The Logic of the 26S Proteasome

Cell

Volumn 169, Issue 5, 2017, Pages 792-806

  Collins, Galen Andrew ^a   Goldberg, Alfred L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

proteasome phosphorylation; protein degradation; protein turnover; ubiquitin proteasome system

Indexed keywords

26S PROTEASOME; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; POLYPEPTIDE; PROTEASOME; UBIQUITIN; UNCLASSIFIED DRUG; ATP DEPENDENT 26S PROTEASE;

ALLOSTERISM; BINDING COMPETITION; CELLS; CONJUGATE; DEUBIQUITINATION; ENERGY COST; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME DEGRADATION; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN DEGRADATION; PROTEIN HYDROLYSIS; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; REVIEW; UBIQUITINATION; ANIMAL; CHEMISTRY; EUKARYOTE; METABOLISM; PHOSPHORYLATION;

ADENOSINE TRIPHOSPHATASES; ALLOSTERIC REGULATION; ANIMALS; EUKARYOTA; HUMANS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; UBIQUITINATION;

EID: 85019546678     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.04.023     Document Type: Review

References (138)

1. Asano, S., Fukuda, Y., Beck, F., Aufderheide, A., Förster, F., Danev, R., Baumeister, W., Proteasomes. A molecular census of 26S proteasomes in intact neurons. Science 347 (2015), 439–442.
2. Aufderheide, A., Beck, F., Stengel, F., Hartwig, M., Schweitzer, A., Pfeifer, G., Goldberg, A.L., Sakata, E., Baumeister, W., Förster, F., Structural characterization of the interaction of Ubp6 with the 26S proteasome. Proc. Natl. Acad. Sci. USA 112 (2015), 8626–8631.
3. Aviram, S., Kornitzer, D., The ubiquitin ligase Hul5 promotes proteasomal processivity. Mol. Cell. Biol. 30 (2010), 985–994.
4. Bajorek, M., Finley, D., Glickman, M.H., Proteasome disassembly and downregulation is correlated with viability during stationary phase. Curr. Biol. 13 (2003), 1140–1144.
5. Bashore, C., Dambacher, C.M., Goodall, E.A., Matyskiela, M.E., Lander, G.C., Martin, A., Ubp6 deubiquitinase controls conformational dynamics and substrate degradation of the 26S proteasome. Nat. Struct. Mol. Biol. 22 (2015), 712–719.
6. Beck, F., Unverdorben, P., Bohn, S., Schweitzer, A., Pfeifer, G., Sakata, E., Nickell, S., Plitzko, J.M., Villa, E., Baumeister, W., Förster, F., Near-atomic resolution structural model of the yeast 26S proteasome. Proc. Natl. Acad. Sci. USA 109 (2012), 14870–14875.
7. Beckwith, R., Estrin, E., Worden, E.J., Martin, A., Reconstitution of the 26S proteasome reveals functional asymmetries in its AAA+ unfoldase. Nat. Struct. Mol. Biol. 20 (2013), 1164–1172.
8. Berko, D., Tabachnick-Cherny, S., Shental-Bechor, D., Cascio, P., Mioletti, S., Levy, Y., Admon, A., Ziv, T., Tirosh, B., Goldberg, A.L., Navon, A., The direction of protein entry into the proteasome determines the variety of products and depends on the force needed to unfold its two termini. Mol. Cell 48 (2012), 601–611.
9. Berko, D., Herkon, O., Braunstein, I., Isakov, E., David, Y., Ziv, T., Navon, A., Stanhill, A., Inherent asymmetry in the 26S proteasome is defined by the ubiquitin receptor RPN13. J. Biol. Chem. 289 (2014), 5609–5618.
10. Besche, H.C., Sha, Z., Kukushkin, N.V., Peth, A., Hock, E.M., Kim, W., Gygi, S., Gutierrez, J.A., Liao, H., Dick, L., Goldberg, A.L., Autoubiquitination of the 26S proteasome on Rpn13 regulates breakdown of ubiquitin conjugates. EMBO J. 33 (2014), 1159–1176.
11. Bingol, B., Wang, C.F., Arnott, D., Cheng, D., Peng, J., Sheng, M., Autophosphorylated CaMKIIalpha acts as a scaffold to recruit proteasomes to dendritic spines. Cell 140 (2010), 567–578.
