Reversible phosphorylation of the 26S proteasome

Protein and Cell

Volumn 8, Issue 4, 2017, Pages 255-272

  Guo, Xing ^a   Huang, Xiuliang ^b   Chen, Mark J ^c  

^a ZHEJIANG UNIVERSITY   (China)

^b TSINGHUA UNIVERSITY   (China)

^c GENENTECH INC   (United States)

Author keywords

kinase; phosphatase; phosphorylation; proteasome; protein degradation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BICUCULLINE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II ALPHA; CASEIN KINASE II; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; DNA 26S; GAMMA INTERFERON; GYRASE INHIBITOR; HYDROGEN PEROXIDE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 14; OKADAIC ACID; PROTEASOME; SILDENAFIL; TETRODOTOXIN; UBIQUITIN LIKE DOMAIN CONTAINING CTD PHOSPHATASE 1; UNCLASSIFIED DRUG; ATP DEPENDENT 26S PROTEASE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE;

AMINO ACID SEQUENCE; BREAST CANCER; CARDIAC MUSCLE CELL; CELL CYCLE; ENZYME ACTIVITY; HIPPOCAMPUS; HUMAN; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; ANIMAL; GENETICS; METABOLISM; PHOSPHORYLATION;

ANIMALS; HUMANS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN KINASES;

EID: 85014231465     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-017-0382-x     Document Type: Review

References (163)

1. Asai M, Tsukamoto O, Minamino T, Asanuma H, Fujita M, Asano Y, Takahama H, Sasaki H, Higo S, Asakura M et al (2009) PKA rapidly enhances proteasome assembly and activity in in vivo canine hearts. J Mol Cell Cardiol 46:452–462
2. Asano S, Fukuda Y, Beck F, Aufderheide A, Forster F, Danev R, Baumeister W (2015) Proteasomes. A molecular census of 26S proteasomes in intact neurons. Science 347:439–442
3. Bai Y, Li J, Fang B, Edwards A, Zhang G, Bui M, Eschrich S, Altiok S, Koomen J, Haura EB (2012) Phosphoproteomics identifies driver tyrosine kinases in sarcoma cell lines and tumors. Cancer Res 72:2501–2511
4. Bardag-Gorce F, Venkatesh R, Li J, French BA, French SW (2004) Hyperphosphorylation of rat liver proteasome subunits: the effects of ethanol and okadaic acid are compared. Life Sci 75:585–597
5. Beausoleil SA, Villen J, Gerber SA, Rush J, Gygi SP (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 24:1285–1292
6. Becker W (2012) Emerging role of DYRK family protein kinases as regulators of protein stability in cell cycle control. Cell Cycle 11:3389–3394
7. Benedict CM, Clawson GA (1996) Nuclear multicatalytic proteinase subunit RRC3 is important for growth regulation in hepatocytes. Biochemistry 35:11612–11621
8. Bian Y, Li L, Dong M, Liu X, Kaneko T, Cheng K, Liu H, Voss C, Cao X, Wang Y et al (2016) Ultra-deep tyrosine phosphoproteomics enabled by a phosphotyrosine superbinder. Nat Chem Biol 12:959–966
9. Bingol B, Schuman EM (2006) Activity-dependent dynamics and sequestration of proteasomes in dendritic spines. Nature 441:1144–1148
10. Bingol B, Sheng M (2011) Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease. Neuron 69:22–32
11. Bingol B, Wang C-F, Arnott D, Cheng D, Peng J, Sheng M (2010) Autophosphorylated CaMKIIα acts as a Scaffold to recruit proteasomes to dendritic spines. Cell 140:567–578
12. Bose S, Brooks P, Mason GG, Rivett AJ (2001) gamma-Interferon decreases the level of 26 S proteasomes and changes the pattern of phosphorylation. Biochem J 353:291–297
13. Bose S, Stratford FL, Broadfoot KI, Mason GG, Rivett AJ (2004) Phosphorylation of 20S proteasome alpha subunit C8 (alpha7) stabilizes the 26S proteasome and plays a role in the regulation of proteasome complexes by gamma-interferon. Biochem J 378:177–184
14. Brill LM, Xiong W, Lee KB, Ficarro SB, Crain A, Xu Y, Terskikh A, Snyder EY, Ding S (2009) Phosphoproteomic analysis of human embryonic stem cells. Cell Stem Cell 5:204–213
15. Castano JG, Mahillo E, Arizti P, Arribas J (1996) Phosphorylation of C8 and C9 subunits of the multicatalytic proteinase by casein kinase II and identification of the C8 phosphorylation sites by direct mutagenesis. Biochemistry 35:3782–3789
