Specific Modification of Aged Proteasomes Revealed by Tag-Exchangeable Knock-In Mice

REFERENCES

• Glickman MH, Ciechanover A. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428. https://doi.org/10.1152/physrev.00027.2001.
   PubMed Web of Science ®Google Scholar
• Finley D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78:477–513. https://doi.org/10.1146/annurev.biochem.78.081507.101607.
   PubMed Web of Science ®Google Scholar
• Murata S, Yashiroda H, Tanaka K. 2009. Molecular mechanisms of proteasome assembly. Nat Rev Mol Cell Biol 10:104–115. https://doi.org/10.1038/nrm2630.
   PubMed Web of Science ®Google Scholar
• Hirano Y, Hendil KB, Yashiroda H, Iemura S, Nagane R, Hioki Y, Natsume T, Tanaka K, Murata S. 2005. A heterodimeric complex that promotes the assembly of mammalian 20S proteasomes. Nature 437:1381–1385. https://doi.org/10.1038/nature04106.
   PubMed Web of Science ®Google Scholar
• Hirano Y, Hayashi H, Iemura S-I, Hendil KB, Niwa S-I, Kishimoto T, Kasahara M, Natsume T, Tanaka K, Murata S. 2006. Cooperation of multiple chaperones required for the assembly of mammalian 20S proteasomes. Mol Cell 24:977–984. https://doi.org/10.1016/j.molcel.2006.11.015.
   PubMed Web of Science ®Google Scholar
• Borodovsky A, Kessler BM, Casagrande R, Overkleeft HS, Wilkinson KD, Ploegh HL. 2001. A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14. EMBO J 20:5187–5196. https://doi.org/10.1093/emboj/20.18.5187.
   PubMed Web of Science ®Google Scholar
• Hamazaki J, Iemura S-I, Natsume T, Yashiroda H, Tanaka K, Murata S. 2006. A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J 25:4524–4536. https://doi.org/10.1038/sj.emboj.7601338.
   PubMed Web of Science ®Google Scholar
• Hiyama H, Yokoi M, Masutani C, Sugasawa K, Maekawa T, Tanaka K, Hoeijmakers JHJ, Hanaoka F. 1999. Interaction of hHR23 with S5a. J Biol Chem 274:28019–28025. https://doi.org/10.1074/jbc.274.39.28019.
   PubMed Web of Science ®Google Scholar
• Mah AL, Perry G, Smith MA, Monteiro MJ. 2000. Identification of ubiquilin, a novel presenilin interactor that increases presenilin protein accumulation. J Cell Physiol 151:847–862.
   Google Scholar
• Andersen KM, Madsen L, Prag S, Johnsen AH, Semple CA, Hendil KB, Hartmann-Petersen R. 2009. Thioredoxin Txnl1/TRP32 is a redox-active cofactor of the 26 S proteasome. J Biol Chem 284:15246–15254. https://doi.org/10.1074/jbc.M900016200.
   PubMed Web of Science ®Google Scholar
• Wiseman RL, Chin K-T, Haynes CM, Stanhill A, Xu C-F, Roguev A, Krogan NJ, Neubert TA, Ron D. 2009. Thioredoxin-related protein 32 is an arsenite-regulated thiol reductase of the proteasome 19S particle. J Biol Chem 284:15233–15245. https://doi.org/10.1074/jbc.M109.002121.
   PubMed Web of Science ®Google Scholar
• Ravid T, Hochstrasser M. 2008. Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol 9:679–690. https://doi.org/10.1038/nrm2468.
   PubMed Web of Science ®Google Scholar
• Schwartz AL, Ciechanover A. 2009. Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu Rev Pharmacol Toxicol 49:73–96. https://doi.org/10.1146/annurev.pharmtox.051208.165340.
   PubMed Web of Science ®Google Scholar
• Schmidt M, Finley D. 2014. Regulation of proteasome activity in health and disease. Biochim Biophys Acta 1843:13–25. https://doi.org/10.1016/j.bbamcr.2013.08.012.