12. Borodovsky, A., Kessler, B.M., Casagrande, R., Overkleeft, H.S., Wilkinson, K.D., Ploegh, H.L., A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14. EMBO J. 20 (2001), 5187–5196.
13. Braten, O., Livneh, I., Ziv, T., Admon, A., Kehat, I., Caspi, L.H., Gonen, H., Bercovich, B., Godzik, A., Jahandideh, S., et al. Numerous proteins with unique characteristics are degraded by the 26S proteasome following monoubiquitination. Proc. Natl. Acad. Sci. USA 113 (2016), E4639–E4647.
14. Chen, P.C., Bhattacharyya, B.J., Hanna, J., Minkel, H., Wilson, J.A., Finley, D., Miller, R.J., Wilson, S.M., Ubiquitin homeostasis is critical for synaptic development and function. J. Neurosci. 31 (2011), 17505–17513.
15. Chen, S., Wu, J., Lu, Y., Ma, Y.B., Lee, B.H., Yu, Z., Ouyang, Q., Finley, D.J., Kirschner, M.W., Mao, Y., Structural basis for dynamic regulation of the human 26S proteasome. Proc. Natl. Acad. Sci. USA 113 (2016), 12991–12996.
16. Chernova, T.A., Allen, K.D., Wesoloski, L.M., Shanks, J.R., Chernoff, Y.O., Wilkinson, K.D., Pleiotropic effects of Ubp6 loss on drug sensitivities and yeast prion are due to depletion of the free ubiquitin pool. J. Biol. Chem. 278 (2003), 52102–52115.
17. Choi, W.H., de Poot, S.A., Lee, J.H., Kim, J.H., Han, D.H., Kim, Y.K., Finley, D., Lee, M.J., Open-gate mutants of the mammalian proteasome show enhanced ubiquitin-conjugate degradation. Nat. Commun., 7, 2016, 10963.
18. Coffino, P., Too, P.H., Erales, J., Slippery substrates impair ATP-dependent protease function by slowing unfolding. J. Biol. Chem., 289, 2014, 3826.
19. Cohen-Kaplan, V., Livneh, I., Avni, N., Fabre, B., Ziv, T., Kwon, Y.T., Ciechanover, A., p62- and ubiquitin-dependent stress-induced autophagy of the mammalian 26S proteasome. Proc. Natl. Acad. Sci. USA 113 (2016), E7490–E7499.
20. Crosas, B., Hanna, J., Kirkpatrick, D.S., Zhang, D.P., Tone, Y., Hathaway, N.A., Buecker, C., Leggett, D.S., Schmidt, M., King, R.W., et al. Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities. Cell 127 (2006), 1401–1413.
21. Dambacher, C.M., Worden, E.J., Herzik, M.A., Martin, A., Lander, G.C., Atomic structure of the 26S proteasome lid reveals the mechanism of deubiquitinase inhibition. eLife, 5, 2016, e13027.
22. Dantuma, N.P., Bott, L.C., The ubiquitin-proteasome system in neurodegenerative diseases: precipitating factor, yet part of the solution. Front. Mol. Neurosci., 7, 2014, 70.
23. Dayal, S., Sparks, A., Jacob, J., Allende-Vega, N., Lane, D.P., Saville, M.K., Suppression of the deubiquitinating enzyme USP5 causes the accumulation of unanchored polyubiquitin and the activation of p53. J. Biol. Chem. 284 (2009), 5030–5041.
24. Deng, H.X., Chen, W., Hong, S.T., Boycott, K.M., Gorrie, G.H., Siddique, N., Yang, Y., Fecto, F., Shi, Y., Zhai, H., et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 477 (2011), 211–215.
25. Deriziotis, P., André, R., Smith, D.M., Goold, R., Kinghorn, K.J., Kristiansen, M., Nathan, J.A., Rosenzweig, R., Krutauz, D., Glickman, M.H., et al. Misfolded PrP impairs the UPS by interaction with the 20S proteasome and inhibition of substrate entry. EMBO J. 30 (2011), 3065–3077.
26. Deveraux, Q., Ustrell, V., Pickart, C., Rechsteiner, M., A 26 S protease subunit that binds ubiquitin conjugates. J. Biol. Chem. 269 (1994), 7059–7061.