16. Chen S, Wu J, Lu Y, Ma YB, Lee BH, Yu Z, Ouyang Q, Finley DJ, Kirschner MW, Mao Y (2016) Structural basis for dynamic regulation of the human 26S proteasome. Proc Natl Acad Sci USA 113:12991–12996
17. Chou TF, Deshaies RJ (2011) Quantitative cell-based protein degradation assays to identify and classify drugs that target the ubiquitin-proteasome system. J Biol Chem 286:16546–16554
18. Choudhary C, Olsen JV, Brandts C, Cox J, Reddy PN, Bohmer FD, Gerke V, Schmidt-Arras DE, Berdel WE, Muller-Tidow C et al (2009) Mislocalized activation of oncogenic RTKs switches downstream signaling outcomes. Mol Cell 36:326–339
19. Cui Z, Scruggs SB, Gilda JE, Ping P, Gomes AV (2014) Regulation of cardiac proteasomes by ubiquitination, SUMOylation, and beyond. J Mol Cell Cardiol 71:32–42
20. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP (2008) A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 105:10762–10767
21. Deveraux Q, Jensen C, Rechsteiner M (1995) Molecular cloning and expression of a 26 S protease subunit enriched in dileucine repeats. J Biol Chem 270:23726–23729
22. Djakovic SN, Schwarz LA, Barylko B, DeMartino GN, Patrick GN (2009) Regulation of the proteasome by neuronal activity and calcium/calmodulin-dependent protein kinase II. J Biol Chem 284:26655–26665
23. Djakovic SN, Marquez-Lona EM, Jakawich SK, Wright R, Chu C, Sutton MA, Patrick GN (2012) Phosphorylation of Rpt6 regulates synaptic strength in hippocampal neurons. J Neurosci 32:5126–5131
24. Djuranovic S, Hartmann MD, Habeck M, Ursinus A, Zwickl P, Martin J, Lupas AN, Zeth K (2009) Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol Cell 34:580–590
25. Drake JM, Graham NA, Stoyanova T, Sedghi A, Goldstein AS, Cai H, Smith DA, Zhang H, Komisopoulou E, Huang J et al (2012) Oncogene-specific activation of tyrosine kinase networks during prostate cancer progression. Proc Natl Acad Sci USA 109:1643–1648
26. Dulla K, Daub H, Hornberger R, Nigg EA, Korner R (2010) Quantitative site-specific phosphorylation dynamics of human protein kinases during mitotic progression. Mol Cell Proteomics 9:1167–1181
27. Eang R, Girbal-Neuhauser E, Xu B, Gairin JE (2009) Characterization and differential expression of a newly identified phosphorylated isoform of the human 20S proteasome beta7 subunit in tumor vs. normal cell lines. Fundam Clin Pharmacol 23:215–224
28. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6:231–242
29. Ehlinger A, Walters KJ (2013) Structural insights into proteasome activation by the 19S regulatory particle. Biochemistry 52:3618–3628
30. Feng Y, Longo DL, Ferris DK (2001) Polo-like kinase interacts with proteasomes and regulates their activity. Cell Growth Differ 12:29–37
31. Finley D (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78:477–513
32. Finley D, Chen X, Walters KJ (2016) Gates, channels, and switches: elements of the proteasome machine. Trends Biochem Sci 41:77–93
33. Franchin C, Cesaro L, Salvi M, Millioni R, Iori E, Cifani P, James P, Arrigoni G, Pinna L (2015) Quantitative analysis of a phosphoproteome readily altered by the protein kinase CK2 inhibitor quinalizarin in HEK-293T cells. Biochim Biophys Acta 1854:609–623
34. Fuhs SR, Meisenhelder J, Aslanian A, Ma L, Zagorska A, Stankova M, Binnie A, Al-Obeidi F, Mauger J, Lemke G et al (2015) Monoclonal 1- and 3-phosphohistidine antibodies: new tools to study histidine phosphorylation. Cell 162:198–210
35. Funakoshi M, Tomko RJ Jr, Kobayashi H, Hochstrasser M (2009) Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base. Cell 137:887–899
36. Gersch M, Hackl MW, Dubiella C, Dobrinevski A, Groll M, Sieber SA (2015) A mass spectrometry platform for a streamlined investigation of proteasome integrity, posttranslational modifications, and inhibitor binding. Chem Biol 22:404–411