   PubMed Web of Science ®Google Scholar
• Saez I, Vilchez D. 2014. The mechanistic links between proteasome activity, aging and age-related diseases. Curr Genomics 15:38–51. https://doi.org/10.2174/138920291501140306113344.
   PubMed Web of Science ®Google Scholar
• Dennissen FJA, Kholod N, van Leeuwen FW. 2012. The ubiquitin proteasome system in neurodegenerative diseases: culprit, accomplice or victim? Prog Neurobiol 96:190–207. https://doi.org/10.1016/j.pneurobio.2012.01.003.
   PubMed Web of Science ®Google Scholar
• Agarwal AK, Xing C, DeMartino GN, Mizrachi D, Hernandez MD, Sousa AB, Martínez de Villarreal L, dos Santos HG, Garg A. 2010. PSMB8 encoding the β5i proteasome subunit is mutated in joint contractures, muscle atrophy, microcytic anemia, and panniculitis-induced lipodystrophy syndrome. Am J Hum Genet 87:866–872. https://doi.org/10.1016/j.ajhg.2010.10.031.
   PubMed Web of Science ®Google Scholar
• Arima K, Kinoshita A, Mishima H, Kanazawa N, Kaneko T, Mizushima T, Ichinose K, Nakamura H, Tsujino A, Kawakami A, Matsunaka M, Kasagi S, Kawano S, Kumagai S, Ohmura K, Mimori T, Hirano M, Ueno S, Tanaka K, Tanaka M, Toyoshima I, Sugino H, Yamakawa A, Tanaka K, Niikawa N, Furukawa F, Murata S, Eguchi K, Ida H, Yoshiura K-I. 2011. Proteasome assembly defect due to a proteasome subunit beta type 8 (PSMB8) mutation causes the autoinflammatory disorder, Nakajo-Nishimura syndrome. Proc Natl Acad Sci U S A 108:14914–14919. https://doi.org/10.1073/pnas.1106015108.
   PubMed Web of Science ®Google Scholar
• Kitamura A, Maekawa Y, Uehara H, Izumi K, Kawachi I, Nishizawa M, Toyoshima Y, Takahashi H, Standley DM, Tanaka K, Hamazaki J, Murata S, Obara K, Toyoshima I, Yasutomo K. 2011. A mutation in the immunoproteasome subunit PSMB8 causes autoinflammation and lipodystrophy in humans. J Clin Invest 121:4150–4160. https://doi.org/10.1172/JCI58414.
   PubMed Web of Science ®Google Scholar
• Liu Y, Ramot Y, Torrelo A, Paller AS, Si N, Babay S, Kim PW, Sheikh A, Lee C-CR, Chen Y, Vera A, Zhang X, Goldbach-Mansky R, Zlotogorski A. 2012. Mutations in proteasome subunit β type 8 cause chronic atypical neutrophilic dermatosis with lipodystrophy and elevated temperature with evidence of genetic and phenotypic heterogeneity. Arthritis Rheum 64:895–907. https://doi.org/10.1002/art.33368.
   PubMed Web of Science ®Google Scholar
• Vilchez D, Morantte I, Liu Z, Douglas PM, Merkwirth C, Rodrigues APC, Manning G, Dillin A. 2012. RPN-6 determines Caenorhabditis elegans longevity under proteotoxic stress conditions. Nature 489:263–268. https://doi.org/10.1038/nature11315.
   PubMed Web of Science ®Google Scholar
• Vilchez D, Boyer L, Morantte I, Lutz M, Merkwirth C, Joyce D, Spencer B, Page L, Masliah E, Berggren WT, Gage FH, Dillin A. 2012. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature 489:304–308. https://doi.org/10.1038/nature11468.
