biochem 65 810 47 8811196
  2. [2]Pickart CM Cohen RE 2004 Proteasomes and their kin: proteases in the machine age Nat Rev Mol Cell Biol 5 177 87 14990998
  3. [3]Downes B Vierstra RD 2005 Post-translational regulation in plants employing a diverse set of polypeptide tags Biochem Soc Trans 33 393 99 15787614
  4. [4]Groll M Ditzel L Lowe J Stock D Bochtler M 1997 Structure of 20S proteasome from yeast at 2.4 Å resolution Nature 386 463 71 9087403
  5. [5]Borisssenko L Groll M 2007 20S Proteasome and its inhibitors: crystallographic knowledge for drug development Chem Rev 107 687 717 17316053
  6. [6]Groll M Bajorek M Kohler A Huber R Glickman MH 2000 A gated channel into the proteasome core particle Nature Struct Biol 7 1062 67 11062564
  7. [7]Kohler A Cascio P Leggett DL Woo KM Goldberg AL 2001 The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release Mol Cell 7 1143 52 11430818
  8. [8]Whitby FG Masters EI Kramer L Knowlton JR Yao Y 2000 Structural basis for the activation of 20S proteasomes by 11S regulators Nature 408 115 20 11081519
  9. [9]Forster A Masters EI Whitby FG Robinson H Hill CP 2005 The 1.9 Å structure of a proteasome-11S activator complex and implications for proteasome-PAN/PA700 interactions Mol Cell 18 589 99 15916965
  10. [10]Smith DM Kafri G Cheng Y Ng D Walz T 2005 ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins Mol Cell 20 687 98 16337593
  11. [11]Smith DM Chang S-C Park S Finley D Cheng Y 2007 Docking of the proteasomal ATPases’ carboxyl termini in the 20S proteasome’s alpha ring opens the gate for substrate entry Mol Cell 20 687 98 17803938 PMC2083707
  12. [12]Rabl J Smith DM Yu Y Chang S-C Goldberg AL 2008 Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases Mol Cell 30 360 68 18471981 PMC4141531
  13. [13]Walz J Erdmann A Kania M Typke D Koster AJ 1998 26S proteasome structure revealed by three-dimensional electron microscopy J Struct Biol 121 19 29 9573617
  14. [14]Lee C Prakash S Matouschek A 2002 Concurrent translocation of multiple polypeptide chains through the proteasomal degradation channel J Biol Chem 277 34760 65 12080075
  15. [15]Weber-Ban EU Reid BG Miranker AD Horwich AL 1999 Global unfolding of a substrate protein by the Hsp100 chaperone ClpA Nature 401 90 93 10485712
  16. [16]Braun BC Glickman M Kraft R Dahlmann B Kloetzel PM 1999 The base of the proteasome regulatory particle exhibits chaperone-like activity Nat Cell Biol 1 221 26 10559920
  17. [17]Liu C-W Millen L Roman TB Xiong H Gilbert HF 2002 Conformational remodeling of proteasomal substrates by PA700, the 19 S regulatory complex of the 26 S proteasome J Biol Chem 277 26815 20 12011044
  18. [18]Navon A Goldberg AL 2001 Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome Mol Cell 8 1339 49 11779508
  19. [20]Lee C Schwartz MP Prakash S Iwakura M Matouschek A 2001 ATP-Dependent proteases degrade their substrates by processively unraveling them from the degradation signal Mol Cell 7 627 37 11463387
  20. [21]Nickell S Beck F Korinek A Mihalache O Baumeister W 2007 Automated cryoelectron microscopy of “single particles” applied to the 26S proteasome FEBS Lett 581 2751 56 17531228
  21. [22]Deveraux Q Ustrell V Pickart CM Rechsteiner M 1994 A 26 S protease subunit that binds ubiquitin conjugates J Biol Chem 269 7059 61 8125911
  22. [23]van Nocker S Sadis S Rubin DM Glickman M Fu H 1996 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 16 6020 28 8887631 PMC231604
  23. [24]Fu H Sadis S Rubin DM Glickman M van Nocker S 1998 Multiubiquitin chain binding and protein degradation are mediated by distinct domains within the 26 S proteasome subunit Mcb1 J Biol Chem 273 1970 81 9442033
  24. [25]Elsasser S Gali RR Schwickart M Larsen CN Leggett DS 2002 Proteasome subunit Rpn1 binds ubiquitin-like protein domains Nat Cell Biol 4 725 30 12198498
  25. [26]Verma R Oania R Graumann J Deshaies RJ 2004 Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system Cell 118 99 110 15242647
  26. [27]Elsasser S Chandler-Militello D Mueller B Finley D 2004 Rad23 and Rpn10 serve as alternative ubiquitin receptors for the proteasome J Biol Chem 279 26817 22 15117949
  27. [28]Mayor T Graumann J Bryan J MacCoss MJ Deshaies RJ 2007 Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway Mol Cell Proteomics 6 1885 95 17644757
  28. [29]Husnjak K Elsasser S Zhang N Chen X Randles L 2008 Proteasome subunit Rpn13 is a novel ubiquitin receptor Nature 453 481 88 18497817 PMC2839886