27. Dimova, N.V., Hathaway, N.A., Lee, B.H., Kirkpatrick, D.S., Berkowitz, M.L., Gygi, S.P., Finley, D., King, R.W., APC/C-mediated multiple monoubiquitylation provides an alternative degradation signal for cyclin B1. Nat. Cell Biol. 14 (2012), 168–176.
28. Ding, Z., Fu, Z., Xu, C., Wang, Y., Wang, Y., Li, J., Kong, L., Chen, J., Li, N., Zhang, R., Cong, Y., High-resolution cryo-EM structure of the proteasome in complex with ADP-AlFx. Cell Res. 27 (2017), 373–385.
29. Elsasser, S., Gali, R.R., Schwickart, M., Larsen, C.N., Leggett, D.S., Müller, B., Feng, M.T., Tübing, F., Dittmar, G.A., Finley, D., Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 4 (2002), 725–730.
30. Erales, J., Hoyt, M.A., Troll, F., Coffino, P., Functional asymmetries of proteasome translocase pore. J. Biol. Chem. 287 (2012), 18535–18543.
31. Finley, D., Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78 (2009), 477–513.
32. Finley, D., Chen, X., Walters, K.J., Gates, channels, and switches: elements of the proteasome machine. Trends Biochem. Sci. 41 (2016), 77–93.
33. Goldberg, A.L., Development of proteasome inhibitors as research tools and cancer drugs. J. Cell Biol. 199 (2012), 583–588.
34. Goldberg, A.L., Dice, J.F., Intracellular protein degradation in mammalian and bacterial cells. Annu. Rev. Biochem. 43 (1974), 835–869.
35. Gomez, T.A., Kolawa, N., Gee, M., Sweredoski, M.J., Deshaies, R.J., Identification of a functional docking site in the Rpn1 LRR domain for the UBA-UBL domain protein Ddi1. BMC Biol., 9, 2011, 33.
36. Groll, M., Bajorek, M., Köhler, A., Moroder, L., Rubin, D.M., Huber, R., Glickman, M.H., Finley, D., A gated channel into the proteasome core particle. Nat. Struct. Biol. 7 (2000), 1062–1067.
37. Guo, X., Wang, X., Wang, Z., Banerjee, S., Yang, J., Huang, L., Dixon, J.E., Site-specific proteasome phosphorylation controls cell proliferation and tumorigenesis. Nat. Cell Biol. 18 (2016), 202–212.
38. Guo, X., Huang, X., Chen, M.J., Reversible phosphorylation of the 26S proteasome. Protein Cell 8 (2017), 255–272.
39. Hamazaki, J., Hirayama, S., Murata, S., Redundant roles of Rpn10 and Rpn13 in recognition of ubiquitinated proteins and cellular homeostasis. PLoS Genet., 11, 2015, e1005401.
40. Hanna, J., Leggett, D.S., Finley, D., Ubiquitin depletion as a key mediator of toxicity by translational inhibitors. Mol. Cell. Biol. 23 (2003), 9251–9261.
41. Hanna, J., Hathaway, N.A., Tone, Y., Crosas, B., Elsasser, S., Kirkpatrick, D.S., Leggett, D.S., Gygi, S.P., King, R.W., Finley, D., Deubiquitinating enzyme Ubp6 functions noncatalytically to delay proteasomal degradation. Cell 127 (2006), 99–111.
42. Hartl, F.U., Bracher, A., Hayer-Hartl, M., Molecular chaperones in protein folding and proteostasis. Nature 475 (2011), 324–332.
43. Hershko, A., Ciechanover, A., Heller, H., Haas, A.L., Rose, I.A., Proposed role of ATP in protein breakdown: conjugation of protein with multiple chains of the polypeptide of ATP-dependent proteolysis. Proc. Natl. Acad. Sci. USA 77 (1980), 1783–1786.
44. Hinnerwisch, J., Fenton, W.A., Furtak, K.J., Farr, G.W., Horwich, A.L., Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 121 (2005), 1029–1041.
45. Hishiya, A., Iemura, S., Natsume, T., Takayama, S., Ikeda, K., Watanabe, K., A novel ubiquitin-binding protein ZNF216 functioning in muscle atrophy. EMBO J. 25 (2006), 554–564.
46. Hofmann, R.M., Pickart, C.M., In vitro assembly and recognition of Lys-63 polyubiquitin chains. J. Biol. Chem. 276 (2001), 27936–27943.
