Reversible phosphorylation of the 26S proteasome

Xing Guo, Xiuliang Huang, Mark J. Chen

PDF(1426 KB)
PDF(1426 KB)
Protein Cell ›› 2017, Vol. 8 ›› Issue (4) : 255-272. DOI: 10.1007/s13238-017-0382-x
REVIEW
REVIEW

Reversible phosphorylation of the 26S proteasome

Author information +
History +

Abstract

The 26S proteasome at the center of the ubiquitinproteasome system (UPS) is essential for virtually all cellular processes of eukaryotes. A common misconception about the proteasome is that, once made, it remains as a static and uniform complex with spontaneous and constitutive activity for protein degradation. Recent discoveries have provided compelling evidence to support the exact opposite insomuch as the 26S proteasome undergoes dynamic and reversible phosphorylation under a variety of physiopathological conditions. In this review, we summarize the history and current understanding of proteasome phosphorylation, and advocate the idea of targeting proteasome kinases/phosphatases as a new strategy for clinical interventions of several human diseases.

Keywords

proteasome / phosphorylation / kinase / phosphatase / protein degradation

Cite this article

Download citation ▾
Xing Guo, Xiuliang Huang, Mark J. Chen. Reversible phosphorylation of the 26S proteasome. Protein Cell, 2017, 8(4): 255‒272 https://doi.org/10.1007/s13238-017-0382-x