  29. [30]Schreiner P Chen X Husnjak K Randles L Zhang N 2008 Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction Nature 453 548 52 18497827 PMC2825158
  30. [31]Schauber C Chen L Tongaonkar P Vega I Lambertson D 1998 Rad23 links DNA repair to the ubiquitin/proteasome pathway Nature 391 715 18 9490418
  31. [32]Chen L Madura K 2002 Rad23 Promotes the Targeting of Proteolytic Substrates to the Proteasome Mol Cell Biol 22 4902 13 12052895 PMC133919
  32. [33]Wilkinson CR Seeger M Hartmann-Petersen R Stone M Wallace M 2001 Proteins containing the UBA domain are able to bind to multi-ubiquitin chains Nat Cell Biol 3 939 43 11584278
  33. [34]Hicke L Schubert HL Hill CP 2005 Ubiquitin binding domains Nat Rev Mol Cell Biol 6 610 21 16064137
  34. [35]Goldberg AL Cascio P Saric T Rock KL 2002 The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides Mol Immunol 39 147 64 12200047
  35. [36]Kisselev AF Akopian TN Woo KM Goldberg AL 1999 The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes. Implications for understanding the degradative mechanism and antigen presentation J Biol Chem 274 3363 71 9920878
  36. [37]Massey AC Zhang C Cuervo AM 2006 Chaperone-mediated autophagy in aging and disease Curr Top Dev Biol 73 205 35 16782460
  37. [40]Xie Z Klionsky DJ 2007 Autophagosome formation: core machinery and adaptations Nat Cell Biol 9 1102 09 17909521
  38. [41]Peng J Schwartz D Elias JE Thoreen CC Cheng D 2003 A proteomics approach to understanding protein ubiquitination Nat Biotechnol 21 921 26 12872131
  39. [42]Meierhofer D Wang X Huang L Kaiser P 2008 Quantitative analysis of global ubiquitination in HeLa Cells by mass spectrometry J Proteome Res in press PMC2758155 18781797
  40. [43]Belle A Tanay A Bitincka L Shamir R O’Shea EK 2006 Quantification of protein half-lives in the budding yeast proteome Proc Natl Acad Sci USA 103 13004 09 16916930 PMC1550773
  41. [44]Wojcik C DeMartino GN 2003 Intracellular localization of proteasomes Int J Biochem Cell Biol 35 579 89 12672451
  42. [45]Elsasser S Finley D 2005 Delivery of ubiquitinated substrates to protein-unfolding machines Nat Cell Biol 7 742 49 16056265
  43. [46]Demartino GN Gillette TG 2007 Proteasomes: machines for all reasons Cell 129 659 62 17512401
  44. [47]Inobe T Matouschek A 2008 Protein targeting to ATP-dependent proteases Curr Op Struct Biol 18 43 51 PMC2346608 18276129
  45. [48]Kusmierczyk AR Hochstrasser M 2008 Some assembly required: dedicated chaperones in eukaryotic proteasome biogenesis Biol Chem in press PMC2650809 18713001
  46. [49]Chauhan D Hideshima T Anderson KC 2008 Targeting proteasomes as therapy in multiple myeloma Adv Exp Med Biol 615 251 60 18437898
  47. [50]Orlowski RZ Kuhn DJ 2008 Proteasome inhibitors in cancer therapy: lessons from the first decade Clin Cancer Res 14 1649 57 18347166
  48. [51]Dohmen RJ Willers I Marques AJ 2007 Biting the hand that feeds: Rpn4-dependent feedback regulation of proteasome function Biochim Biophys Acta 1773 1599 604 17604855
  49. [52]Kraft DC Deocaris CC Wadhwa R Rattan SI 2006 Preincubation with the proteasome inhibitor MG-132 enhances proteasome activity via the Nrf2 transcription factor in aging human skin fibroblasts Ann NY Acad Sci 1067 420 24 16804021
  50. [53]Finley D Tanaka K Mann C Feldmann H Hochstrasser M 1998 Unified nomenclature for subunits of the Saccharomyces cerevisiae proteasome regulatory particle Trends Biochem Sci 23 244 45 9697412
  51. [54]Baker TA Sauer RT 2006 ATP-dependent proteases of bacteria: recognition logic and operating principles Trends Biochem Sci 31 647 53 17074491 PMC2717004
  52. [55]Snider J Houry WA 2008 AAA+ proteins: diversity in function, similarity in structure Biochem Soc Trans 36 72 77 18208389
  53. [56]Bochtler M Hartmann C Song HK Bourenkov GP Bartunik HD 2000 The structures of HsIU and the ATP-dependent protease HsIU-HsIV Nature 403 800 05 10693812
  54. [57]Sousa MC Trame CB Tsuruta H Wilbanks SM Reddy VS 2000 Crystal and solution structures of an HslUV protease-chaperone complex Cell 103 633 43 11106733
  55. [58]Wang J Song JJ Seong IS Franklin MC Kamtekar S 2001 Nucleotide-dependent conformational changes in a protease-associated ATPase HslU Structure 9 1107 16 11709174
  56. [59]Horwitz AA Navon A Groll M Smith DM Reis C 2007 ATP-induced structural transitions in PAN, the proteasome-regulatory ATPase complex in archaea J Biol Chem 282 22921 29 17553803
  57. [60]Singh SK Grimaud R Hoskins JR Wickner S Maurizi MR 2000 Unfolding and internalization of proteins by the ATP-dependent proteases ClpXP and ClpAP Proc Natl Acad Sci USA 97 8898 903 10922052 PMC16793