47. Hough, R., Pratt, G., Rechsteiner, M., Purification of two high molecular weight proteases from rabbit reticulocyte lysate. J. Biol. Chem. 262 (1987), 8303–8313.
48. Huang, X., Luan, B., Wu, J., Shi, Y., An atomic structure of the human 26S proteasome. Nat. Struct. Mol. Biol. 23 (2016), 778–785.
49. Husnjak, K., Elsasser, S., Zhang, N., Chen, X., Randles, L., Shi, Y., Hofmann, K., Walters, K.J., Finley, D., Dikic, I., Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453 (2008), 481–488.
50. Inobe, T., Matouschek, A., Paradigms of protein degradation by the proteasome. Curr. Opin. Struct. Biol. 24 (2014), 156–164.
51. Isasa, M., Katz, E.J., Kim, W., Yugo, V., González, S., Kirkpatrick, D.S., Thomson, T.M., Finley, D., Gygi, S.P., Crosas, B., Monoubiquitination of RPN10 regulates substrate recruitment to the proteasome. Mol. Cell 38 (2010), 733–745.
52. Itakura, E., Zavodszky, E., Shao, S., Wohlever, M.L., Keenan, R.J., Hegde, R.S., Ubiquilins chaperone and triage mitochondrial membrane proteins for degradation. Mol. Cell 63 (2016), 21–33.
53. Jacobson, A.D., MacFadden, A., Wu, Z., Peng, J., Liu, C.W., Autoregulation of the 26S proteasome by in situ ubiquitination. Mol. Biol. Cell 25 (2014), 1824–1835.
54. Johnston, J.A., Johnson, E.S., Waller, P.R., Varshavsky, A., Methotrexate inhibits proteolysis of dihydrofolate reductase by the N-end rule pathway. J. Biol. Chem. 270 (1995), 8172–8178.
55. Kaiser, S.E., Riley, B.E., Shaler, T.A., Trevino, R.S., Becker, C.H., Schulman, H., Kopito, R.R., Protein standard absolute quantification (PSAQ) method for the measurement of cellular ubiquitin pools. Nat. Methods 8 (2011), 691–696.
56. Kenniston, J.A., Baker, T.A., Fernandez, J.M., Sauer, R.T., Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of an AAA+ degradation machine. Cell 114 (2003), 511–520.
57. Khandros, E., Thom, C.S., D'Souza, J., Weiss, M.J., Integrated protein quality-control pathways regulate free α-globin in murine β-thalassemia. Blood 119 (2012), 5265–5275.
58. Kim, H.T., Goldberg, A.L., The deubiquitinating enzyme Usp14 allosterically inhibits multiple proteasome activities and ubiquitin-independent proteolysis. J Biol Chem., 2017, 10.1074/jbc.M116.763128 Published online April 17, 2017.
59. Kim, H.T., Kim, K.P., Uchiki, T., Gygi, S.P., Goldberg, A.L., S5a promotes protein degradation by blocking synthesis of nondegradable forked ubiquitin chains. EMBO J. 28 (2009), 1867–1877.
60. Kim, Y.C., Snoberger, A., Schupp, J., Smith, D.M., ATP binding to neighbouring subunits and intersubunit allosteric coupling underlie proteasomal ATPase function. Nat. Commun., 6, 2015, 8520.
61. Kisselev, A.F., Akopian, T.N., Woo, K.M., Goldberg, A.L., 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 (1999), 3363–3371.
62. Koegl, M., Hoppe, T., Schlenker, S., Ulrich, H.D., Mayer, T.U., Jentsch, S., A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell 96 (1999), 635–644.
63. Koizumi, S., Irie, T., Hirayama, S., Sakurai, Y., Yashiroda, H., Naguro, I., Ichijo, H., Hamazaki, J., Murata, S., The aspartyl protease DDI2 activates Nrf1 to compensate for proteasome dysfunction. eLife, 5, 2016, e18357.
64. Kraut, D.A., Slippery substrates impair ATP-dependent protease function by slowing unfolding. J. Biol. Chem. 288 (2013), 34729–34735.
65. Kraut, D.A., Israeli, E., Schrader, E.K., Patil, A., Nakai, K., Nanavati, D., Inobe, T., Matouschek, A., Sequence- and species-dependence of proteasomal processivity. ACS Chem. Biol. 7 (2012), 1444–1453.