37. Gillette TG, Hill JA (2013) PKG primes the proteasome. Circulation 128:325–327
38. Gnad F, Young A, Zhou W, Lyle K, Ong CC, Stokes MP, Silva JC, Belvin M, Friedman LS, Koeppen H et al (2013) Systems-wide analysis of K-Ras, Cdc42, and PAK4 signaling by quantitative phosphoproteomics. Mol Cell Proteomics 12:2070–2080
39. Goswami T, Li X, Smith AM, Luderowski EM, Vincent JJ, Rush J, Ballif BA (2012) Comparative phosphoproteomic analysis of neonatal and adult murine brain. Proteomics 12:2185–2189
40. Groll M, Ditzel L, Lowe J, Stock D, Bochtler M, Bartunik HD, Huber R (1997) Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386:463–471
41. Grosstessner-Hain K, Hegemann B, Novatchkova M, Rameseder J, Joughin BA, Hudecz O, Roitinger E, Pichler P, Kraut N, Yaffe MB et al (2011) Quantitative phospho-proteomics to investigate the polo-like kinase 1-dependent phospho-proteome. Mol Cell Proteomics 10(M111):008540
42. Gu TL, Goss VL, Reeves C, Popova L, Nardone J, Macneill J, Walters DK, Wang Y, Rush J, Comb MJ et al (2006) Phosphotyrosine profiling identifies the KG-1 cell line as a model for the study of FGFR1 fusions in acute myeloid leukemia. Blood 108:4202–4204
43. Guo X, Dixon JE (2016) The 26S proteasome: a cell cycle regulator regulated by cell cycle. Cell Cycle 15:875–876
44. Guo A, Villen J, Kornhauser J, Lee KA, Stokes MP, Rikova K, Possemato A, Nardone J, Innocenti G, Wetzel R et al (2008) Signaling networks assembled by oncogenic EGFR and c-Met. Proc Natl Acad Sci USA 105:692–697
45. Guo X, Engel JL, Xiao J, Tagliabracci VS, Wang X, Huang L, Dixon JE (2011) UBLCP1 is a 26S proteasome phosphatase that regulates nuclear proteasome activity. Proc Natl Acad Sci USA 108:18649–18654
46. Guo X, Wang X, Wang Z, Banerjee S, Yang J, Huang L, Dixon JE (2016) Site-specific proteasome phosphorylation controls cell proliferation and tumorigenesis. Nat Cell Biol 18:202–212
47. Haass C, Kloetzel PM (1989) The Drosophila proteasome undergoes changes in its subunit pattern during development. Exp Cell Res 180:243–252
48. Hamilton AM, Oh WC, Vega-Ramirez H, Stein IS, Hell JW, Patrick GN, Zito K (2012) Activity-dependent growth of new dendritic spines is regulated by the proteasome. Neuron 74:1023–1030
49. He Y, Guo X, Yu ZH, Wu L, Gunawan AM, Zhang Y, Dixon JE, Zhang ZY (2015) A potent and selective inhibitor for the UBLCP1 proteasome phosphatase. Bioorg Med Chem 23:2798–2809
50. Hoeller D, Dikic I (2009) Targeting the ubiquitin system in cancer therapy. Nature 458:438–444
51. Holt LJ, Tuch BB, Villen J, Johnson AD, Gygi SP, Morgan DO (2009) Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325:1682–1686
52. Hough R, Pratt G, Rechsteiner M (1987) Purification of two high molecular weight proteases from rabbit reticulocyte lysate. J Biol Chem 262:8303–8313
53. Howard CJ, Hanson-Smith V, Kennedy KJ, Miller CJ, Lou HJ, Johnson AD, Turk BE, Holt LJ (2014) Ancestral resurrection reveals evolutionary mechanisms of kinase plasticity. Elife 3:e04126
54. Huang X, Luan B, Wu J, Shi Y (2016) An atomic structure of the human 26S proteasome. Nat Struct Mol Biol 23:778–785
55. Huibregtse JM, Matouschek A (2016) Ramping up degradation for proliferation. Nat Cell Biol 18:141–142
56. Hunter T, Sefton BM (1980) Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci USA 77:1311–1315
57. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I (2008) Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481–488
58. Iliuk AB, Martin VA, Alicie BM, Geahlen RL, Tao WA (2010) In-depth analyses of kinase-dependent tyrosine phosphoproteomes based on metal ion-functionalized soluble nanopolymers. Mol Cell Proteomics 9:2162–2172
59. Imami K, Sugiyama N, Imamura H, Wakabayashi M, Tomita M, Taniguchi M, Ueno T, Toi M, Ishihama Y (2012) Temporal profiling of lapatinib-suppressed phosphorylation signals in EGFR/HER2 pathways. Mol Cell Proteomics 11:1741–1757