  58. [61]Herman C Prakash S Lu CZ Matouschek A Gross CA 2003 Lack of a robust unfoldase activity confers a unique level of substrate specificity to the universal AAA protease FtsH Mol Cell 11 659 69 12667449
  59. [62]Mogk A Haslberger T Tessarz P Bukau B 2008 Common and specific mechanisms of AAA+ proteins involved in protein quality control Biochem Soc Trans 36 120 25 18208398
  60. [63]Forster A Whitby FG Hill CP 2003 The pore of activated 20S proteasomes has an ordered 7-fold symmetric conformation EMBO J 22 4356 64 12941688 PMC202378
  61. [64]Glickman MH Rubin DM Coux O Wefes I Pfeifer G 1998 A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3 Cell 94 615 23 9741626
  62. [65]Rubin DM Glickman MH Larsen CN Dhruvakumar S Finley D 1998 Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome EMBO J 17 4909 19 9724628 PMC1170820
  63. [66]Liu C-W Li X Thompson D Wooding K Chang T-L 2006 ATP binding and ATP hydrolysis play distinct roles in the function of 26S proteasome Mol Cell 24 39 50 17018291 PMC3951175
  64. [67]Kleijnen MF Roelofs J Park S Hathaway NA Glickman M 2007 Stability of the proteasome can be regulated allosterically through engagement of its proteolytic active sites Nat Struct Mol Biol 14 1180 88 18026118
  65. [68]Verma R Aravind L Oania R McDonald WH Yates JR III 2002 Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome Science 298 611 15 12183636
  66. [69]Yao T Cohen RE 2002 A cryptic protease couples deubiquitination and degradation by the proteasome Nature 419 403 7 12353037
  67. [70]Groettrup M Soza A Eggers M Kuehn L Dick TP 1996 A role for the proteasome regulator PA28alpha in antigen presentation Nature 381 166 68 8610016
  68. [71]Strehl B Seifert U Krüger E Heink S Kuckelkorn U 2005 Interferon-gamma, the functional plasticity of the ubiquitin-proteasome system, and MHC class I antigen processing Immunol Rev 207 19 30 16181324
  69. [72]Cascio P Call M Petre BM Walz T Goldberg AL 2002 Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes EMBO J 21 2636 45 12032076 PMC126027
  70. [73]Zhang Z Clawson A Realini C Jensen CC Knowlton JR 1998 Identification of an activation region in the proteasome activator REGalpha Proc Natl Acad Sci USA 95 2807 11 9501171 PMC19650
  71. [74]Osmulski PA Gaczynska M 2000 Atomic force microscopy reveals two conformations of the 20 S proteasome from fission yeast J Biol Chem 275 13171 74 10747864
  72. [75]Bajorek M Finley D Glickman MH 2003 Proteasome disassembly and downregulation is correlated with viability during stationary phase Curr Biol 13 1140 44 12842014
  73. [76]Kajava AV 2002 What Curves a-Solenoids? Evidence for an α-helical toroid structure of Rpn1 and Rpn2 proteins of the 26S proteasome J Biol Chem 277 49791 98 12270919
  74. [77]Rosenzweig R Osmulski PA Gaczynska M Glickman MH 2008 The central unit within the 19S regulatory particle of the proteasome Nat Struct Mol Biol 15 573 80 18511945 PMC2481239
  75. [78]Yao T Song L Xu W DeMartino GN Florens L 2006 Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1 Nat Cell Biol 8 994 1002 16906146
  76. [79]Hamazaki J Iemura S Natsume T Yashiroda H Tanaka K 2006 A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes EMBO J 25 4524 36 16990800 PMC1589993
  77. [80]Hiyama H Yokoi M Masutani C Sugasawa K Maekawa T 1999 Interaction of hHR23 with S5a. The ubiquitin-like domain of hHR23 mediates interaction with S5a subunit of 26 S proteasome J Biol Chem 274 28019 25 10488153
  78. [81]Walters KJ Kleijnen MF Goh AM Wagner G Howley PM 2002 Structural studies of the interaction between ubiquitin family proteins and proteasome subunit S5a Biochemistry 41 1767 77 11827521
  79. [82]Leggett DS Hanna J Borodovsky A Crosas B Schmidt M 2002 Multiple associated proteins regulate proteasome structure and function Molec Cell 10 495 507 12408819
  80. [83]Stone M Hartmann-Petersen R Seeger M Bech-Otschir D Wallace M 2004 Uch2/Uch37 is the major deubiquitinating enzyme associated with the 26 S proteasome in fission yeast J Mol Biol 344 697 706 15533439
  81. [84]Crosas B Hanna J Kirkpatrick DS Zhang DP Tone Y 2006 Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities Cell 127 1401 13 17190603
  82. [85]Maytal-Kivity V Reis N Hofmann K Glickman MH 2002 MPN+, a putative catalytic motif found in a subset of MPN domain proteins from eukaryotes and prokaryotes, is critical for Rpn11 function BMC Biochemistry 3 28 39 12370088 PMC129983
