195
Views
15
CrossRef citations to date
0
Altmetric
Review

Proteasome, a Promising Therapeutic Target for Multiple Diseases Beyond Cancer

, , , , , , & show all
Pages 4327-4342 | Published online: 19 Oct 2020

References

  • HannaJ, Guerra-MorenoA, AngJ, MicoogullariY. Protein degradation and the pathologic basis of disease. Am J Pathol. 2019;189(1):94–103. doi:10.1016/j.ajpath.2018.09.00430312581
  • BedfordL, LoweJ, DickLR, MayerRJ, BrownellJE. Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat Rev Drug Discov. 2011;10(1):29–46. doi:10.1038/nrd332121151032
  • DohmenRJ, HuibregtseJ, ScheffnerM. Ubiquitin, Ubiquitin-Like Proteins, and Proteasome-Mediated Degradation. Encyclopedia Cell Biol. 2016;1:582–595.
  • Meyer-SchwesingerC. The ubiquitin-proteasome system in kidney physiology and disease. Nat Rev Nephrol. 2019;15(7):393–411. doi:10.1038/s41581-019-0148-131036905
  • KarG, KeskinO, FraternaliF, GursoyA. Emerging role of the ubiquitin-proteasome system as drug targets. Curr Pharm Des. 2013;19(18):3175–3189. doi:10.2174/138161281131918000223151131
  • Mata-CanteroL, Lobato-GilS, AilletF, et al. The Ubiquitin-Proteasome System (UPS) as a Cancer Drug Target: Emerging Mechanisms and Therapeutics. 2015.
  • CollinsGA, GoldbergAL. The Logic of the 26S Proteasome. Cell. 2017;169(5):792–806. doi:10.1016/j.cell.2017.04.02328525752
  • MicelLN, TentlerJJ, SmithPG, EckhardtGS. Role of ubiquitin ligases and the proteasome in oncogenesis: novel targets for anticancer therapies. J Clin Oncol. 2013;31(9):1231–1238. doi:10.1200/JCO.2012.44.095823358974
  • JungT, GruneT. The proteasome and the degradation of oxidized proteins: part I-structure of proteasomes. Redox Biol. 2013;1:178–182. doi:10.1016/j.redox.2013.01.00424024151
  • DouQP. Targeting tumor ubiquitin-proteasome pathway with new and old drugs. Curr Cancer Drug Targets. 2011;11(3):236–238. doi:10.2174/15680091179451978921247390
  • FrezzaM, SchmittS, DouQP. Targeting the ubiquitin-proteasome pathway: an emerging concept in cancer therapy. Curr Top Med Chem. 2011;11(23):2888–2905. doi:10.2174/15680261179828131121824109
  • BerkersCR, OvaaH. Drug discovery and assay development in the ubiquitin-proteasome system. Biochem Soc Trans. 2010;38(Pt1):14–20. doi:10.1042/BST038001420074028
  • MattinglyLH, GaultRA, MurphyWJ. Use of systemic proteasome inhibition as an immune-modulating agent in disease. Endocr Metab Immune Disord Drug Targets. 2007;7(1):29–34. doi:10.2174/18715300778005939717346202
  • HuH. Abnormal protein aggregation and neurodegenerative diseases. Chin Sci Bull. 2001;46(1):1–3.
  • CaoB, MaoX. The ubiquitin-proteasomal system is critical for multiple myeloma: implications in drug discovery. Am J Blood Res. 2011;1(1):46–56.22432065
  • HideshimaT, BradnerJE, WongJ, et al. Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc Natl Acad Sci U S A. 2005;102(24):8567–8572. doi:10.1073/pnas.050322110215937109
  • HolkovaB, GrantS. Proteasome inhibitors in mantle cell lymphoma. Best Pract Res Clin Haematol. 2012;25(2):133–141. doi:10.1016/j.beha.2012.04.00722687449
  • SpanoJP, BayJO, BlayJY, RixeO. Proteasome inhibition: a new approach for the treatment of malignancies. Bull Cancer. 2005;92(11):E61–66, 945–952.