60. Jarome TJ, Kwapis JL, Ruenzel WL, Helmstetter FJ (2013) CaMKII, but not protein kinase A, regulates Rpt6 phosphorylation and proteasome activity during the formation of long-term memories. Front Behav Neurosci 7:115
61. Jarome TJ, Ferrara NC, Kwapis JL, Helmstetter FJ (2016) CaMKII regulates proteasome phosphorylation and activity and promotes memory destabilization following retrieval. Neurobiol Learn Mem 128:103–109
62. Johnson H, Del Rosario AM, Bryson BD, Schroeder MA, Sarkaria JN, White FM (2012) Molecular characterization of EGFR and EGFRvIII signaling networks in human glioblastoma tumor xenografts. Mol Cell Proteomics 11:1724–1740
63. Kaneko T, Hamazaki J, Iemura S, Sasaki K, Furuyama K, Natsume T, Tanaka K, Murata S (2009) Assembly pathway of the Mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 137:914–925
64. Kettenbach AN, Schweppe DK, Faherty BK, Pechenick D, Pletnev AA, Gerber SA (2011) Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci Signal 4:rs5
65. Kikuchi J, Iwafune Y, Akiyama T, Okayama A, Nakamura H, Arakawa N, Kimura Y, Hirano H (2010) Co- and post-translational modifications of the 26S proteasome in yeast. Proteomics 10:2769–2779
66. Kim BG, Lee JH, Ahn JM, Park SK, Cho JH, Hwang D, Yoo JS, Yates JR III, Ryoo HM, Cho JY (2009) ‘Two-stage double-technique hybrid (TSDTH)’ identification strategy for the analysis of BMP2-induced transdifferentiation of premyoblast C2C12 cells to osteoblast. J Proteome Res 8:4441–4454
67. Kloetzel PM (2001) Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2:179–187
68. Lee BH, Lee MJ, Park S, Oh DC, Elsasser S, Chen PC, Gartner C, Dimova N, Hanna J, Gygi SP et al (2010a) Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 467:179–184
69. Lee SH, Park Y, Yoon SK, Yoon JB (2010b) Osmotic stress inhibits proteasome by p38 MAPK-dependent phosphorylation. J Biol Chem 285:41280–41289
70. Li N, Zhang Z, Zhang W, Wei Q (2011) Calcineurin B subunit interacts with proteasome subunit alpha type 7 and represses hypoxia-inducible factor-1alpha activity via the proteasome pathway. Biochem Biophys Res Commun 405:468–472
71. Li D, Dong Q, Tao Q, Gu J, Cui Y, Jiang X, Yuan J, Li W, Xu R, Jin Y et al (2015) c-Abl regulates proteasome abundance by controlling the ubiquitin-proteasomal degradation of PSMA7 subunit. Cell Rep 10:484–496
72. Li J, Wilkinson B, Clementel VA, Hou J, O’Dell TJ, Coba MP (2016) Long-term potentiation modulates synaptic phosphorylation networks and reshapes the structure of the postsynaptic interactome. Sci Signal 9:rs8
73. Lin JT, Chang WC, Chen HM, Lai HL, Chen CY, Tao MH, Chern Y (2013) Regulation of feedback between protein kinase A and the proteasome system worsens Huntington’s disease. Mol Cell Biol 33:1073–1084
74. Liu X, Huang W, Li C, Li P, Yuan J, Li X, Qiu XB, Ma Q, Cao C (2006) Interaction between c-Abl and Arg tyrosine kinases and proteasome subunit PSMA7 regulates proteasome degradation. Mol Cell 22:317–327
75. Livneh I, Cohen-Kaplan V, Cohen-Rosenzweig C, Avni N, Ciechanover A (2016) The life cycle of the 26S proteasome: from birth, through regulation and function, and onto its death. Cell Res 26:869–885
76. Lokireddy S, Kukushkin NV, Goldberg AL (2015) cAMP-induced phosphorylation of 26S proteasomes on Rpn6/PSMD11 enhances their activity and the degradation of misfolded proteins. Proc Natl Acad Sci USA 112:E7176–7185
77. Lowery DM, Clauser KR, Hjerrild M, Lim D, Alexander J, Kishi K, Ong SE, Gammeltoft S, Carr SA, Yaffe MB (2007) Proteomic screen defines the Polo-box domain interactome and identifies Rock2 as a Plk1 substrate. Embo J 26:2262–2273
78. Lu H, Zong C, Wang Y, Young GW, Deng N, Souda P, Li X, Whitelegge J, Drews O, Yang PY et al (2008) Revealing the dynamics of the 20 S proteasome phosphoproteome: a combined CID and electron transfer dissociation approach. Mol Cell Proteomics 7:2073–2089