References

[1]
AsaiM, TsukamotoO, MinaminoT, AsanumaH, FujitaM, AsanoY, TakahamaH, SasakiH, HigoS, AsakuraM (2009) PKA rapidly enhances proteasome assembly and activity in in vivo canine hearts.J Mol Cell Cardiol46:452–462
CrossRef Google scholar
[2]
AsanoS, FukudaY, BeckF, AufderheideA, ForsterF, DanevR, BaumeisterW (2015) Proteasomes. A molecular census of 26S proteasomes in intact neurons.Science347:439–442
CrossRef Google scholar
[3]
BaiY, LiJ, FangB, EdwardsA, ZhangG, BuiM, EschrichS, AltiokS, KoomenJ, HauraEB (2012) Phosphoproteomics identifies driver tyrosine kinases in sarcoma cell lines and tumors.Cancer Res72:2501–2511
CrossRef Google scholar
[4]
Bardag-GorceF, VenkateshR, LiJ, FrenchBA, FrenchSW (2004) Hyperphosphorylation of rat liver proteasome subunits: the effects of ethanol and okadaic acid are compared.Life Sci75:585–597
CrossRef Google scholar
[5]
BeausoleilSA, VillenJ, GerberSA, RushJ, GygiSP (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization.Nat Biotechnol24: 1285–1292
CrossRef Google scholar
[6]
BeckerW (2012) Emerging role of DYRK family protein kinases as regulators of protein stability in cell cycle control.Cell Cycle11:3389–3394
CrossRef Google scholar
[7]
BenedictCM, ClawsonGA (1996) Nuclear multicatalytic proteinase subunit RRC3 is important for growth regulation in hepatocytes.Biochemistry35:11612–11621
CrossRef Google scholar
[8]
BianY, LiL, DongM, LiuX, KanekoT, ChengK, LiuH, VossC, CaoX, WangY (2016) Ultra-deep tyrosine phosphoproteomics enabled by a phosphotyrosine superbinder.Nat Chem Biol12:959–966
CrossRef Google scholar
[9]
BingolB, SchumanEM (2006) Activity-dependent dynamics and sequestration of proteasomes in dendritic spines.Nature441:1144–1148
CrossRef Google scholar
[10]
BingolB, ShengM (2011) Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease.Neuron69:22–32
CrossRef Google scholar
[11]
BingolB, WangC-F, ArnottD, ChengD, PengJ, ShengM (2010) Autophosphorylated CaMKIIα acts as a Scaffold to recruit proteasomes to dendritic spines.Cell140:567–578
CrossRef Google scholar
[12]
BoseS, BrooksP, MasonGG, RivettAJ (2001) gamma-Interferon decreases the level of 26 S proteasomes and changes the pattern of phosphorylation.Biochem J353:291–297
[13]
BoseS, StratfordFL, BroadfootKI, MasonGG, RivettAJ (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 J378:177–184
CrossRef Google scholar
[14]
BrillLM, XiongW, LeeKB, FicarroSB, CrainA, XuY, TerskikhA, SnyderEY, DingS (2009) Phosphoproteomic analysis of human embryonic stem cells.Cell Stem Cell5:204–213
CrossRef Google scholar
[15]
CastanoJG, MahilloE, AriztiP, ArribasJ (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.Biochemistry35:3782–3789
CrossRef Google scholar
[16]
ChenS, WuJ, LuY, MaYB, LeeBH, YuZ, OuyangQ, FinleyDJ, KirschnerMW, MaoY(2016) Structural basis for dynamic regulation of the human 26S proteasome.Proc Natl Acad Sci USA113:12991–12996
CrossRef Google scholar
[17]
ChouTF, DeshaiesRJ (2011) Quantitative cell-based protein degradation assays to identify and classify drugs that target the ubiquitin-proteasome system.J Biol Chem286:16546–16554
CrossRef Google scholar
[18]
ChoudharyC, OlsenJV, BrandtsC, CoxJ, ReddyPN, BohmerFD, GerkeV, Schmidt-ArrasDE, BerdelWE, Muller-TidowC (2009) Mislocalized activation of oncogenic RTKs switches downstream signaling outcomes.Mol Cell36:326–339
CrossRef Google scholar
[19]
CuiZ, ScruggsSB, GildaJE, PingP, GomesAV (2014) Regulation of cardiac proteasomes by ubiquitination, SUMOylation, and beyond.J Mol Cell Cardiol71:32–42
CrossRef Google scholar
[20]
DephoureN, ZhouC, VillenJ, BeausoleilSA, BakalarskiCE, ElledgeSJ, GygiSP (2008) A quantitative atlas of mitotic phosphorylation.Proc Natl Acad Sci USA105:10762–10767
CrossRef Google scholar
[21]
DeverauxQ, JensenC, RechsteinerM (1995) Molecular cloning and expression of a 26 S protease subunit enriched in dileucine repeats.J Biol Chem270:23726–23729
CrossRef Google scholar
[22]
DjakovicSN, SchwarzLA, BarylkoB, DeMartinoGN, PatrickGN (2009) Regulation of the proteasome by neuronal activity and calcium/calmodulin-dependent protein kinase II.J Biol Chem284:26655–26665
CrossRef Google scholar
[23]
DjakovicSN, Marquez-LonaEM, JakawichSK, WrightR, ChuC, SuttonMA, PatrickGN (2012) Phosphorylation of Rpt6 regulates synaptic strength in hippocampal neurons.J Neurosci32:5126–5131
CrossRef Google scholar
[24]
DjuranovicS, HartmannMD, HabeckM, UrsinusA, ZwicklP, MartinJ, LupasAN, ZethK (2009) Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases.Mol Cell34:580–590
CrossRef Google scholar
[25]