66. Kuo, C.-L., Goldberg, A.L., Ubiquitinated proteins promote the association of proteasomes with the deubiquitinating enzyme Usp14 and the ubiquitin ligase Ube3c. Proc. Natl. Acad. Sci. USA, 2017, 10.1073/pnas.1701734114 Published online April 10, 2017.
67. Lander, G.C., Estrin, E., Matyskiela, M.E., Bashore, C., Nogales, E., Martin, A., Complete subunit architecture of the proteasome regulatory particle. Nature 482 (2012), 186–191.
68. Lander, G.C., Martin, A., Nogales, E., The proteasome under the microscope: the regulatory particle in focus. Curr. Opin. Struct. Biol. 23 (2013), 243–251.
69. Lee, C., Schwartz, M.P., Prakash, S., Iwakura, M., Matouschek, A., ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell 7 (2001), 627–637.
70. Lee, B.H., Lee, M.J., Park, S., Oh, D.C., Elsasser, S., Chen, P.C., Gartner, C., Dimova, N., Hanna, J., Gygi, S.P., et al. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 467 (2010), 179–184.
71. Lee, B.H., Lu, Y., Prado, M.A., Shi, Y., Tian, G., Sun, S., Elsasser, S., Gygi, S.P., King, R.W., Finley, D., USP14 deubiquitinates proteasome-bound substrates that are ubiquitinated at multiple sites. Nature 532 (2016), 398–401.
72. Leggett, D.S., Hanna, J., Borodovsky, A., Crosas, B., Schmidt, M., Baker, R.T., Walz, T., Ploegh, H., Finley, D., Multiple associated proteins regulate proteasome structure and function. Mol. Cell 10 (2002), 495–507.
73. Lehrbach, N.J., Ruvkun, G., Proteasome dysfunction triggers activation of SKN-1A/Nrf1 by the aspartic protease DDI-1. eLife, 5, 2016, e17721.
74. Liu, C.W., Jacobson, A.D., Functions of the 19S complex in proteasomal degradation. Trends Biochem. Sci. 38 (2013), 103–110.
75. Liu, C., Liu, W., Ye, Y., Li, W., Ufd2p synthesizes branched ubiquitin chains to promote the degradation of substrates modified with atypical chains. Nat. Commun., 8, 2017, 14274.
76. Livneh, I., Cohen-Kaplan, V., Cohen-Rosenzweig, C., Avni, N., Ciechanover, A., The life cycle of the 26S proteasome: from birth, through regulation and function, and onto its death. Cell Res. 26 (2016), 869–885.
77. Lokireddy, S., Kukushkin, N.V., Goldberg, A.L., cAMP-induced phosphorylation of 26S proteasomes on Rpn6/PSMD11 enhances their activity and the degradation of misfolded proteins. Proc. Natl. Acad. Sci. USA 112 (2015), E7176–E7185.
78. Lu, Y., Lee, B.H., King, R.W., Finley, D., Kirschner, M.W., Substrate degradation by the proteasome: a single-molecule kinetic analysis. Science, 348, 2015, 1250834.
79. Ma, C.P., Slaughter, C.A., DeMartino, G.N., Identification, purification, and characterization of a protein activator (PA28) of the 20 S proteasome (macropain). J. Biol. Chem. 267 (1992), 10515–10523.
80. Marshall, R.S., Li, F., Gemperline, D.C., Book, A.J., Vierstra, R.D., Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol. Cell 58 (2015), 1053–1066.
81. Marshall, R.S., McLoughlin, F., Vierstra, R.D., Autophagic turnover of inactive 26S proteasomes in yeast is directed by the ubiquitin receptor Cue5 and the Hsp42 chaperone. Cell Rep. 16 (2016), 1717–1732.
82. Matyskiela, M.E., Lander, G.C., Martin, A., Conformational switching of the 26S proteasome enables substrate degradation. Nat. Struct. Mol. Biol. 20 (2013), 781–788.
83. McShane, E., Sin, C., Zauber, H., Wells, J.N., Donnelly, N., Wang, X., Hou, J., Chen, W., Storchova, Z., Marsh, J.A., et al. Kinetic analysis of protein stability reveals age-dependent degradation. Cell 167 (2016), 803–815.
84. Meyer, H.J., Rape, M., Enhanced protein degradation by branched ubiquitin chains. Cell 157 (2014), 910–921.
85. Myeku, N., Clelland, C.L., Emrani, S., Kukushkin, N.V., Yu, W.H., Goldberg, A.L., Duff, K.E., Tau-driven 26S proteasome impairment and cognitive dysfunction can be prevented early in disease by activating cAMP-PKA signaling. Nat. Med. 22 (2016), 46–53.