79. Lu Y, Lee BH, King RW, Finley D, Kirschner MW (2015) Substrate degradation by the proteasome: a single-molecule kinetic analysis. Science 348:1250834
80. Ludemann R, Lerea KM, Etlinger JD (1993) Copurification of casein kinase II with 20 S proteasomes and phosphorylation of a 30-kDa proteasome subunit. J Biol Chem 268:17413–17417
81. Lundby A, Andersen MN, Steffensen AB, Horn H, Kelstrup CD, Francavilla C, Jensen LJ, Schmitt N, Thomsen MB, Olsen JV (2013) In vivo phosphoproteomics analysis reveals the cardiac targets of beta-adrenergic receptor signaling. Sci Signal 6:rs11
82. Luo W, Slebos RJ, Hill S, Li M, Brabek J, Amanchy R, Chaerkady R, Pandey A, Ham AJ, Hanks SK (2008) Global impact of oncogenic Src on a phosphotyrosine proteome. J Proteome Res 7:3447–3460
83. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298:1912–1934
84. Marambaud P, Wilk S, Checler F (1996) Protein kinase A phosphorylation of the proteasome: a contribution to the alpha-secretase pathway in human cells. J Neurochem 67:2616–2619
85. Mason GG, Hendil KB, Rivett AJ (1996) Phosphorylation of proteasomes in mammalian cells. Identification of two phosphorylated subunits and the effect of phosphorylation on activity. Eur J Biochem 238:453–462
86. Mason GG, Murray RZ, Pappin D, Rivett AJ (1998) Phosphorylation of ATPase subunits of the 26S proteasome. FEBS Lett 430:269–274
87. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER 3rd, Hurov KE, Luo J, Bakalarski CE, Zhao Z, Solimini N, Lerenthal Y et al (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316:1160–1166
88. Matyskiela ME, Lander GC, Martin A (2013) Conformational switching of the 26S proteasome enables substrate degradation. Nat Struct Mol Biol 20:781–788
89. Mayya V, Lundgren DH, Hwang SI, Rezaul K, Wu L, Eng JK, Rodionov V, Han DK (2009) Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci Signal 2:ra46
90. Mertins P, Yang F, Liu T, Mani DR, Petyuk VA, Gillette MA, Clauser KR, Qiao JW, Gritsenko MA, Moore RJ et al (2014) Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Mol Cell Proteomics 13:1690–1704
91. Moreno D, Knecht E, Viollet B, Sanz P (2008) A769662, a novel activator of AMP-activated protein kinase, inhibits non-proteolytic components of the 26S proteasome by an AMPK-independent mechanism. FEBS Lett 582:2650–2654
92. Murata S, Sasaki K, Kishimoto T, Niwa S, Hayashi H, Takahama Y, Tanaka K (2007) Regulation of CD8+ T cell development by thymus-specific proteasomes. Science 316:1349–1353
93. Murata S, Yashiroda H, Tanaka K (2009) Molecular mechanisms of proteasome assembly. Nat Rev Mol Cell Biol 10:104–115
94. Murray PF, Pardo PS, Zelada AM, Passeron S (2002) In vivo and in vitro phosphorylation of Candida albicans 20S proteasome. Arch Biochem Biophys 404:116–125
95. Myeku N, Wang H, Figueiredo-Pereira ME (2012) cAMP stimulates the ubiquitin/proteasome pathway in rat spinal cord neurons. Neurosci Lett 527:126–131
96. Myeku N, Clelland CL, Emrani S, Kukushkin NV, Yu WH, Goldberg AL, Duff KE (2016) Tau-driven 26S proteasome impairment and cognitive dysfunction can be prevented early in disease by activating cAMP-PKA signaling. Nat Med 22:46–53
97. Nagano K, Shinkawa T, Mutoh H, Kondoh O, Morimoto S, Inomata N, Ashihara M, Ishii N, Aoki Y, Haramura M (2009) Phosphoproteomic analysis of distinct tumor cell lines in response to nocodazole treatment. Proteomics 9:2861–2874
98. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127:635–648
99. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, Jensen LJ, Gnad F, Cox J, Jensen TS, Nigg EA et al (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3:ra3
100. Pack CG, Yukii H, Toh-e A, Kudo T, Tsuchiya H, Kaiho A, Sakata E, Murata S, Yokosawa H, Sako Y et al (2014) Quantitative live-cell imaging reveals spatio-temporal dynamics and cytoplasmic assembly of the 26S proteasome. Nat Commun 5:3396
101. Pan C, Olsen JV, Daub H, Mann M (2009) Global effects of kinase inhibitors on signaling networks revealed by quantitative phosphoproteomics. Mol Cell Proteomics 8:2796–2808