DrakeJM, GrahamNA, StoyanovaT, SedghiA, GoldsteinAS, CaiH, SmithDA, ZhangH, KomisopoulouE, HuangJ (2012) Oncogene-specific activation of tyrosine kinase networks during prostate cancer progression.Proc Natl Acad Sci USA109:1643–1648
CrossRef Google scholar
[26]
DullaK, DaubH, HornbergerR, NiggEA, KornerR (2010) Quantitative site-specific phosphorylation dynamics of human protein kinases during mitotic progression.Mol Cell Proteomics9:1167–1181
CrossRef Google scholar
[27]
EangR, Girbal-NeuhauserE, XuB, GairinJE (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 Pharmacol23:215–224
CrossRef Google scholar
[28]
EhlersMD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system.Nat Neurosci6:231–242
CrossRef Google scholar
[29]
EhlingerA, WaltersKJ (2013) Structural insights into proteasome activationby the19Sregulatory particle.Biochemistry52:3618–3628
CrossRef Google scholar
[30]
FengY, LongoDL, FerrisDK (2001) Polo-like kinase interacts with proteasomes and regulates their activity.Cell Growth Differ12:29–37
[31]
FinleyD (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome.Annu Rev Biochem78:477–513
CrossRef Google scholar
[32]
FinleyD, ChenX, WaltersKJ (2016) Gates, channels, and switches: elements of the proteasome machine.Trends Biochem Sci41:77–93
CrossRef Google scholar
[33]
FranchinC, CesaroL, SalviM, MillioniR, IoriE, CifaniP, JamesP, ArrigoniG, PinnaL (2015) Quantitative analysis of a phosphoproteome readily altered by the protein kinase CK2 inhibitor quinalizarin in HEK-293T cells.Biochim Biophys Acta1854:609–623
CrossRef Google scholar
[34]
FuhsSR, MeisenhelderJ, AslanianA, MaL, ZagorskaA, StankovaM, BinnieA, Al-ObeidiF, MaugerJ, LemkeG (2015) Monoclonal 1- and 3-phosphohistidine antibodies: new tools to study histidine phosphorylation.Cell162:198–210
CrossRef Google scholar
[35]
FunakoshiM, TomkoRJ Jr, KobayashiH, HochstrasserM (2009) Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base.Cell137:887–899
CrossRef Google scholar
[36]
GerschM, HacklMW, DubiellaC, DobrinevskiA, GrollM, SieberSA (2015) A mass spectrometry platform for a streamlined investigation of proteasome integrity, posttranslational modifications, and inhibitor binding.Chem Biol22:404–411
CrossRef Google scholar
[37]
GilletteTG, HillJA (2013) PKG primes the proteasome.Circulation128:325–327
CrossRef Google scholar
[38]
GnadF, YoungA, ZhouW, LyleK, OngCC, StokesMP, SilvaJC, BelvinM, FriedmanLS, KoeppenH (2013) Systems-wide analysis of K-Ras, Cdc42, and PAK4 signaling by quantitative phosphoproteomics.Mol Cell Proteomics12:2070–2080
CrossRef Google scholar
[39]
GoswamiT, LiX, SmithAM, LuderowskiEM, VincentJJ, RushJ, BallifBA (2012) Comparative phosphoproteomic analysis of neonatal and adult murine brain.Proteomics12:2185–2189
CrossRef Google scholar
[40]
GrollM, DitzelL, LoweJ, StockD, BochtlerM, BartunikHD, HuberR (1997) Structure of 20S proteasome from yeast at 2.4 A resolution.Nature386:463–471
CrossRef Google scholar
[41]
Grosstessner-HainK, HegemannB, NovatchkovaM, RamesederJ, JoughinBA, HudeczO, RoitingerE, PichlerP, KrautN, YaffeMB (2011) Quantitative phospho-proteomics to investigate the polo-like kinase 1-dependent phospho-proteome.Mol Cell Proteomics10(M111):008540
CrossRef Google scholar
[42]
GuTL, GossVL, ReevesC, PopovaL, NardoneJ, MacneillJ, WaltersDK, WangY, RushJ, CombMJ (2006) Phosphotyrosine profiling identifies the KG-1 cell line as a model for the study of FGFR1 fusions in acute myeloid leukemia.Blood108:4202–4204
CrossRef Google scholar
[43]
GuoX, DixonJE (2016) The 26S proteasome: a cell cycle regulator regulated by cell cycle.Cell Cycle15:875–876
CrossRef Google scholar
[44]
GuoA, VillenJ, KornhauserJ, LeeKA, StokesMP, RikovaK, PossematoA, NardoneJ, InnocentiG, WetzelR (2008) Signaling networks assembled by oncogenic EGFR and c-Met.Proc Natl Acad Sci USA105:692–697
CrossRef Google scholar
[45]
GuoX, EngelJL, XiaoJ, TagliabracciVS, WangX, HuangL, DixonJE (2011) UBLCP1 is a 26S proteasome phosphatase that regulates nuclear proteasome activity.Proc Natl Acad Sci USA108:18649–18654
CrossRef Google scholar
[46]
GuoX, WangX, WangZ, BanerjeeS, YangJ, HuangL, DixonJE (2016) Site-specific proteasome phosphorylation controls cell proliferation and tumorigenesis.Nat Cell Biol18:202–212
CrossRef Google scholar
[47]
HaassC, KloetzelPM (1989) The Drosophila proteasome undergoes changes in its subunit pattern during development.Exp Cell Res180:243–252
CrossRef Google scholar
[48]
HamiltonAM, OhWC, Vega-RamirezH, SteinIS, HellJW, PatrickGN, ZitoK (2012) Activity-dependent growth of new dendritic spines is regulated by the proteasome.Neuron74:1023–1030
CrossRef Google scholar
[49]