  83. [86]Gallery M Blank JL Lin Y Gutierrez JA Pulido JC 2007 The JAMM motif of human deubiquitinase Poh1 is essential for cell viability Mol Cancer Ther 6 262 68 17237285
  84. [87]Kapelari B Bech-Otschir D Hegerl R Schade R Dumdey R 2000 Electron microscopy and subunit-subunit interaction studies reveal a first architecture of COP9 signalosome J Mol Biol 300 1169 78 10903862
  85. [88]Sharon M Taverner T Ambroggio XI Deshaies RJ Robinson CV 2006 Structural organization of the 19S proteasome lid: insights from MS of intact complexes PLoS Biol 4 e267 16869714 PMC1523230
  86. [89]Scheel H Hofmann K 2005 Prediction of a common structural scaffold for proteasome lid, COP9-signalosome and eIF3 complexes BMC Bioinformatics 6 71 15790418 PMC1274264
  87. [90]Cope GA Suh GS Aravind L Schwarz SE Zipursky SL 2002 Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1 Science 298 608 11 12183637
  88. [91]Duda DM Borg LA Scott DC Hunt HW Hammel M 2008 Structural Insights into NEDD8 Activation of Cullin-RING Ligases: Conformational Control of Conjugation Cell (in press) 10.1016/j.cell.2008.07.022 PMC2628631 18805092 · DOI · Paper page
  89. [92]Peng Z Shen Y Feng S Wang X Chitteti BN 2003 Evidence for a physical association of the COP9 signalosome, the proteasome, and specific SCF E3 ligases in vivo Curr Biol 13 R504 05 12842023
  90. [93]Huang X Hetfeld BK Seifert U Kähne T Kloetzel PM 2005 Consequences of COP9 signalosome and 26S proteasome interaction FEBS J 272 3909 17 16045761
  91. [94]Fu H Reis N Lee Y Glickman MH Vierstra RD 2001 Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome EMBO J 20 7096 107 11742986 PMC125776
  92. [95]Hanna J Hathaway NA Tone Y Elsasser S Kirkpatrick DS 2006 Deubiquitinating enzyme Ubp6 functions noncatalytically to delay proteasomal degradation Cell 127 99 111 17018280
  93. [96]Hanna J Leggett DL Finley D 2003 Ubiquitin depletion as a key mediator of toxicity by translational inhibitors Mol Cell Biol 23 9251 61 14645527 PMC309641
  94. [97]Liu CW Corboy MJ DeMartino GN Thomas PJ 2003 Endoproteolytic activity of the proteasome Science 299 408 11 12481023 PMC3516294
  95. [98]Lee C Prakash S Matouschek A 2002 Concurrent translocation of multiple polypeptide chains through the proteasomal degradation channel J Biol Chem 277 34760 65 12080075
  96. [99]Piwko W Jentsch S 2006 Proteasome-mediated protein processing by bidirectional degradation initiated from an internal site Nat Struct Mol Biol 13 691 97 16845392
  97. [100]Lam YA Xu W DeMartino GN Cohen RE 1997 Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome Nature 385 737 40 9034192
  98. [101]Thrower JS Hoffman L Rechsteiner M Pickart CM 2000 Recognition of the polyubiquitin proteolytic signal EMBO J 19 94 102 10619848 PMC1171781
  99. [102]Chernova TA Allen KD Wesoloski LM Shanks JR Chernoff YO 2003 Pleiotropic effects of Ubp6 loss on drug sensitivities and yeast prion are due to depletion of the free ubiquitin pool J Biol Chem 278 52102 15 14559899
  100. [103]Li T Naqvi IN Yang H Teo TS 2000 Identification of a 26S proteasome-associated UCH in fission yeast Biochem Biophys Res Commun 272 270 75 10872838
  101. [104]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 82 18162577 PMC2262970
  102. [105]Hanna J Meides A Zhang DP Finley D 2007 A ubiquitin stress response induces altered proteasome composition Cell 129 747 59 17512408
  103. [106]Mimnaugh EG Chen HY Davie JR Celis JE Neckers L 1997 Rapid deubiquitination of nucleosomal histones in human tumor cells caused by proteasome inhibitors and stress response inducers: effects on replication, transcription, translation, and the cellular stress response Biochemistry 36 14418 29 9398160
  104. [107]Osaka H Wang YL Takada K Takizawa S Setsuie R 2003 Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neuron Hum Mol Genet 12 1945 58 12913066
  105. [108]Anderson C Crimmins S Wilson JA Korbel GA Ploegh HL 2005 Loss of Usp14 results in reduced levels of ubiquitin in ataxia mice J Neurochem 95 724 31 16190881
  106. [109]Walters BJ Campbell SL Chen PC Taylor AP Schroeder DG 2008 Differential effects of Usp14 and Uch-L1 on the ubiquitin proteasome system and synaptic activity Mol Cell Neurosci (in press) PMC2734958 18771733
  107. [110]Hamazaki J Sasaki K Kawahara H Hisanaga S Tanaka K 2007 Rpn10-mediated degradation of ubiquitinated proteins is essential for mouse development Mol Cell Biol 27 6629 38 17646385 PMC2099239