102. Pardo PS, Murray PF, Walz K, Franco L, Passeron S (1998) In vivo and in vitro phosphorylation of the alpha 7/PRS1 subunit of Saccharomyces cerevisiae 20 S proteasome: in vitro phosphorylation by protein kinase CK2 is absolutely dependent on polylysine. Arch Biochem Biophys 349:397–401
103. Park S, Roelofs J, Kim W, Robert J, Schmidt M, Gygi SP, Finley D (2009) Hexameric assembly of the proteasomal ATPases is templated through their C termini. Nature 459:866–870
104. Pereira ME, Wilk S (1990) Phosphorylation of the multicatalytic proteinase complex from bovine pituitaries by a copurifying cAMP-dependent protein kinase. Arch Biochem Biophys 283:68–74
105. Peth A, Kukushkin N, Bosse M, Goldberg AL (2013) Ubiquitinated proteins activate the proteasomal ATPases by binding to Usp14 or Uch37 homologs. J Biol Chem 288:7781–7790
106. Petrocca F, Altschuler G, Tan SM, Mendillo ML, Yan H, Jerry DJ, Kung AL, Hide W, Ince TA, Lieberman J (2013) A genome-wide siRNA screen identifies proteasome addiction as a vulnerability of basal-like triple-negative breast cancer cells. Cancer Cell 24:182–196
107. Rabl J, Smith DM, Yu Y, Chang SC, Goldberg AL, Cheng Y (2008) Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol Cell 30:360–368
108. Rainer PP, Kass DA (2016) Old dog, new tricks: novel cardiac targets and stress regulation by protein kinase G. Cardiovasc Res 111:154–162
109. Ranek MJ, Terpstra EJ, Li J, Kass DA, Wang X (2013) Protein kinase g positively regulates proteasome-mediated degradation of misfolded proteins. Circulation 128:365–376
110. Rigbolt KT, Prokhorova TA, Akimov V, Henningsen J, Johansen PT, Kratchmarova I, Kassem M, Mann M, Olsen JV, Blagoev B (2011) System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci Signal 4:rs3
111. Rikova K, Guo A, Zeng Q, Possemato A, Yu J, Haack H, Nardone J, Lee K, Reeves C, Li Y et al (2007) Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131:1190–1203
112. Rivett JA, Bose S, Brooks P, Broadfoot KI (2001) Regulation of proteasome complexes by γ-interferon and phosphorylation. Biochimie 83:363–366
113. Roelofs J, Park S, Haas W, Tian G, McAllister FE, Huo Y, Lee BH, Zhang F, Shi Y, Gygi SP et al (2009) Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 459:861–865
114. Ruperez P, Gago-Martinez A, Burlingame AL, Oses-Prieto JA (2012) Quantitative phosphoproteomic analysis reveals a role for serine and threonine kinases in the cytoskeletal reorganization in early T cell receptor activation in human primary T cells. Mol Cell Proteomics 11:171–186
115. Rush J, Moritz A, Lee KA, Guo A, Goss VL, Spek EJ, Zhang H, Zha XM, Polakiewicz RD, Comb MJ (2005) Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat Biotechnol 23:94–101
116. Santamaria A, Wang B, Elowe S, Malik R, Zhang F, Bauer M, Schmidt A, Sillje HH, Korner R, Nigg EA (2011) The Plk1-dependent phosphoproteome of the early mitotic spindle. Mol Cell Proteomics 10(M110):004457
117. Santarius T, Shipley J, Brewer D, Stratton MR, Cooper CS (2010) A census of amplified and overexpressed human cancer genes. Nat Rev Cancer 10:59–64
118. Satoh K, Nishikawa T, Yokosawa H, Sawada H (1995) Phosphorylation of proteasome substrate by a protein kinase associated with the 26 S proteasome is linked to the ATP-dependent proteolysis of the 26 S proteasome. Biochem Biophys Res Commun 213:7–14
119. Satoh K, Sasajima H, Nyoumura K-I, Yokosawa H, Sawada H (2000) Assembly of the 26S proteasome is regulated by phosphorylation of the p45/Rpt6 ATPase subunit. Biochemistry 40:314–319
120. Schmidt M, Finley D (2014) Regulation of proteasome activity in health and disease. Biochim Biophys Acta 1843:13–25
121. Schmidt F, Dahlmann B, Hustoft HK, Koehler CJ, Strozynski M, Kloss A, Zimny-Arndt U, Jungblut PR, Thiede B (2011) Quantitative proteome analysis of the 20S proteasome of apoptotic Jurkat T cells. Amino Acids 41:351–361