HeY, GuoX, YuZH, WuL, GunawanAM, ZhangY, DixonJE, ZhangZY (2015) A potent and selective inhibitor for the UBLCP1 proteasome phosphatase.Bioorg Med Chem23:2798–2809
CrossRef Google scholar
[50]
HoellerD, DikicI (2009) Targeting the ubiquitin system in cancer therapy.Nature458:438–444
CrossRef Google scholar
[51]
HoltLJ, TuchBB, VillenJ, JohnsonAD, GygiSP, MorganDO (2009) Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution.Science325:1682–1686
CrossRef Google scholar
[52]
HoughR, PrattG, RechsteinerM (1987) Purification of two high molecular weight proteases from rabbit reticulocyte lysate.J Biol Chem262:8303–8313
[53]
HowardCJ, Hanson-SmithV, KennedyKJ, MillerCJ, LouHJ, JohnsonAD, TurkBE, HoltLJ (2014) Ancestral resurrection reveals evolutionary mechanisms of kinase plasticity.Elife3:e04126
CrossRef Google scholar
[54]
HuangX, LuanB, WuJ, ShiY (2016) An atomic structure of the human 26S proteasome.Nat Struct Mol Biol23:778–785
CrossRef Google scholar
[55]
HuibregtseJM, MatouschekA (2016) Ramping up degradation for proliferation.Nat Cell Biol18:141–142
CrossRef Google scholar
[56]
HunterT, SeftonBM (1980) Transforming gene product of Rous sarcoma virus phosphorylates tyrosine.Proc Natl Acad Sci USA77:1311–1315
CrossRef Google scholar
[57]
HusnjakK, ElsasserS, ZhangN, ChenX, RandlesL, ShiY, HofmannK, WaltersKJ, FinleyD, DikicI (2008) Proteasome subunit Rpn13 is a novel ubiquitin receptor.Nature453:481–488
CrossRef Google scholar
[58]
IliukAB, MartinVA, AlicieBM, GeahlenRL, TaoWA (2010) In-depth analyses of kinase-dependent tyrosine phosphoproteomes based on metal ion-functionalized soluble nanopolymers.Mol Cell Proteomics9:2162–2172
CrossRef Google scholar
[59]
ImamiK, SugiyamaN, ImamuraH, WakabayashiM, TomitaM, TaniguchiM, UenoT, ToiM, IshihamaY (2012) Temporal profiling of lapatinib-suppressed phosphorylation signals in EGFR/HER2 pathways.Mol Cell Proteomics11:1741–1757
CrossRef Google scholar
[60]
JaromeTJ, KwapisJL, RuenzelWL, HelmstetterFJ (2013) CaMKII, but not protein kinase A, regulates Rpt6 phosphorylation and proteasome activity during the formation of long-term memories.Front Behav Neurosci7:115
CrossRef Google scholar
[61]
JaromeTJ, FerraraNC, KwapisJL, HelmstetterFJ (2016) CaMKII regulates proteasome phosphorylation and activity and promotes memory destabilization following retrieval.Neurobiol Learn Mem128:103–109
CrossRef Google scholar
[62]
JohnsonH, Del RosarioAM, BrysonBD, SchroederMA, SarkariaJN, WhiteFM (2012) Molecular characterization of EGFR and EGFRvIII signaling networks in human glioblastoma tumor xenografts.Mol Cell Proteomics11:1724–1740
CrossRef Google scholar
[63]
KanekoT, HamazakiJ, IemuraS, SasakiK, FuruyamaK, NatsumeT, TanakaK, MurataS (2009) Assembly pathway of the Mammalian proteasome base subcomplex is mediated by multiple specific chaperones.Cell137:914–925
CrossRef Google scholar
[64]
KettenbachAN, SchweppeDK, FahertyBK, PechenickD, PletnevAA, GerberSA (2011) Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells.Sci Signal4:rs5
CrossRef Google scholar
[65]
KikuchiJ, IwafuneY, AkiyamaT, OkayamaA, NakamuraH, ArakawaN, KimuraY, HiranoH (2010) Co- and post-translational modifications of the 26S proteasome in yeast.Proteomics10:2769–2779
CrossRef Google scholar
[66]
KimBG, LeeJH, AhnJM, ParkSK, ChoJH, HwangD, YooJS, YatesJR III, RyooHM, ChoJY(2009) ‘Two-stage doubletechnique hybrid (TSDTH)’ identification strategy for the analysis of BMP2-induced transdifferentiation of premyoblast C2C12 cells to osteoblast.J Proteome Res8:4441–4454
CrossRef Google scholar
[67]
KloetzelPM (2001) Antigen processing by the proteasome.Nat Rev Mol Cell Biol2:179–187
CrossRef Google scholar
[68]
LeeBH, LeeMJ, ParkS, OhDC, ElsasserS, ChenPC, GartnerC, DimovaN, HannaJ, GygiSP (2010a) Enhancement of proteasome activity by a small-molecule inhibitor of USP14.Nature467:179–184
CrossRef Google scholar
[69]
LeeSH, ParkY, YoonSK, YoonJB (2010b) Osmotic stress inhibits proteasome by p38 MAPK-dependent phosphorylation.J Biol Chem285:41280–41289
CrossRef Google scholar
[70]
LiN, ZhangZ, ZhangW, WeiQ (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 Commun405:468–472
CrossRef Google scholar
[71]
LiD, DongQ, TaoQ, GuJ, CuiY, JiangX, YuanJ, LiW, XuR, JinY (2015) c-Abl regulates proteasome abundance by controlling the ubiquitin-proteasomal degradation of PSMA7 subunit.Cell Rep10:484–496
CrossRef Google scholar
[72]
LiJ, WilkinsonB, ClementelVA, HouJ, O’DellTJ, CobaMP (2016) Long-term potentiation modulates synaptic phosphorylation networks and reshapes the structure of the postsynaptic interactome.Sci Signal9:rs8
CrossRef Google scholar