  108. [111]Ng JM Vermeulen W van der Horst GT Bergink S Sugasawa K 2003 A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein Genes Dev 17 1630 45 12815074 PMC196135
  109. [112]Lam YA Lawson TG Velayutham M Zweier JL Pickart CM 2002 A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal Nature 416 763 67 11961560
  110. [113]Archer CT Burdine L Liu B Ferdous A Johnston SA 2008 Physical and functional interactions of monoubiquitylated transactivators with the proteasome J Biol Chem 283 21789 98 18515799 PMC2490782
  111. [114]Kang Y Chen X Lary JW Cole JL Walters KJ 2007 Defining how ubiquitin receptors hHR23a and S5a bind polyubiquitin J Mol Biol 369 168 76 17408689 PMC3864866
  112. [115]Wang Q Young P Walters KJ 2005 Structure of S5a bound to monoubiquitin provides a model for polyubiquitin recognition J Mol Biol 348 727 39 15826667
  113. [116]Kawahara H Kasahara M Nishiyama A Ohsumi K Goto T 2000 Developmentally regulated, alternative splicing of the Rpn10 gene generates multiple forms of 26S proteasomes EMBO J 19 4144 53 10921894 PMC306610
  114. [117]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 67 9488668
  115. [118]Qiu XB Ouyang SY Li CJ Miao S Wang L 2006 hRpn13/ADRM1/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37 EMBO J 25 5742 53 17139257 PMC1698896
  116. [119]Yao T Song L Jin J Cai Y Takahashi H 2008 Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the Ino80 chromatin remodeling complex Mol Cell (in press) PMC2577292 18922472
  117. [120]Wang Q Goh AM Howley PM Walters KJ 2003 Ubiquitin recognition by the DNA repair protein hHR23a Biochemistry 42 13529 35 14621999
  118. [121]Kim I Mi K Rao H 2004 Multiple interactions of Rad23 suggest a mechanism for ubiquitylated substrate delivery important in proteolysis Mol Biol Cell 15 3357 65 15121879 PMC452589
  119. [122]Richly H Rape M Braun S Rumpf S Hoege C 2005 A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting Cell 120 73 84 15652483
  120. [123]Kaplun L Tzirkin R Bakhrat A Shabek N Ivantsiv Y 2005 The DNA damage-inducible UbL-UbA protein Ddi1 participates in Mec1-mediated degradation of Ho endonuclease Mol Cell Biol 25 5355 62 15964793 PMC1156969
  121. [124]Ivantsiv Y Kaplun L Tzirkin-Goldin R Shabek N Raveh D 2006 Unique role for the UbL-UbA protein Ddi1 in turnover of SCFUfo1 complexes Mol Cell Biol 26 1579 88 16478980 PMC1430233
  122. [125]Hara T Kamura T Kotoshiba S Takahashi H Fujiwara K 2005 Role of the UBL-UBA protein KPC2 in degradation of p27 at G1 phase of the cell cycle Mol Cell Biol 25 9292 303 16227581 PMC1265808
  123. [126]Kumar S Talis AL Howley PM 1999 Identification of HHR23A as a substrate for E6-associated protein-mediated ubiquitination J Biol Chem 274 18785 92 10373495
  124. [127]Kleijnen MF Shih AH Zhou P Kumar S Soccio RE 2000 The hPLIC proteins may provide a link between the ubiquitination machinery and the proteasome Mol Cell 6 409 19 10983987
  125. [128]Ortolan TG Tongaonkar P Lambertson D Chen L Schauber C 2000 The DNA repair protein Rad23 is a negative regulator of multi-ubiquitin chain assembly Nat Cell Biol 2 601 08 10980700
  126. [129]Chen L Shinde U Ortolan TG Madura K 2001 Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition of multi-ubiquitin chain assembly EMBO Rep 2 933 38 11571271 PMC1084081
  127. [130]Hartmann-Petersen R Hendil KB Gordon C 2003 Ubiquitin binding proteins protect ubiquitin conjugates from disassembly FEBS Lett 535 77 81 12560082
  128. [131]Saeki Y Sone T Toh-e A Yokosawa H 2002 Identification of ubiquitin-like protein-binding subunits of the 26S proteasome Biochem Biophys Res Commun 296 813 19 12200120
  129. [132]Seeger M Hartmann-Petersen R Wilkinson CR Wallace M Samejima I 2003 Interaction of the anaphase-promoting complex/cyclosome and proteasome protein complexes with multiubiquitin chain-binding proteins J Biol Chem 278 16791 96 12615927
  130. [133]Haracska L Udvardy A 1995 Cloning and sequencing of a non-ATPase subunit of the regulatory complex of the Drosophila 26S protease Eur J Biochem 231 720 25 7649173
  131. [134]Matiuhin Y Kirkpatrick DS Ziv I Kim W Dakshinamurthy A 2008 Extraproteasomal Rpn10 restricts access of the polyubiquitin-binding protein Dsk2 to proteasome (submitted) PMC2643056 18995839
  132. [135]Ishii T Funakoshi M Kobayashi H 2006 Yeast Pth2 is a UBL domain-binding protein that participates in the ubiquitin-proteasome pathway EMBO J 25 5492 503 17082762 PMC1679763
  133. [136]Krylov DM Koonin EV 2001 A novel family of predicted retroviral-like aspartyl proteases with a possible key role in eukaryotic cell cycle control Curr Biol 11 R584 R587 11516960