122. Schreiner P, Chen X, Husnjak K, Randles L, Zhang N, Elsasser S, Finley D, Dikic I, Walters KJ, Groll M (2008) Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 453:548–552
123. Schweitzer A, Aufderheide A, Rudack T, Beck F, Pfeifer G, Plitzko JM, Sakata E, Schulten K, Forster F, Baumeister W (2016) Structure of the human 26S proteasome at a resolution of 3.9 A. Proc Natl Acad Sci USA 113:7816–7821
124. Scruggs SB, Zong NC, Wang D, Stefani E, Ping P (2012) Post-translational modification of cardiac proteasomes: functional delineation enabled by proteomics. Am J Physiol Heart Circ Physiol 303:H9–18
125. Sha Z, Peth A, Goldberg AL (2011) Keeping proteasomes under control—a role for phosphorylation in the nucleus. Proc Natl Acad Sci USA 108:18573–18574
126. Sharma K, D’Souza RC, Tyanova S, Schaab C, Wisniewski JR, Cox J, Mann M (2014) Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Rep 8:1583–1594
127. Shi Y, Chen X, Elsasser S, Stocks BB, Tian G, Lee BH, Shi Y, Zhang N, de Poot SA, Tuebing F et al (2016) Rpn1 provides adjacent receptor sites for substrate binding and deubiquitination by the proteasome. Science. doi:10.1126/science.aad9421
128. Smith DM, Kafri G, Cheng Y, Ng D, Walz T, Goldberg AL (2005) ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins. Mol Cell 20:687–698
129. Smith DM, Chang SC, Park S, Finley D, Cheng Y, Goldberg AL (2007) Docking of the proteasomal ATPases’ carboxyl termini in the 20S proteasome’s alpha ring opens the gate for substrate entry. Mol Cell 27:731–744
130. Stadtmueller BM, Hill CP (2011) Proteasome activators. Mol Cell 41:8–19
131. Stokes MP, Rush J, Macneill J, Ren JM, Sprott K, Nardone J, Yang V, Beausoleil SA, Gygi SP, Livingstone M et al (2007) Profiling of UV-induced ATM/ATR signaling pathways. Proc Natl Acad Sci USA 104:19855–19860
132. Taipale M, Krykbaeva I, Koeva M, Kayatekin C, Westover KD, Karras GI, Lindquist S (2012) Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150:987–1001
133. Tan CS, Pasculescu A, Lim WA, Pawson T, Bader GD, Linding R (2009) Positive selection of tyrosine loss in metazoan evolution. Science 325:1686–1688
134. Trost M, Sauvageau M, Herault O, Deleris P, Pomies C, Chagraoui J, Mayotte N, Meloche S, Sauvageau G, Thibault P (2012) Posttranslational regulation of self-renewal capacity: insights from proteome and phosphoproteome analyses of stem cell leukemia. Blood 120:e17–27
135. Tsai CF, Wang YT, Yen HY, Tsou CC, Ku WC, Lin PY, Chen HY, Nesvizhskii AI, Ishihama Y, Chen YJ (2015) Large-scale determination of absolute phosphorylation stoichiometries in human cells by motif-targeting quantitative proteomics. Nat Commun 6:6622
136. Uechi H, Hamazaki J, Murata S (2014) Characterization of the testis-specific proteasome subunit alpha4s in mammals. J Biol Chem 289:12365–12374
137. Um JW, Im E, Park J, Oh Y, Min B, Lee HJ, Yoon JB, Chung KC (2010) ASK1 negatively regulates the 26 S proteasome. J Biol Chem 285:36434–36446
138. Umeda M, Manabe Y, Uchimiya H (1997) Phosphorylation of the C2 subunit of the proteasome in rice (Oryza sativa L.). FEBS Lett 403:313–317
139. Unno M, Mizushima T, Morimoto Y, Tomisugi Y, Tanaka K, Yasuoka N, Tsukihara T (2002) The structure of the mammalian 20S proteasome at 2.75 A resolution. Structure 10:609–618
140. Unverdorben P, Beck F, Sledz P, Schweitzer A, Pfeifer G, Plitzko JM, Baumeister W, Forster F (2014) Deep classification of a large cryo-EM dataset defines the conformational landscape of the 26S proteasome. Proc Natl Acad Sci USA 111:5544–5549
141. van de Weerdt BC, Medema RH (2006) Polo-like kinases: a team in control of the division. Cell Cycle 5:853–864
142. Verma R, Aravind L, Oania R, McDonald WH, Yates JR 3rd, Koonin EV, Deshaies RJ (2002) Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298:611–615