[73]
LinJT, ChangWC, ChenHM, LaiHL, ChenCY, TaoMH, ChernY (2013) Regulation of feedback between protein kinase A and the proteasome system worsens Huntington’s disease.Mol Cell Biol33:1073–1084
CrossRef Google scholar
[74]
LiuX, HuangW, LiC, LiP, YuanJ, LiX, QiuXB, MaQ, CaoC(2006) Interaction between c-Abl and Arg tyrosine kinases and proteasome subunit PSMA7 regulates proteasome degradation.Mol Cell22:317–327
CrossRef Google scholar
[75]
LivnehI, Cohen-KaplanV, Cohen-RosenzweigC, AvniN, CiechanoverA (2016) The life cycle of the 26S proteasome: from birth, through regulation and function, and onto its death.Cell Res26:869–885
CrossRef Google scholar
[76]
LokireddyS, KukushkinNV, GoldbergAL (2015) cAMP-induced phosphorylation of 26S proteasomes on Rpn6/PSMD11 enhances their activity and the degradation of misfolded proteins.Proc Natl Acad Sci USA112:E7176–7185
CrossRef Google scholar
[77]
LoweryDM, ClauserKR, HjerrildM, LimD, AlexanderJ, KishiK, OngSE, GammeltoftS, CarrSA, YaffeMB (2007) Proteomic screen defines the Polo-box domain interactome and identifies Rock2 as a Plk1 substrate.Embo J26:2262–2273
CrossRef Google scholar
[78]
LuH, ZongC, WangY, YoungGW, DengN, SoudaP, LiX, WhiteleggeJ, DrewsO, YangPY (2008) Revealing the dynamics of the 20 S proteasome phosphoproteome: a combined CID and electron transfer dissociation approach.Mol Cell Proteomics7:2073–2089
CrossRef Google scholar
[79]
LuY, LeeBH, KingRW, FinleyD, KirschnerMW (2015) Substrate degradation by the proteasome: a single-molecule kinetic analysis.Science348:1250834
CrossRef Google scholar
[80]
LudemannR, LereaKM, EtlingerJD (1993) Copurification of casein kinase II with 20 S proteasomes and phosphorylation of a 30-kDa proteasome subunit.J Biol Chem268:17413–17417
[81]
LundbyA, AndersenMN, SteffensenAB, HornH, KelstrupCD, FrancavillaC, JensenLJ, SchmittN, ThomsenMB, OlsenJV (2013) In vivo phosphoproteomics analysis reveals the cardiac targets of beta-adrenergic receptor signaling.Sci Signal6:rs11
CrossRef Google scholar
[82]
LuoW, SlebosRJ, HillS, LiM, BrabekJ, AmanchyR, ChaerkadyR, PandeyA, HamAJ, HanksSK (2008) Global impact of oncogenic Src on a phosphotyrosine proteome.J Proteome Res7:3447–3460
CrossRef Google scholar
[83]
ManningG, WhyteDB, MartinezR, HunterT, SudarsanamS (2002) The protein kinase complement of the human genome.Science298:1912–1934
CrossRef Google scholar
[84]
MarambaudP, WilkS, CheclerF (1996) Protein kinase A phosphorylation of the proteasome: a contribution to the alpha-secretase pathway in human cells.J Neurochem67:2616–2619
CrossRef Google scholar
[85]
MasonGG, HendilKB, RivettAJ (1996) Phosphorylation of proteasomes in mammalian cells. Identification of two phosphorylated subunits and the effect of phosphorylation on activity.Eur J Biochem238:453–462
CrossRef Google scholar
[86]
MasonGG, MurrayRZ, PappinD, RivettAJ (1998) Phosphorylation of ATPase subunits of the 26S proteasome.FEBS Lett430: 269–274
CrossRef Google scholar
[87]
MatsuokaS, BallifBA, SmogorzewskaA, McDonaldER 3rd, HurovKE, LuoJ, BakalarskiCE, ZhaoZ, SoliminiN, LerenthalY (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage.Science316:1160–1166
CrossRef Google scholar
[88]
MatyskielaME, LanderGC, MartinA (2013) Conformational switching of the 26S proteasome enables substrate degradation.Nat Struct Mol Biol20:781–788
CrossRef Google scholar
[89]
MayyaV, LundgrenDH, HwangSI, RezaulK, WuL, EngJK, RodionovV, HanDK (2009) Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions.Sci Signal2:ra46
CrossRef Google scholar
[90]
MertinsP, YangF, LiuT, ManiDR, PetyukVA, GilletteMA, ClauserKR, QiaoJW, GritsenkoMA, MooreRJ (2014) Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels.Mol Cell Proteomics13:1690–1704
CrossRef Google scholar
[91]
MorenoD, KnechtE, ViolletB, SanzP (2008) A769662, a novel activator of AMP-activated protein kinase, inhibits non-proteolytic components of the 26S proteasome by an AMPK-independent mechanism.FEBS Lett582:2650–2654
CrossRef Google scholar
[92]
MurataS, SasakiK, KishimotoT, NiwaS, HayashiH, TakahamaY, TanakaK (2007) Regulation of CD8+ T cell development by thymus-specific proteasomes.Science316:1349–1353
CrossRef Google scholar
[93]
MurataS, YashirodaH, TanakaK (2009) Molecular mechanisms of proteasome assembly.Nat Rev Mol Cell Biol10:104–115
CrossRef Google scholar
[94]
MurrayPF, PardoPS, ZeladaAM, PasseronS (2002) In vivo and in vitro phosphorylation of Candida albicans 20S proteasome.Arch Biochem Biophys404:116–125
CrossRef Google scholar
[95]
MyekuN, WangH, Figueiredo-PereiraME (2012) cAMP stimulates the ubiquitin/proteasome pathway in rat spinal cord neurons.Neurosci Lett527:126–131