  134. [137]Sirkis R Gerst JE Fass D 2006 Ddi1, a eukaryotic protein with the retroviral protease fold J Mol Biol 364 376 87 17010377
  135. [138]Gabriely G Kama R Gelin-Licht R Gerst JE 2008 Different Domains of the UBL-UBA Ubiquitin Receptor, Ddi1/Vsm1, Are Involved in Its Multiple Cellular Roles Mol Biol Cell (in press) PMC2526698 18562697
  136. [139]Riley BE Xu Y Zoghbi HY Orr HT 2004 The effects of the polyglutamine repeat protein ataxin-1 on the UbL-UBA protein A1Up J Biol Chem 279 42290 301 15280365
  137. [140]Li X Su V Kurata WE Jin C Lau AF 2008 A novel connexin43-interacting protein, CIP75, which belongs to the UbL-UBA protein family, regulates the turnover of connexin43 J Biol Chem 283 5748 59 18079109 PMC2877505
  138. [141]Geetha T Seibenhener ML Chen L Madura K Wooten MW 2008 p62 serves as a shuttling factor for TrkA interaction with the proteasome Biochem Biophys Res Comm 374 33 37 18598672 PMC2561188
  139. [142]Chau V Tobias JW Bachmair A Marriott D Ecker DJ 1989 A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein Science 243 1576 83 2538923
  140. [143]Finley D Sadis S Monia BP Boucher P Ecker DJ 1994 Inhibition of proteolysis and cell cycle progression in a multiubiquitination-deficient yeast mutant Mol Cell Biol 14 5501 09 8035826 PMC359070
  141. [144]Spence J Sadis S Haas AL Finley D 1995 A ubiquitin mutant with specific defects in DNA repair and multiubiquitination Mol Cell Biol 15 1265 73 7862120 PMC230349
  142. [145]Hoege C Pfander B Moldovan GL Pyrowolakis G Jentsch S 2002 RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO Nature 419 135 41 12226657
  143. [146]Adhikari A Xu M Chen ZJ 2007 Ubiquitin-mediated activation of TAK1 and IKK Oncogene 26 3214 26 17496917
  144. [147]Baboshina OV Haas AL 1996 Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26 S proteasome subunit 5 J Biol Chem 271 2823 31 8576261
  145. [148]Koegl M Hoppe T Schlenker S Ulrich HD Mayer TU 1999 A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly Cell 96 635 44 10089879
  146. [149]Hofmann RM Pickart CM 2001 In vitro assembly and recognition of Lys-63 polyubiquitin chains J Biol Chem 276 27936 43 11369780
  147. [150]Kirkpatrick DS Hathaway NA Hanna J Elsasser S Rush J 2006 Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology Nat Cell Biol 8 700 10 16799550
  148. [151]Jin L Williamson A Banerjee S Philipp I Rape M 2008 Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex Cell 133 653 65 18485873 PMC2696189
  149. [152]Raasi S Varadan R Fushman D Pickart CM 2005 Diverse polyubiquitin interaction properties of ubiquitin-associated domains Nat Struct Mol Biol 12 708 14 16007098
  150. [153]Kim HT Kim KP Lledias F Kisselev AF Scaglione KM 2007 Certain pairs of ubiquitin-conjugating enzymes (E2s) and ubiquitin-protein ligases (E3s) synthesize nondegradable forked ubiquitin chains containing all possible isopeptide linkages J Biol Chem 282 17375 86 17426036
  151. [154]Boutet SC Disatnik MH Chan LS Iori K Rando TA 2007 Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors Cell 130 349 62 17662948
  152. [155]Murakami Y Matsufuji S Kameji T Hayashi S Igarashi K 1992 Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination Nature 360 597 99 1334232
  153. [156]Zhang M Pickart CM Coffino P 2003 Determinants of proteasome recognition of ornithine decarboxylase, a ubiquitin-independent substrate EMBO J 22 1488 96 12660156 PMC152902
  154. [157]Hipp MS Kalveram B Raasi S Groettrup M Schmidtke G 2005 FAT10, a ubiquitin-independent signal for proteasomal degradation Mol Cell Biol 25 3483 91 15831455 PMC1084302
  155. [158]Schmidtke G Kalveram B Weber E Bochtler P Lukasiak S 2006 The UBA domains of NUB1L are required for binding but not for accelerated degradation of the ubiquitin-like modifier FAT10 J Biol Chem 281 20045 54 16707496
  156. [159]Tanahashi N Murakami Y Minami Y Shimbara N Hendil KB 2000 Hybrid proteasomes. Induction by interferon-gamma and contribution to ATP-dependent proteolysis J Biol Chem 275 14336 45 10799514
  157. [160]Shibatani T Carlson EJ Larabee F McCormack AL Fruh K 2006 Global organization and function of mammalian cytosolic proteasome pools: Implications for PA28 and 19S regulatory complexes Mol Biol Cell 17 4962 71 16987959 PMC1679665
  158. [161]Schmidt M Haas W Crosas B Santamaria PG Gygi SP 2005 The HEAT repeat protein Blm10 regulates the yeast proteasome by capping the core particle Nat Struct Mol Biol 12 294 303 15778719