   PubMed Web of Science ®Google Scholar
• Tonoki A, Kuranaga E, Tomioka T, Hamazaki J, Murata S, Tanaka K, Miura M. 2009. Genetic evidence linking age-dependent attenuation of the 26S proteasome with the aging process. Mol Cell Biol 29:1095–1106. https://doi.org/10.1128/MCB.01227-08.
   PubMed Web of Science ®Google Scholar
• Marshall RS, Li F, Gemperline DC, Book AJ, Vierstra RD. 2015. Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol Cell 58:1053–1066. https://doi.org/10.1016/j.molcel.2015.04.023.
   PubMed Web of Science ®Google Scholar
• Waite KA, De-La Mota-Peynado A, Vontz G, Roelofs J. 2016. Starvation induces proteasome autophagy with different pathways for core and regulatory particles. J Biol Chem 291:3239–3253. https://doi.org/10.1074/jbc.M115.699124.
   PubMed Web of Science ®Google Scholar
• Marshall RS, McLoughlin F, Vierstra RD. 2016. Autophagic turnover of inactive 26S proteasomes in yeast is directed by the ubiquitin receptor Cue5 and the Hsp42 chaperone. Cell Rep 16:1717–1732. https://doi.org/10.1016/j.celrep.2016.07.015.
   PubMed Web of Science ®Google Scholar
• Cohen-Kaplan V, Livneh I, Avni N, Fabre B, Ziv T, Kwon YT, Ciechanover A. 2016. p62- and ubiquitin-dependent stress-induced autophagy of the mammalian 26S proteasome. Proc Natl Acad Sci U S A 113:E7490–E7499. https://doi.org/10.1073/pnas.1615455113.
   PubMed Web of Science ®Google Scholar
• Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M. 2011. Global quantification of mammalian gene expression control. Nature 473:337–342. https://doi.org/10.1038/nature10098.
   PubMed Web of Science ®Google Scholar
• Tanaka K, Ichihara A. 1989. Half-life of proteasomes (multiprotease complexes) in rat liver. Biochem Biophys Res Commun 159:1309–1315. https://doi.org/10.1016/0006-291X(89)92253-5.
   PubMed Web of Science ®Google Scholar
• Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H. 1996. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci U S A 93:5860–5865. https://doi.org/10.1073/pnas.93.12.5860.
   PubMed Web of Science ®Google Scholar
• Hirano H, Kimura Y, Kimura A. 2016. Biological significance of co- and posttranslational modifications of the yeast 26S proteasome. J Proteomics 134:37–46. https://doi.org/10.1016/j.jprot.2015.11.016.
   PubMed Web of Science ®Google Scholar
• Aiken CT, Kaake RM, Wang X, Huang L. 2011. Oxidative stress-mediated regulation of proteasome complexes. Mol Cell Proteomics 10:R110.006924. https://doi.org/10.1074/mcp.M110.006924.
   PubMed Web of Science ®Google Scholar
• 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. https://doi.org/10.1016/j.yjmcc.2013.10.008.
   PubMed Web of Science ®Google Scholar
• Collins GA, Goldberg AL. 2017. The logic of the 26S proteasome. Cell 169:792–806. https://doi.org/10.1016/j.cell.2017.04.023.
   PubMed Web of Science ®Google Scholar
• Guo X, Huang X, Chen MJ. 2017. Reversible phosphorylation of the 26S proteasome. Protein Cell 8:255–272. https://doi.org/10.1007/s13238-017-0382-x.
   PubMed Web of Science ®Google Scholar
• Sell DR, Strauch CM, Shen W, Monnier VM. 2007. 2-aminoadipic acid is a marker of protein carbonyl oxidation in the aging human skin: effects of diabetes, renal failure and sepsis. Biochem J 404:269–277. https://doi.org/10.1042/BJ20061645.