CrossRef Google scholar
[96]
MyekuN, ClellandCL, EmraniS, KukushkinNV, YuWH, GoldbergAL, DuffKE (2016) Tau-driven 26S proteasome impairment and cognitive dysfunction can be prevented early in disease by activating cAMP-PKA signaling.Nat Med22:46–53
CrossRef Google scholar
[97]
NaganoK, ShinkawaT, MutohH, KondohO, MorimotoS, InomataN, AshiharaM, IshiiN, AokiY, HaramuraM (2009) Phosphoproteomic analysis of distinct tumor cell lines in response to nocodazole treatment.Proteomics9:2861–2874
CrossRef Google scholar
[98]
OlsenJV, BlagoevB, GnadF, MacekB, KumarC, MortensenP, MannM (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks.Cell127:635–648
CrossRef Google scholar
[99]
OlsenJV, VermeulenM, SantamariaA, KumarC, MillerML, JensenLJ, GnadF, CoxJ, JensenTS, NiggEA (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis.Sci Signal3:ra3
CrossRef Google scholar
[100]
PackCG, YukiiH, Toh-eA, KudoT, TsuchiyaH, KaihoA, SakataE, MurataS, YokosawaH, SakoY (2014) Quantitative live-cell imaging reveals spatio-temporal dynamics and cytoplasmic assembly of the 26S proteasome.Nat Commun5:3396
CrossRef Google scholar
[101]
PanC, OlsenJV, DaubH, MannM (2009) Global effects of kinase inhibitors on signaling networks revealed by quantitative phosphoproteomics.Mol Cell Proteomics8:2796–2808
CrossRef Google scholar
[102]
PardoPS, MurrayPF,WalzK, FrancoL, PasseronS(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 Biophys349:397–401
CrossRef Google scholar
[103]
ParkS, RoelofsJ, KimW, RobertJ, SchmidtM, GygiSP, FinleyD (2009) Hexameric assembly of the proteasomal ATPases is templated through their C termini.Nature459:866–870
CrossRef Google scholar
[104]
PereiraME, WilkS (1990) Phosphorylation of the multicatalytic proteinase complex from bovine pituitaries by a copurifying cAMP-dependent protein kinase.Arch Biochem Biophys283:68–74
CrossRef Google scholar
[105]
PethA, KukushkinN, BosseM, GoldbergAL (2013) Ubiquitinated proteins activate the proteasomal ATPases by binding to Usp14 or Uch37 homologs.J Biol Chem288:7781–7790
CrossRef Google scholar
[106]
PetroccaF, AltschulerG, TanSM, MendilloML, YanH, JerryDJ, KungAL, HideW, InceTA, LiebermanJ (2013) A genome-wide siRNA screen identifies proteasome addiction as a vulnerability of basal-like triple-negative breast cancer cells.Cancer Cell24:182–196
CrossRef Google scholar
[107]
RablJ, SmithDM, YuY, ChangSC, GoldbergAL, ChengY (2008) Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases.Mol Cell30:360–368
CrossRef Google scholar
[108]
RainerPP, KassDA (2016) Old dog, new tricks: novel cardiac targets and stress regulation by protein kinase G.Cardiovasc Res111:154–162
CrossRef Google scholar
[109]
RanekMJ, TerpstraEJ, LiJ, KassDA, WangX (2013) Protein kinase g positively regulates proteasome-mediated degradation of misfolded proteins.Circulation128:365–376
CrossRef Google scholar
[110]
RigboltKT, ProkhorovaTA, AkimovV, HenningsenJ, JohansenPT, KratchmarovaI, KassemM, MannM, OlsenJV, BlagoevB (2011) System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation.Sci Signal4:rs3
CrossRef Google scholar
[111]
RikovaK, GuoA, ZengQ, PossematoA, YuJ, HaackH, NardoneJ, LeeK, ReevesC, LiY (2007) Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer.Cell131:1190–1203
CrossRef Google scholar
[112]
RivettJA, BoseS, BrooksP, BroadfootKI (2001) Regulation of proteasome complexes by γ-interferon and phosphorylation.Biochimie83:363–366
CrossRef Google scholar
[113]
RoelofsJ, ParkS, HaasW, TianG, McAllisterFE, HuoY, LeeBH, ZhangF, ShiY, GygiSP (2009) Chaperone-mediated pathway of proteasome regulatory particle assembly.Nature459:861–865
CrossRef Google scholar
[114]
RuperezP, Gago-MartinezA, BurlingameAL, Oses-PrietoJA (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 Proteomics11:171–186
CrossRef Google scholar
[115]
RushJ, MoritzA, LeeKA, GuoA, GossVL, SpekEJ, ZhangH, ZhaXM, PolakiewiczRD, CombMJ (2005) Immunoaffinity profiling of tyrosine phosphorylation in cancer cells.Nat Biotechnol23:94–101
CrossRef Google scholar
[116]
SantamariaA, WangB, EloweS, MalikR, ZhangF, BauerM, SchmidtA, SilljeHH, KornerR, NiggEA (2011) The Plk1-dependent phosphoproteome of the early mitotic spindle.Mol Cell Proteomics10(M110):004457
CrossRef Google scholar
[117]
SantariusT, ShipleyJ, BrewerD, StrattonMR, CooperCS (2010) A census of amplified and overexpressed human cancer genes.Nat Rev Cancer10:59–64
CrossRef Google scholar
[118]
SatohK, NishikawaT, YokosawaH, SawadaH (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 Commun213:7–14
CrossRef Google scholar
[119]