  159. [162]Masson P Andersson O Petersen UM Young P 2001 Identification and characterization of a Drosophila nuclear proteasome regulator. A homolog of human 11 S REGgamma (PA28gamma) J Biol Chem 276 1383 90 11027688
  160. [163]Li X Lonard DM Jung SY Malovannaya A Feng Q 2006 The SRC-3/AIB1 coactivator is degraded in a ubiquitin- and ATP-independent manner by the REGgamma proteasome Cell 124 381 92 16439211
  161. [164]Chen X Barton LF Chi Y Clurman BE Roberts JM 2007 Ubiquitin-independent degradation of cell-cycle inhibitors by the REGgamma proteasome Mol Cell 26 843 52 17588519 PMC2031223
  162. [165]Moriishi K Okabayashi T Nakai K Moriya K Koike K 2003 Proteasome activator PA28gamma-dependent nuclear retention and degradation of hepatitis C virus core protein J Virol 77 10237 49 12970408 PMC228494
  163. [166]Murata S Kawahara H Tohma S Yamamoto K Kasahara M 1999 Growth retardation in mice lacking the proteasome activator PA28gamma J Biol Chem 274 38211 15 10608895
  164. [167]Barton LF Runnels HA Schell TD Cho Y Gibbons R 2004 Immune defects in 28-kDa proteasome activator g-deficient mice J Immunol 172 3948 54 15004203
  165. [168]Mao I Liu J Li X Luo H 2008 REGgamma, a proteasome activator and beyond? Cell Mol Life Sci in press PMC11131756 18679578
  166. [169]Ustrell V Hoffman L Pratt G Rechsteiner M 2002 PA200, a nuclear proteasome activator involved in DNA repair EMBO J 21 3516 25 12093752 PMC126083
  167. [170]Iwanczyk J Sadre-Bazzaz K Ferrell K Kondrashkina E Formosa T 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 59 16952374 PMC2980845
  168. [171]Kajava AV Gorbea C Ortega J Rechsteiner M Steven AC 2004 New HEAT-like repeat motifs in proteins regulating proteasome structure and function J Struct Biol 146 425 30 15099583
  169. [172]Khor B Bredemeyer AL Huang C-Y Turnbull IR Evans R 2006 Proteasome activator PA200 is required for normal spermatogenesis Mol Cell Biol 26 2999 3007 16581775 PMC1446934
  170. [173]Fehlker M Wendler P Lehmann A Enenkel C 2003 Blm3 is part of nascent proteasomes and is involved in a late stage of nuclear proteasome assembly EMBO Rep 4 959 63 12973301 PMC1326396
  171. [174]Marques AJ Glanemann C Ramos PC Dohmen RJ 2007 The C-terminal extension of the beta7 subunit and activator complexes stabilize nascent 20 S proteasomes and promote their maturation J Biol Chem 282 34869 76 17911101
  172. [175]Verma R Chen S Feldman R Schieltz D Yates J 2000 Proteasomal proteomics: identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes Mol Biol Cell 11 3425 39 11029046 PMC15004
  173. [176]Guerrero C Tagwerker C Kaiser P Huang L 2006 An integrated mass spectrometry-based proteomic approach: quantitative analysis of tandem affinity-purified in vivo cross-linked protein complexes (QTAX) to decipher the 26 S proteasome-interacting network Mol Cell Proteomics 5 366 78 16284124
  174. [177]Wang X Chen C-F Baker PR Chen P-L Kaiser P 2007 Mass spectrometric characterization of the affinity-purified human 26S proteasome complex Biochemistry 46 3553 65 17323924
  175. [178]Wang X Huang L 2008 Identifying dynamic interactors of protein complexes by quantitative mass spectrometry Mol Cell Proteomics 7 46 57 17934176
  176. [179]Guerrero C Milenkovic T a Pržulj N Kaiser P Huang L 2008 Characterization of the proteasome interaction network using a QTAX-based tag-team strategy and protein interaction network analysis Proc Nat Acad Sci USA (in press) PMC2533190 18757749
  177. [180]Hartmann-Petersen R Gordon C 2004 Integral UBL domain proteins: a family of proteasome interacting proteins Sem Cell Dev Biol 14 247 59 15209385
  178. [181]Kikukawa Y Minami R Shimada M Kobayashi M Tanaka K 2005 Unique proteasome subunit Xrpn10c is a specific receptor for the antiapoptotic ubiquitin-like protein Scythe FEBS J 272 6373 86 16336274
  179. [182]Kee Y Muñoz W Lyon N Huibregtse JM 2006 The deubiquitinating enzyme Ubp2 modulates Rsp5-dependent Lys63-linked polyubiquitin conjugates in Saccharomyces cerevisiae J Biol Chem 281 36724 31 17028178
  180. [183]Kohlmann S Schäfer A Wolf DH 2008 Ubiquitin ligase Hul5 is required for fragment-specific substrate degradation in endoplasmic reticulum-associated degradation J Biol Chem 283 16374 83 18436532
  181. [184]Xie Y Varshavsky A 2002 UFD4 lacking the proteasome-binding region catalyses ubiquitination but is impaired in proteolysis Nat Cell Biol 4 1003 07 12447385