86. Nathan, J.A., Kim, H.T., Ting, L., Gygi, S.P., Goldberg, A.L., Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes?. EMBO J. 32 (2013), 552–565.
87. Ortega, J., Heymann, J.B., Kajava, A.V., Ustrell, V., Rechsteiner, M., Steven, A.C., The axial channel of the 20S proteasome opens upon binding of the PA200 activator. J. Mol. Biol. 346 (2005), 1221–1227.
88. Paraskevopoulos, K., Kriegenburg, F., Tatham, M.H., Rösner, H.I., Medina, B., Larsen, I.B., Brandstrup, R., Hardwick, K.G., Hay, R.T., Kragelund, B.B., et al. Dss1 is a 26S proteasome ubiquitin receptor. Mol. Cell 56 (2014), 453–461.
89. Peth, A., Besche, H.C., Goldberg, A.L., Ubiquitinated proteins activate the proteasome by binding to Usp14/Ubp6, which causes 20S gate opening. Mol. Cell 36 (2009), 794–804.
90. Peth, A., Uchiki, T., Goldberg, A.L., ATP-dependent steps in the binding of ubiquitin conjugates to the 26S proteasome that commit to degradation. Mol. Cell 40 (2010), 671–681.
91. Peth, A., Kukushkin, N., Bossé, M., Goldberg, A.L., Ubiquitinated proteins activate the proteasomal ATPases by binding to Usp14 or Uch37 homologs. J. Biol. Chem. 288 (2013), 7781–7790.
92. Peth, A., Nathan, J.A., Goldberg, A.L., The ATP costs and time required to degrade ubiquitinated proteins by the 26 S proteasome. J. Biol. Chem. 288 (2013), 29215–29222.
93. Piwko, W., Jentsch, S., Proteasome-mediated protein processing by bidirectional degradation initiated from an internal site. Nat. Struct. Mol. Biol. 13 (2006), 691–697.
94. Prakash, S., Tian, L., Ratliff, K.S., Lehotzky, R.E., Matouschek, A., An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 11 (2004), 830–837.
95. Qian, M.X., Pang, Y., Liu, C.H., Haratake, K., Du, B.Y., Ji, D.Y., Wang, G.F., Zhu, Q.Q., Song, W., Yu, Y., et al. Acetylation-mediated proteasomal degradation of core histones during DNA repair and spermatogenesis. Cell 153 (2013), 1012–1024.
96. Qiu, X.B., Ouyang, S.Y., Li, C.J., Miao, S., Wang, L., Goldberg, A.L., hRpn13/ADRM1/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37. EMBO J. 25 (2006), 5742–5753.
97. Rabl, J., Smith, D.M., Yu, Y., Chang, S.C., Goldberg, A.L., Cheng, Y., Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 30 (2008), 360–368.
98. Radhakrishnan, S.K., Lee, C.S., Young, P., Beskow, A., Chan, J.Y., Deshaies, R.J., Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 38 (2010), 17–28.
99. Ranek, M.J., Terpstra, E.J., Li, J., Kass, D.A., Wang, X., Protein kinase g positively regulates proteasome-mediated degradation of misfolded proteins. Circulation 128 (2013), 365–376.
100. 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 120 (2005), 73–84.
101. Rodriguez-Aliaga, P., Ramirez, L., Kim, F., Bustamante, C., Martin, A., Substrate-translocating loops regulate mechanochemical coupling and power production in AAA+ protease ClpXP. Nat. Struct. Mol. Biol. 23 (2016), 974–981.
102. Rubin, D.M., van Nocker, S., Glickman, M., Coux, O., Wefes, I., Sadis, S., Fu, H., Goldberg, A., Vierstra, R., Finley, D., ATPase and ubiquitin-binding proteins of the yeast proteasome. Mol. Biol. Rep. 24 (1997), 17–26.
103. Scanlon, T.C., Gottlieb, B., Durcan, T.M., Fon, E.A., Beitel, L.K., Trifiro, M.A., Isolation of human proteasomes and putative proteasome-interacting proteins using a novel affinity chromatography method. Exp. Cell Res. 315 (2009), 176–189.