SatohK, SasajimaH, NyoumuraK-I, YokosawaH, SawadaH (2000) Assembly of the 26S proteasome is regulated by phosphorylation of the p45/Rpt6 ATPase subunit.Biochemistry40:314–319
CrossRef Google scholar
[120]
SchmidtM, FinleyD (2014) Regulation of proteasome activity in health and disease.Biochim Biophys Acta1843:13–25
CrossRef Google scholar
[121]
SchmidtF, DahlmannB, HustoftHK, KoehlerCJ, StrozynskiM, KlossA, Zimny-ArndtU, JungblutPR, ThiedeB (2011) Quantitative proteome analysis of the 20S proteasome of apoptotic Jurkat T cells.Amino Acids41:351–361
CrossRef Google scholar
[122]
SchreinerP, ChenX, HusnjakK, RandlesL, ZhangN, ElsasserS, FinleyD, DikicI, WaltersKJ, GrollM (2008) Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction.Nature453:548–552
CrossRef Google scholar
[123]
SchweitzerA, AufderheideA, RudackT, BeckF, PfeiferG, PlitzkoJM, SakataE, SchultenK, ForsterF, BaumeisterW (2016) Structure of the human 26S proteasome at a resolution of 3.9 A.Proc Natl Acad Sci USA113:7816–7821
CrossRef Google scholar
[124]
ScruggsSB, ZongNC, WangD, StefaniE, PingP (2012) Posttranslational modification of cardiac proteasomes: functional delineation enabled by proteomics.Am J Physiol Heart Circ Physiol303:H9–18
CrossRef Google scholar
[125]
ShaZ, PethA, GoldbergAL (2011) Keeping proteasomes under control—a role for phosphorylation in the nucleus.Proc Natl Acad Sci USA108:18573–18574
CrossRef Google scholar
[126]
SharmaK, D’SouzaRC, TyanovaS, SchaabC, WisniewskiJR, CoxJ, MannM (2014) Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling.Cell Rep8:1583–1594
CrossRef Google scholar
[127]
ShiY, ChenX, ElsasserS, StocksBB, TianG, LeeBH, ShiY, ZhangN, de PootSA, TuebingF (2016)Rpn1 provides adjacent receptor sites for substrate binding and deubiquitination by the proteasome.Science.
CrossRef Google scholar
[128]
SmithDM, KafriG, ChengY, NgD, WalzT, GoldbergAL (2005) ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins.Mol Cell20:687–698
CrossRef Google scholar
[129]
SmithDM, ChangSC, ParkS, FinleyD, ChengY, GoldbergAL (2007) Docking of the proteasomal ATPases’ carboxyl termini in the 20S proteasome’s alpha ring opens the gate for substrate entry.Mol Cell27:731–744
CrossRef Google scholar
[130]
StadtmuellerBM, HillCP (2011) Proteasome activators.Mol Cell41:8–19
CrossRef Google scholar
[131]
StokesMP, RushJ, MacneillJ, RenJM, SprottK, NardoneJ, YangV, BeausoleilSA, GygiSP, LivingstoneM (2007) Profiling of UV-induced ATM/ATR signaling pathways.Proc Natl Acad Sci USA104:19855–19860
CrossRef Google scholar
[132]
TaipaleM, KrykbaevaI, KoevaM, KayatekinC, WestoverKD, KarrasGI, LindquistS (2012) Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition.Cell150:987–1001
CrossRef Google scholar
[133]
TanCS, PasculescuA, LimWA, PawsonT, BaderGD, LindingR (2009) Positive selection of tyrosine loss in metazoan evolution.Science325:1686–1688
CrossRef Google scholar
[134]
TrostM, SauvageauM, HeraultO, DelerisP, PomiesC, ChagraouiJ, MayotteN, MelocheS, SauvageauG, ThibaultP (2012) Posttranslational regulation of self-renewal capacity: insights from proteome and phosphoproteome analyses of stem cell leukemia.Blood120:e17–27
CrossRef Google scholar
[135]
TsaiCF, WangYT, YenHY, TsouCC, KuWC, LinPY, ChenHY, NesvizhskiiAI, IshihamaY, ChenYJ (2015) Large-scale determination of absolute phosphorylation stoichiometries in human cells by motif-targeting quantitative proteomics.Nat Commun6:6622
CrossRef Google scholar
[136]
UechiH, HamazakiJ, MurataS (2014) Characterization of the testisspecific proteasome subunit alpha4s in mammals.J Biol Chem289:12365–12374
CrossRef Google scholar
[137]
UmJW, ImE, ParkJ, OhY, MinB, LeeHJ, YoonJB, ChungKC (2010) ASK1 negatively regulates the 26 S proteasome.J Biol Chem285:36434–36446
CrossRef Google scholar
[138]
UmedaM, ManabeY, UchimiyaH (1997) Phosphorylation of the C2 subunit of the proteasome in rice (Oryza sativa L.).FEBS Lett403:313–317
CrossRef Google scholar
[139]
UnnoM, MizushimaT, MorimotoY, TomisugiY, TanakaK, YasuokaN, TsukiharaT (2002) The structure of the mammalian 20S proteasome at 2.75 A resolution.Structure10:609–618
CrossRef Google scholar
[140]
UnverdorbenP, BeckF, SledzP, SchweitzerA, PfeiferG, PlitzkoJM, BaumeisterW, ForsterF (2014) Deep classification of a large cryo-EM dataset defines the conformational landscape of the 26S proteasome.Proc Natl Acad Sci USA111:5544–5549
CrossRef Google scholar
[141]
van de WeerdtBC, MedemaRH (2006) Polo-like kinases: a team in control of the division.Cell Cycle5:853–864
CrossRef Google scholar
[142]