  182. [185]Chuang S-M Madura K 2005 Saccharomyces cerevisiae ub-conjugating enzyme Ubc4 binds the proteasome in the presence of translationally damaged proteins Genetics 171 1477 84 16118187 PMC1456077
  183. [186]Farras R Ferrando A Jasik J Kleinow T Okresz L 2001 SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase EMBO J 20 2742 56 11387208 PMC125500
  184. [187]Sakata E Yamaguchi Y Kurimoto E Kikuchi J Yokoyama S 2003 Parkin binds the Rpn10 subunit of 26S proteasomes through its ubiquitin-like domain EMBO Rep 4 301 06 12634850 PMC1315892
  185. [188]Jäger S Strayle J Heinemeyer W Wolf DH 2001 Cic1, an adaptor protein specifically linking the 26S proteasome to its substrate, the SCF component Cdc4 EMBO J 20 4423 31 11500370 PMC125261
  186. [189]Stanhill A Haynes CM Zhang Y Min G Steele MC 2006 An arsenite-inducible 19S regulatory particle-associated protein adapts proteasomes to proteotoxicity Mol Cell 23 875 85 16973439
  187. [191]Unno M Mizushima T Morimoto Y Tomisugi Y Tanaka K 2002 The structure of the mammalian 20S proteasome at 2.75 Å resolution Structure 10 609 18 12015144
  188. [192]Murata S Takahama Y Tanaka K 2008 Thymoproteasome: probable role in generating positively selecting peptides Curr Op Immunol 20 192 96 18403190
  189. [193]Murata S Sasaki K Kishimoto T Niwa S-I Hayashi H 2007 Regulation of CD8+ T cell development by thymus-specific proteasomes Science 316 1349 53 17540904
  190. [194]Yang P Fu H Walker J Papa CM Smalle J 2004 Purification of the Arabidopsis 26 S proteasome: biochemical and molecular analyses revealed the presence of multiple isoforms J Biol Chem 279 6401 13 14623884
  191. [195]Kenniston JA Baker TA Fernandez JM Sauer RT 2003 Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of an AAA+ degradation machine Cell 114 511 20 12941278
  192. [196]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 37 15311270
  193. [197]Park E Rho YM Koh OJ Ahn SW Seong IS 2005 Role of the GYVG pore motif of HslU ATPase in protein unfolding and translocation for degradation by HslV peptidase J Biol Chem 280 22892 98 15849200
  194. [198]Siddiqui SM Sauer RT Baker TA 2004 Role of the processing pore of the ClpX AAA+ ATPase in the recognition and engagement of specific protein substrates Genes Dev 18 369 74 15004005 PMC359390
  195. [199]Hinnerwisch J Fenton WA Furtak KJ Farr GW Horwich AL 2005 Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation Cell 121 1029 41 15989953
  196. [200]Takeuchi J Chen H Coffino P 2007 Proteasome substrate degradation requires association plus extended peptide EMBO J 26 123 31 17170706 PMC1782366
  197. [201]Levitskaya J Sharipo A Leonchiks A Ciechanover A Masucci MG 1997 Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein–Barr virus nuclear antigen 1 Proc Natl Acad Sci USA 94 12616 21 9356498 PMC25057
  198. [202]Zhang M Coffino P 2004 Repeat sequence of Epstein-Barr virus-encoded nuclear antigen 1 protein interrupts proteasome substrate processing J Biol Chem 279 8635 41 14688254
  199. [203]Hoyt MA Zich J Takeuchi J Zhang M Govaerts C 2006 Glycine–alanine repeats impair proper substrate unfolding by the proteasome EMBO J 25 1720 29 16601692 PMC1440830
  200. [204]Hoppe T Rape M Jentsch S 2001 Membrane-bound transcription factors: regulated release by RIP or RUP Curr Opin Cell Biol 13 344 48 11343906

200 of 206 shown

Cited by

Sorted by citations

Authors
Finley, D.
Affiliations
Harvard University (US)
Corresponding author
Finley, Daniel
Venue
Annual Review of Biochemistry
Published
2009-06-01
Volume
78
Issue
1
Pages
477-513
ISSN
  • 0066-4154 (ISSN-L)
  • 1545-4509
OpenAlex
W2097164847
Cited by
1,764
References
4
Citations by year
2026: 55 · 2025: 74 · 2024: 86 · 2023: 97 · 2022: 96 · 2021: 96 · 2020: 110 · 2019: 96 · 2018: 100 · 2017: 94 · 2016: 110 · 2015: 111 · 2014: 134 · 2013: 129 · 2012: 145
FWCI
9.57
Type
journal article
Language
en
Open access
Locations
  • Annual Review of Biochemistry (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of General Medical Sciences (R01GM043601, GM43601, R01GM065592, GM065592, R37GM043601)
  • National Institute of Diabetes and Digestive and Kidney Diseases (DK 082906, R21DK082906)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Degradation and Inhibitors
Keywords
proteasome, ubiquitin conjugates, protein degradation, ubiquitin receptors, ATPase, substrate unfolding, substrate translocation, deubiquitination, deubiquitinase
MeSH terms
Animals, Humans, Proteins, Arabidopsis, Ubiquitin, Proteasome Endopeptidase Complex

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review