104. Schweitzer, A., Aufderheide, A., Rudack, T., Beck, F., Pfeifer, G., Plitzko, J.M., Sakata, E., Schulten, K., Förster, F., Baumeister, W., Structure of the human 26S proteasome at a resolution of 3.9 Å. Proc. Natl. Acad. Sci. USA 113 (2016), 7816–7821.
105. Scott, D.C., Rhee, D.Y., Duda, D.M., Kelsall, I.R., Olszewski, J.L., Paulo, J.A., de Jong, A., Ovaa, H., Alpi, A.F., Harper, J.W., Schulman, B.A., Two Distinct Types of E3 Ligases Work in Unison to Regulate Substrate Ubiquitylation. Cell 166 (2016), 1198–1214.
106. Sha, Z., Goldberg, A.L., Proteasome-mediated processing of Nrf1 is essential for coordinate induction of all proteasome subunits and p97. Curr. Biol. 24 (2014), 1573–1583.
107. Sha, Z., Goldberg, A.L., Reply to Vangala et al.: Complete inhibition of the proteasome reduces new proteasome production by causing Nrf1 aggregation. Curr. Biol. 26 (2016), R836–R837.
108. Shi, Y., Chen, X., Elsasser, S., Stocks, B.B., Tian, G., Lee, B.H., Shi, Y., Zhang, N., de Poot, S.A., Tuebing, F., et al. Rpn1 provides adjacent receptor sites for substrate binding and deubiquitination by the proteasome. Science, 351, 2016, aad9421.
109. Singh, S.K., Sahu, I., Mali, S.M., Hemantha, H.P., Kleifeld, O., Glickman, M.H., Brik, A., Synthetic uncleavable ubiquitinated proteins dissect proteasome deubiquitination and degradation, and highlight distinctive fate of tetraubiquitin. J. Am. Chem. Soc. 138 (2016), 16004–16015.
110. Śledź, P., Unverdorben, P., Beck, F., Pfeifer, G., Schweitzer, A., Förster, F., Baumeister, W., Structure of the 26S proteasome with ATP-γS bound provides insights into the mechanism of nucleotide-dependent substrate translocation. Proc. Natl. Acad. Sci. USA 110 (2013), 7264–7269.
111. Smith, D.M., Kafri, G., Cheng, Y., Ng, D., Walz, T., Goldberg, A.L., ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins. Mol. Cell 20 (2005), 687–698.
112. Smith, D.M., Chang, S.C., Park, S., Finley, D., Cheng, Y., Goldberg, A.L., Docking of the proteasomal ATPases’ carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol. Cell 27 (2007), 731–744.
113. Smith, D.M., Fraga, H., Reis, C., Kafri, G., Goldberg, A.L., ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 144 (2011), 526–538.
114. Snoberger, A., Anderson, R.T., Smith, D.M., The proteasomal ATPases use a slow but highly processive strategy to unfold proteins. Front. Mol. Biosci., 4, 2017, 18.
115. Stanhill, A., Haynes, C.M., Zhang, Y., Min, G., Steele, M.C., Kalinina, J., Martinez, E., Pickart, C.M., Kong, X.P., Ron, D., An arsenite-inducible 19S regulatory particle-associated protein adapts proteasomes to proteotoxicity. Mol. Cell 23 (2006), 875–885.
116. Steffen, J., Seeger, M., Koch, A., Krüger, E., Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol. Cell 40 (2010), 147–158.
117. Stone, M., Hartmann-Petersen, R., Seeger, M., Bech-Otschir, D., Wallace, M., Gordon, C., Uch2/Uch37 is the major deubiquitinating enzyme associated with the 26S proteasome in fission yeast. J. Mol. Biol. 344 (2004), 697–706.
118. Striebel, F., Kress, W., Weber-Ban, E., Controlled destruction: AAA+ ATPases in protein degradation from bacteria to eukaryotes. Curr. Opin. Struct. Biol. 19 (2009), 209–217.
119. Thrower, J.S., Hoffman, L., Rechsteiner, M., Pickart, C.M., Recognition of the polyubiquitin proteolytic signal. EMBO J. 19 (2000), 94–102.
120. Tomko, R.J. Jr., Hochstrasser, M., Molecular architecture and assembly of the eukaryotic proteasome. Annu. Rev. Biochem. 82 (2013), 415–445.