   PubMed Web of Science ®Google Scholar
• Kinoshita E, Kinoshita-Kikuta E, Koike T. 2009. Separation and detection of large phosphoproteins using Phos-tag SDS-PAGE. Nat Protoc 4:1513–1521. https://doi.org/10.1038/nprot.2009.154.
   PubMed Web of Science ®Google Scholar
• Schweitzer A, Aufderheide A, Rudack T, Beck F, Pfeifer G, Plitzko JM, Sakata E, Schulten K, Förster F, Baumeister W. 2016. Structure of the human 26S proteasome at a resolution of 3.9 Å. Proc Natl Acad Sci U S A 113:7816–7821. https://doi.org/10.1073/pnas.1608050113.
   PubMed Web of Science ®Google Scholar
• Lander GC, Estrin E, Matyskiela ME, Bashore C, Nogales E, Martin A. 2012. Complete subunit architecture of the proteasome regulatory particle. Nature 482:186–191. https://doi.org/10.1038/nature10774.
   PubMed Web of Science ®Google Scholar
• Murakami Y, Matsufuji S, Kameji T, Hayashi S, Igarashi K, Tamura T, Tanaka K, Ichihara A. 1992. Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature 360:597–599. https://doi.org/10.1038/360597a0.
   PubMed Web of Science ®Google Scholar
• Yang Y, Fang S, Jensen JP, Weissman AM, Ashwell JD. 2000. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 288:874–877. https://doi.org/10.1126/science.288.5467.874.
   PubMed Web of Science ®Google Scholar
• Murata S, Sasaki K, Kishimoto T, Niwa S-I, Hayashi H, Takahama Y, Tanaka K. 2007. Regulation of CD8+ T cell development by thymus-specific proteasomes. Science 316:1349–1353. https://doi.org/10.1126/science.1141915.
   PubMed Web of Science ®Google Scholar
• Los GV, Encell LP, McDougall MG, Hartzell DD, Karassina N, Zimprich C, Wood MG, Learish R, Ohana RF, Urh M, Simpson D, Mendez J, Zimmerman K, Otto P, Vidugiris G, Zhu J, Darzins A, Klaubert DH, Bulleit RF, Wood KV. 2008. HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem Biol 3:373–382. https://doi.org/10.1021/cb800025k.
   PubMed Web of Science ®Google Scholar
• Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823. https://doi.org/10.1126/science.1231143.
   PubMed Web of Science ®Google Scholar
• Thul PJ, Åkesson L, Wiking M, Mahdessian D, Geladaki A, Ait Blal H, Alm T, Asplund A, Björk L, Breckels LM, Bäckström A, Danielsson F, Fagerberg L, Fall J, Gatto L, Gnann C, Hober S, Hjelmare M, Johansson F, Lee S, Lindskog C, Mulder J, Mulvey CM, Nilsson P, Oksvold P, Rockberg J, Schutten R, Schwenk JM, Sivertsson Å, Sjöstedt E, Skogs M, Stadler C, Sullivan DP, Tegel H, Winsnes C, Zhang C, Zwahlen M, Mardinoglu A, Pontén F, von Feilitzen K, Lilley KS, Uhlén M, Lundberg E. 2017. A subcellular map of the human proteome. Science 356:eaal3321. https://doi.org/10.1126/science.aal3321.
   PubMed Web of Science ®Google Scholar
• Litchfield DW. 2003. Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem J 369:1–15. https://doi.org/10.1042/bj20021469.
   PubMed Web of Science ®Google Scholar
• Kuo C-L, Goldberg AL. 2017. Ubiquitinated proteins promote the association of proteasomes with the deubiquitinating enzyme Usp14 and the ubiquitin ligase Ube3c. Proc Natl Acad Sci U S A 114:E3404–E3413. https://doi.org/10.1073/pnas.1701734114.
   PubMed Web of Science ®Google Scholar
• Haarer B, Aggeli D, Viggiano S, Burke DJ, Amberg DC. 2011. Novel interactions between actin and the proteasome revealed by complex haploinsufficiency. PLoS Genet 7:e1002288. https://doi.org/10.1371/journal.pgen.1002288.