  • WangJ, MaldonadoMA. The ubiquitin-proteasome system and its role in inflammatory and autoimmune diseases. Cell Mol Immunol. 2006;3(4):255–261.16978533
  • Kish-TrierE, HillCP. Structural biology of the proteasome. Annu Rev Biophys. 2013;42:29–49. doi:10.1146/annurev-biophys-083012-13041723414347
  • JungT, CatalgolB, GruneT. The proteasomal system. Mol Aspects Med. 2009;30(4):191–296. doi:10.1016/j.mam.2009.04.00119371762
  • HiranoY, KanekoT, OkamotoK, et al. Dissecting beta-ring assembly pathway of the mammalian 20S proteasome. EMBO J. 2008;27(16):2204–2213. doi:10.1038/emboj.2008.14818650933
  • SaekiY, TanakaK. Assembly and function of the proteasome. Methods Mol Biol. 2012;832:315–337.22350895
  • HuberEM, BaslerM, SchwabR, et al. Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell. 2012;148(4):727–738. doi:10.1016/j.cell.2011.12.03022341445
  • BaslerM, GroettrupM. Immunoproteasome-specific inhibitors and their application. Methods Mol Biol. 2012;832:391–401.22350900
  • FinleyD. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem. 2009;78:477–513. doi:10.1146/annurev.biochem.78.081507.10160719489727
  • GlickmanMH, RubinDM, CouxO, et al. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell. 1998;94(5):615–623. doi:10.1016/S0092-8674(00)81603-79741626
  • YaoT, CohenRE. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature. 2002;419(6905):403–407. doi:10.1038/nature0107112353037
  • CrommPM, CrewsCM. The proteasome in modern drug discovery: second life of a highly valuable drug target. ACS Central Sci. 2017;3(8):830–838.
  • Menéndez-BenitoV, VerhoefLGGC, MasucciMG, DantumaNP. Endoplasmic reticulum stress compromises the ubiquitin-proteasome system. Hum Mol Genet. 2005;14(19):2787–2799. doi:10.1093/hmg/ddi31216103128
  • HayRT, VuillardL, DesterroJM, RodriguezMS. Control of NF-kappa B transcriptional activation by signal induced proteolysis of I kappa B alpha. Philos Trans R Soc Lond B Biol Sci. 1999;354(1389):1601–1609. doi:10.1098/rstb.1999.050410582246
  • AdamsJ. The proteasome: structure, function, and role in the cell. Cancer Treat Rev. 2003;29(Suppl 1):3–9. doi:10.1016/S0305-7372(03)00081-1
  • CrawfordLJ, WalkerB, IrvineAE. Proteasome inhibitors in cancer therapy. J Cell Commun Signal. 2011;5(2):101–110. doi:10.1007/s12079-011-0121-721484190
  • MoreauP, RichardsonPG, CavoM, et al. Proteasome inhibitors in multiple myeloma: 10 years later. 2012;120(5):947–959.