121. van der Lee, R., Lang, B., Kruse, K., Gsponer, J., Sánchez de Groot, N., Huynen, M.A., Matouschek, A., Fuxreiter, M., Babu, M.M., Intrinsically disordered segments affect protein half-life in the cell and during evolution. Cell Rep. 8 (2014), 1832–1844.
122. Venkatraman, P., Wetzel, R., Tanaka, M., Nukina, N., Goldberg, A.L., Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol. Cell 14 (2004), 95–104.
123. Verma, R., Aravind, L., Oania, R., McDonald, W.H., Yates, J.R. 3rd, Koonin, E.V., Deshaies, R.J., Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298 (2002), 611–615.
124. Waxman, L., Fagan, J.M., Goldberg, A.L., Demonstration of two distinct high molecular weight proteases in rabbit reticulocytes, one of which degrades ubiquitin conjugates. J. Biol. Chem. 262 (1987), 2451–2457.
125. Wehmer, M., Sakata, E., Recent advances in the structural biology of the 26S proteasome. Int. J. Biochem. Cell Biol. 79 (2016), 437–442.
126. Wehmer, M., Rudack, T., Beck, F., Aufderheide, A., Pfeifer, G., Plitzko, J.M., Förster, F., Schulten, K., Baumeister, W., Sakata, E., Structural insights into the functional cycle of the ATPase module of the 26S proteasome. Proc. Natl. Acad. Sci. USA 114 (2017), 1305–1310.
127. Wilkinson, C.R., Seeger, M., Hartmann-Petersen, R., Stone, M., Wallace, M., Semple, C., Gordon, C., Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nat. Cell Biol. 3 (2001), 939–943.
128. Wilson, S.M., Bhattacharyya, B., Rachel, R.A., Coppola, V., Tessarollo, L., Householder, D.B., Fletcher, C.F., Miller, R.J., Copeland, N.G., Jenkins, N.A., Synaptic defects in ataxia mice result from a mutation in Usp14, encoding a ubiquitin-specific protease. Nat. Genet. 32 (2002), 420–425.
129. Wójcik, C., DeMartino, G.N., Intracellular localization of proteasomes. Int. J. Biochem. Cell Biol. 35 (2003), 579–589.
130. Xie, Y., Varshavsky, A., RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc. Natl. Acad. Sci. USA 98 (2001), 3056–3061.
131. Xu, P., Duong, D.M., Seyfried, N.T., Cheng, D., Xie, Y., Robert, J., Rush, J., Hochstrasser, M., Finley, D., Peng, J., Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137 (2009), 133–145.
132. Yao, T., Cohen, R.E., A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419 (2002), 403–407.
133. Yao, T., Song, L., Xu, W., DeMartino, G.N., Florens, L., Swanson, S.K., Washburn, M.P., Conaway, R.C., Conaway, J.W., Cohen, R.E., Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat. Cell Biol. 8 (2006), 994–1002.
134. Yu, Y., Smith, D.M., Kim, H.M., Rodriguez, V., Goldberg, A.L., Cheng, Y., Interactions of PAN's C-termini with archaeal 20S proteasome and implications for the eukaryotic proteasome-ATPase interactions. EMBO J. 29 (2010), 692–702.
135. Yu, H., Singh Gautam, A.K., Wilmington, S.R., Wylie, D., Martinez-Fonts, K., Kago, G., Warburton, M., Chavali, S., Inobe, T., Finkelstein, I.J., et al. Conserved sequence preferences contribute to substrate recognition by the proteasome. J. Biol. Chem. 291 (2016), 14526–14539.
136. Zhao, J., Zhai, B., Gygi, S.P., Goldberg, A.L., mTOR inhibition activates overall protein degradation by the ubiquitin proteasome system as well as by autophagy. Proc. Natl. Acad. Sci. USA 112 (2015), 15790–15797.
137. Zuin, A., Bichmann, A., Isasa, M., Puig-Sàrries, P., Díaz, L.M., Crosas, B., Rpn10 monoubiquitination orchestrates the association of the ubiquilin-type DSK2 receptor with the proteasome. Biochem. J. 472 (2015), 353–365.
138. Zwickl, P., Ng, D., Woo, K.M., Klenk, H.P., Goldberg, A.L., An archaebacterial ATPase, homologous to ATPases in the eukaryotic 26 S proteasome, activates protein breakdown by 20 S proteasomes. J. Biol. Chem. 274 (1999), 26008–26014.