143. Viana R, Aguado C, Esteban I, Moreno D, Viollet B, Knecht E, Sanz P (2008) Role of AMP-activated protein kinase in autophagy and proteasome function. Biochem Biophys Res Commun 369:964–968
144. Wang X, Huang L (2008) Identifying dynamic interactors of protein complexes by quantitative mass spectrometry. Mol Cell Proteomics 7:46–57
145. Wang X, Chen CF, Baker PR, Chen PL, Kaiser P, Huang L (2007) Mass spectrometric characterization of the affinity-purified human 26S proteasome complex. Biochemistry 46:3553–3565
146. Wang S, Zhang M, Liang B, Xu J, Xie Z, Liu C, Viollet B, Yan D, Zou MH (2010) AMPKalpha2 deletion causes aberrant expression and activation of NAD(P)H oxidase and consequent endothelial dysfunction in vivo: role of 26S proteasomes. Circ Res 106:1117–1128
147. Wang R, Ferraris JD, Izumi Y, Dmitrieva N, Ramkissoon K, Wang G, Gucek M, Burg MB (2014) Global discovery of high-NaCl-induced changes of protein phosphorylation. Am J Physiol Cell Physiol 307:C442–454
148. Wani PS, Suppahia A, Capalla X, Ondracek A, Roelofs J (2016) Phosphorylation of the C-terminal tail of proteasome subunit alpha7 is required for binding of the proteasome quality control factor Ecm29. Sci Rep 6:27873
149. Waxman L, Fagan JM, Goldberg AL (1987) Demonstration of two distinct high molecular weight proteases in rabbit reticulocytes, one of which degrades ubiquitin conjugates. J Biol Chem 262:2451–2457
150. Weintz G, Olsen JV, Fruhauf K, Niedzielska M, Amit I, Jantsch J, Mages J, Frech C, Dolken L, Mann M et al (2010) The phosphoproteome of toll-like receptor-activated macrophages. Mol Syst Biol 6:371
151. Williams GR, Bethard JR, Berkaw MN, Nagel AK, Luttrell LM, Ball LE (2016) Exploring G protein-coupled receptor signaling networks using SILAC-based phosphoproteomics. Methods 92:36–50
152. Worden EJ, Padovani C, Martin A (2014) Structure of the Rpn11-Rpn8 dimer reveals mechanisms of substrate deubiquitination during proteasomal degradation. Nat Struct Mol Biol 21:220–227
153. Wu R, Haas W, Dephoure N, Huttlin EL, Zhai B, Sowa ME, Gygi SP (2011) A large-scale method to measure absolute protein phosphorylation stoichiometries. Nat Methods 8:677–683
154. Wu X, Tian L, Li J, Zhang Y, Han V, Li Y, Xu X, Li H, Chen X, Chen J et al (2012) Investigation of receptor interacting protein (RIP3)-dependent protein phosphorylation by quantitative phosphoproteomics. Mol Cell Proteomics 11:1640–1651
155. Xu J, Wang AH, Oses-Prieto J, Makhijani K, Katsuno Y, Pei M, Yan L, Zheng YG, Burlingame A, Bruckner K et al (2013) Arginine methylation initiates BMP-induced Smad signaling. Mol Cell 51:5–19
156. Yano M, Mori S, Kido H (1999) Intrinsic nucleoside diphosphate kinase-like activity is a novel function of the 20 S proteasome. J Biol Chem 274:34375–34382
157. Yao T, Cohen RE (2002) A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419:403–407
158. Yu Y, Smith DM, Kim HM, Rodriguez V, Goldberg AL, Cheng Y (2010) Interactions of PAN’s C-termini with archaeal 20S proteasome and implications for the eukaryotic proteasome-ATPase interactions. Embo J 29:692–702
159. Yuan F, Ma Y, You P, Lin W, Lu H, Yu Y, Wang X, Jiang J, Yang P, Ma Q et al (2013) A novel role of proteasomal beta1 subunit in tumorigenesis. Biosci Rep 33:e0050
160. Zhang W, Wei Q (2011) Calcineurin stimulates the expression of inflammatory factors in RAW 264.7 cells by interacting with proteasome subunit alpha type 6. Biochem Biophys Res Commun 407:668–673
161. Zhang F, Hu Y, Huang P, Toleman CA, Paterson AJ, Kudlow JE (2007a) Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of Rpt6. J Biol Chem 282:22460–22471
162. Zhang F, Paterson AJ, Huang P, Wang K, Kudlow JE (2007b) Metabolic control of proteasome function. Physiology (Bethesda) 22:373–379
163. Zong C, Gomes AV, Drews O, Li X, Young GW, Berhane B, Qiao X, French SW, Bardag-Gorce F, Ping P (2006) Regulation of murine cardiac 20S proteasomes: role of associating partners. Circ Res 99:372–380