   PubMedGoogle Scholar
• Gorbea C, Pratt G, Ustrell V, Bell R, Sahasrabudhe S, Hughes RE, Rechsteiner M. 2010. A protein interaction network for Ecm29 links the 26 S proteasome to molecular motors and endosomal components. J Biol Chem 285:31616–31633. https://doi.org/10.1074/jbc.M110.154120.
   PubMed Web of Science ®Google Scholar
• Hsu M-T, Guo C-L, Liou AY, Chang T-Y, Ng M-C, Florea BI, Overkleeft HS, Wu Y-L, Liao J-C, Cheng P-L. 2015. Stage-dependent axon transport of proteasomes contributes to axon development. Dev Cell 35:418–431. https://doi.org/10.1016/j.devcel.2015.10.018.
   PubMed Web of Science ®Google Scholar
• Dephoure N, Gould KL, Gygi SP, Kellogg DR. 2013. Mapping and analysis of phosphorylation sites: a quick guide for cell biologists. Mol Biol Cell 24:535–542. https://doi.org/10.1091/mbc.e12-09-0677.
   PubMed Web of Science ®Google Scholar
• Wójcik C, DeMartino GN. 2003. Intracellular localization of proteasomes. Int J Biochem Cell Biol 35:579–589. https://doi.org/10.1016/S1357-2725(02)00380-1.
   PubMed Web of Science ®Google Scholar
• Chowdhury M, Enenkel C. 2015. Intracellular dynamics of the ubiquitin-proteasome system. F1000Res 4:367. https://doi.org/10.12688/f1000research.6835.2.
   PubMedGoogle Scholar
• Laporte D, Salin B, Daignan-Fornier B, Sagot I. 2008. Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J Cell Physiol 181:737–745. https://doi.org/10.1083/jcb.200711154.
   Google Scholar
• Hendil KB, Kriegenburg F, Tanaka K, Murata S, Lauridsen A-MB, Johnsen AH, Hartmann-Petersen R. 2009. The 20S proteasome as an assembly platform for the 19S regulatory complex. J Mol Biol 394:320–328. https://doi.org/10.1016/j.jmb.2009.09.038.
   PubMed Web of Science ®Google Scholar
• Gurel PS, Hatch AL, Higgs HN. 2014. Connecting the cytoskeleton to the endoplasmic reticulum and Golgi. Curr Biol 24:R660–R672. https://doi.org/10.1016/j.cub.2014.05.033.
   PubMed Web of Science ®Google Scholar
• Sulistio YA, Heese K. 2016. The ubiquitin-proteasome system and molecular chaperone deregulation in Alzheimer’s disease. Mol Neurobiol 53:905–931. https://doi.org/10.1007/s12035-014-9063-4.
   PubMed Web of Science ®Google Scholar
• Yin R-H, Yu J-T, Tan L. 2015. The role of SORL1 in Alzheimer’s disease. Mol Neurobiol 51:909–918. https://doi.org/10.1007/s12035-014-8742-5.
   PubMed Web of Science ®Google Scholar
• Reinbothe S, Larsson A-M, Vaapil M, Wigerup C, Sun J, Jögi A, Neumann D, Rönnstrand L, Påhlman S. 2014. EPO-independent functional EPO receptor in breast cancer enhances estrogen receptor activity and promotes cell proliferation. Biochem Biophys Res Commun 445:163–169. https://doi.org/10.1016/j.bbrc.2014.01.165.
   PubMed Web of Science ®Google Scholar
• Murata S, Kawahara H, Tohma S, Yamamoto K, Kasahara M, Nabeshima Y, Tanaka K, Chiba T. 1999. Growth retardation in mice lacking the proteasome activator PA28γ. J Biol Chem 274:38211–38215. https://doi.org/10.1074/jbc.274.53.38211.