VermaR, AravindL, OaniaR, McDonaldWH, YatesJR 3rd, KooninEV, DeshaiesRJ (2002) Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome.Science298:611–615
CrossRef Google scholar
[143]
VianaR, AguadoC, EstebanI, MorenoD, ViolletB, KnechtE, SanzP (2008) Role of AMP-activated protein kinase in autophagy and proteasome function.Biochem Biophys Res Commun369: 964–968
CrossRef Google scholar
[144]
WangX, HuangL (2008) Identifying dynamic interactors of protein complexes by quantitative mass spectrometry.Mol Cell Proteomics7:46–57
CrossRef Google scholar
[145]
WangX, ChenCF, BakerPR, ChenPL, KaiserP, HuangL (2007) Mass spectrometric characterization of the affinity-purified human 26S proteasome complex.Biochemistry46:3553–3565
CrossRef Google scholar
[146]
WangS, ZhangM, LiangB, XuJ, XieZ, LiuC, ViolletB, YanD, ZouMH (2010) AMPKalpha2 deletion causes aberrant expression and activation of NAD(P)H oxidase and consequent endothelial dysfunction in vivo: role of 26S proteasomes.Circ Res106: 1117–1128
CrossRef Google scholar
[147]
WangR, FerrarisJD, IzumiY, DmitrievaN, RamkissoonK, WangG, GucekM, BurgMB (2014) Global discovery of high-NaCl-induced changes of protein phosphorylation.Am J Physiol Cell Physiol307:C442–454
CrossRef Google scholar
[148]
WaniPS, SuppahiaA, CapallaX, OndracekA, RoelofsJ (2016) Phosphorylation of the C-terminal tail of proteasome subunit alpha7 is required for binding of the proteasome quality control factor Ecm29.Sci Rep6:27873
CrossRef Google scholar
[149]
WaxmanL, FaganJM, GoldbergAL (1987) Demonstration of two distinct high molecular weight proteases in rabbit reticulocytes, one of which degrades ubiquitin conjugates.J Biol Chem262:2451–2457
[150]
WeintzG, OlsenJV, FruhaufK, NiedzielskaM, AmitI, JantschJ, MagesJ, FrechC, DolkenL, MannM (2010) The phosphoproteome of toll-like receptor-activated macrophages.Mol Syst Biol6:371
CrossRef Google scholar
[151]
WilliamsGR, BethardJR, BerkawMN, NagelAK, LuttrellLM, BallLE (2016) Exploring G protein-coupled receptor signaling networks using SILAC-based phosphoproteomics.Methods92:36–50
CrossRef Google scholar
[152]
WordenEJ, PadovaniC, MartinA (2014) Structure of the Rpn11-Rpn8 dimer reveals mechanisms of substrate deubiquitination during proteasomal degradation.Nat Struct Mol Biol21:220–227
CrossRef Google scholar
[153]
WuR, HaasW, DephoureN, HuttlinEL, ZhaiB, SowaME, GygiSP (2011) A large-scale method to measure absolute protein phosphorylation stoichiometries.Nat Methods8:677–683
CrossRef Google scholar
[154]
WuX, TianL, LiJ, ZhangY, HanV, LiY, XuX, LiH, ChenX, ChenJ (2012) Investigation of receptor interacting protein (RIP3)-dependent protein phosphorylation by quantitative phosphoproteomics.Mol Cell Proteomics11:1640–1651
CrossRef Google scholar
[155]
XuJ, WangAH, Oses-PrietoJ, MakhijaniK, KatsunoY, PeiM, YanL, ZhengYG, BurlingameA, BrucknerK (2013) Arginine methylation initiates BMP-induced Smad signaling.Mol Cell51:5–19
CrossRef Google scholar
[156]
YanoM, MoriS, KidoH (1999) Intrinsic nucleoside diphosphate kinase-like activity is a novel function of the 20 S proteasome.J Biol Chem274:34375–34382
CrossRef Google scholar
[157]
YaoT, CohenRE (2002) A cryptic protease couples deubiquitination and degradation by the proteasome.Nature419:403–407
CrossRef Google scholar
[158]
YuY, SmithDM, KimHM, RodriguezV, GoldbergAL, ChengY (2010) Interactions of PAN’s C-termini with archaeal 20S proteasome and implications for the eukaryotic proteasome-ATPase interactions.Embo J29:692–702
CrossRef Google scholar
[159]
YuanF, MaY, YouP, LinW, LuH, YuY, WangX, JiangJ, YangP, MaQ (2013) A novel role of proteasomal beta1 subunit in tumorigenesis.Biosci Rep33:e0050
CrossRef Google scholar
[160]
ZhangW, WeiQ (2011) Calcineurin stimulates the expression of inflammatory factors in RAW 264.7 cells by interacting with proteasome subunit alpha type 6.Biochem Biophys Res Commun407:668–673
CrossRef Google scholar
[161]
ZhangF, HuY, HuangP, TolemanCA, PatersonAJ, KudlowJE (2007a) Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of Rpt6.J Biol Chem282:22460–22471
CrossRef Google scholar
[162]
ZhangF, PatersonAJ, HuangP, WangK, KudlowJE (2007b) Metabolic control of proteasome function.Physiology (Bethesda)22:373–379
CrossRef Google scholar
[163]
ZongC, GomesAV, DrewsO, LiX, YoungGW, BerhaneB, QiaoX, FrenchSW, Bardag-GorceF, PingP (2006) Regulation of murine cardiac 20S proteasomes: role of associating partners.Circ Res99:372–380
CrossRef Google scholar

RIGHTS & PERMISSIONS

2017 The Author(s) 2017. This article is published with open access at Springerlink.com and journal.hep.com.cn
AI Summary AI Mindmap
PDF(1426 KB)

Accesses

Citations

Detail

Sections
Recommended

/