   PubMed Web of Science ®Google Scholar
• Uchida Y, Osaki T, Yamasaki T, Shimomura T, Hata S, Horikawa K, Shibata S, Todo T, Hirayama J, Nishina H. 2012. Involvement of stress kinase mitogen-activated protein kinase kinase 7 in regulation of mammalian circadian clock. J Biol Chem 287:8318–8326. https://doi.org/10.1074/jbc.M111.308908.
   PubMed Web of Science ®Google Scholar
• Kaneko T, Hamazaki J, Iemura S-I, 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. https://doi.org/10.1016/j.cell.2009.05.008.
   PubMed Web of Science ®Google Scholar
• Uechi H, Hamazaki J, Murata S. 2014. Characterization of the testis-specific proteasome subunit α4s in mammals. J Biol Chem 289:12365–12374. https://doi.org/10.1074/jbc.M114.558866.
   PubMed Web of Science ®Google Scholar
• Hamazaki J, Hirayama S, Murata S. 2015. Redundant roles of Rpn10 and Rpn13 in recognition of ubiquitinated proteins and cellular homeostasis. PLoS Genet 11:e1005401. https://doi.org/10.1371/journal.pgen.1005401.
   Google Scholar
• Hamazaki J, Sasaki K, Kawahara H, Hisanaga S-I, Tanaka K, Murata S. 2007. Rpn10-mediated degradation of ubiquitinated proteins is essential for mouse development. Mol Cell Biol 27:6629–6638. https://doi.org/10.1128/MCB.00509-07.
   PubMed Web of Science ®Google Scholar
• Moriishi K, Okabayashi T, Nakai K, Moriya K, Koike K, Murata S, Chiba T, Tanaka K, Suzuki R, Suzuki T, Miyamura T, Matsuura Y. 2003. Proteasome activator PA28-dependent nuclear retention and degradation of hepatitis C virus core protein. J Virol 77:10237–10249. https://doi.org/10.1128/JVI.77.19.10237-10249.2003.
   PubMed Web of Science ®Google Scholar
• Uechi H, Kuranaga E, Iriki T, Takano K, Hirayama S, Miura M, Hamazaki J, Murata S. 2017. Ubiquitin-binding protein CG5445 suppresses aggregation and cytotoxicity of amyotrophic lateral sclerosis-linked TDP-43 in Drosophila. Mol Cell Biol 38:e00195-17. https://doi.org/10.1128/MCB.00195-17.
   Google Scholar
• Tsuchiya H, Tanaka K, Saeki Y. 2013. The parallel reaction monitoring method contributes to a highly sensitive polyubiquitin chain quantification. Biochem Biophys Res Commun 436:223–229. https://doi.org/10.1016/j.bbrc.2013.05.080.
   PubMed Web of Science ®Google Scholar
• Koyano F, Okatsu K, Kosako H, Tamura Y, Go E, Kimura M, Kimura Y, Tsuchiya H, Yoshihara H, Hirokawa T, Endo T, Fon EA, Trempe J-F, Saeki Y, Tanaka K, Matsuda N. 2014. Ubiquitin is phosphorylated by PINK1 to activate Parkin. Nature 510:162–166. https://doi.org/10.1038/nature13392.
   PubMed Web of Science ®Google Scholar
• Brideau C, Gunter B, Pikounis B, Liaw A. 2003. Improved statistical methods for hit selection in high-throughput screening. J Biomol Screen 8:634–647. https://doi.org/10.1177/1087057103258285.
   PubMed Web of Science ®Google Scholar
• Koizumi S, Irie T, Hirayama S, Sakurai Y, Yashiroda H, Naguro I, Ichijo H, Hamazaki J, Murata S. 2016. The aspartyl protease DDI2 activates Nrf1 to compensate for proteasome dysfunction. Elife 5:e18357. https://doi.org/10.7554/eLife.18357.
   Google Scholar