  • XieSC, DickLR, GouldA, BrandS, TilleyL. The proteasome as a target for protozoan parasites. Expert Opin Ther Targets. 2019;23(11):903–914. doi:10.1080/14728222.2019.168598131679410
  • MitsiadesC, MitsiadesN, HideshimaT, RichardsonP, AndersonK. Proteasome inhibition as a therapeutic strategy for hematologic malignancies. Expert Rev Anticancer Ther. 2005;5:465–476. doi:10.1586/14737140.5.3.46516001954
  • RichardsonP. Clinical update: proteasome inhibitors in hematologic malignancies. Cancer Treat Rev. 2003;29(Suppl 1):33–39. doi:10.1016/S0305-7372(03)00080-X12738241
  • MikhaelJ, ChangH. Bortezomib: proteasome inhibition as a novel mechanism of cancer therapy-implications for hematological malignancies. Lett Drug Des Discov. 2007;4:82–86. doi:10.2174/157018007779422541
  • KhareS, NagleAS, BiggartA, et al. Proteasome inhibition for treatment of leishmaniasis, Chagas disease and sleeping sickness. Nature. 2016;537(7619):229–233. doi:10.1038/nature1933927501246
  • FierabracciA. Proteasome inhibitors: a new perspective for treating autoimmune diseases. Curr Drug Targets. 2012;13(13):1665–1675. doi:10.2174/13894501280353005323092126
  • YingZ, WangH, WangG. The ubiquitin proteasome system as a potential target for the treatment of neurodegenerative diseases. Curr Pharm Des. 2013;19(18):3305–3314. doi:10.2174/138161281131918001323151138
  • Bibo-VerdugoB, JiangZ, CaffreyCR, O’DonoghueAJ. Targeting proteasomes in infectious organisms to combat disease. FEBS J. 2017;284(10):1503–1517.28122162
  • LiH, PonderEL, VerdoesM, et al. Validation of the proteasome as a therapeutic target in Plasmodium using an epoxyketone inhibitor with parasite-specific toxicity. Chem Biol. 2012;19(12):1535–1545. doi:10.1016/j.chembiol.2012.09.01923142757
  • ReynoldsJM, El BissatiK, BrandenburgJ, GunzlA, MamounCB. Antimalarial activity of the anticancer and proteasome inhibitor bortezomib and its analog ZL3B. BMC Clin Pharmacol. 2007;7:13. doi:10.1186/1472-6904-7-1317956613
  • DogovskiC, XieSC, BurgioG, et al. Targeting the cell stress response of Plasmodium falciparum to overcome artemisinin resistance. PLoS Biol. 2015;13(4):e1002132. doi:10.1371/journal.pbio.100213225901609
  • GonzalezJ, BaiGX, FrevertU, CoreyEJ, EichingerD. Proteasome-dependent cyst formation and stage-specific ubiquitin mRNA accumulation in Entamoeba invadens. Eur J Biochem. 1999;264(3):897–904. doi:10.1046/j.1432-1327.1999.00682.x10491138
  • LuthMR, GuptaP, OttilieS, WinzelerEA. Using in vitro evolution and whole genome analysis to discover next generation targets for antimalarial drug discovery. ACS Infect Dis. 2018;4(3):301–314. doi:10.1021/acsinfecdis.7b0027629451780
  • KrishnanKM, WilliamsonKC. The proteasome as a target to combat malaria: hits and misses. Transl Res. 2018;198:40–47. doi:10.1016/j.trsl.2018.04.00730009761
  • BlascoB, LeroyD, FidockDA. Antimalarial drug resistance: linking Plasmodium falciparum parasite biology to the clinic. Nat Med. 2017;23(8):917–928.28777791
  • KreidenweissA, KremsnerPG, MordmullerB. Comprehensive study of proteasome inhibitors against Plasmodium falciparum laboratory strains and field isolates from Gabon. Malar J. 2008;7:187. doi:10.1186/1475-2875-7-18718816382
  • PrasadR, Atul KollaVK, et al. Blocking Plasmodium falciparum development via dual inhibition of hemoglobin degradation and the ubiquitin proteasome system by MG132. PLoS One. 2013;8(9):e73530–e73530.24023882
  • SinnisP, PrasadR, Atul, et al. Blocking plasmodium falciparum development via dual inhibition of hemoglobin degradation and the ubiquitin proteasome system by MG132. PLoS One. 2013;8(9):e73530.24023882
  • LiH, TsuC, BlackburnC, et al. Identification of potent and selective non-covalent inhibitors of the Plasmodium falciparum proteasome. J Am Chem Soc. 2014;136(39):13562–13565. doi:10.1021/ja507692y25226494
  • GanttSM, MyungJM, BrionesMR, et al. Proteasome inhibitors block development of Plasmodium spp. Antimicrob Agents Chemother. 1998;42(10):2731–2738. doi:10.1128/AAC.42.10.27319756786
  • CzesnyB, GoshuS, CookJL, WilliamsonKC. The proteasome inhibitor epoxomicin has potent Plasmodium falciparum gametocytocidal activity. Antimicrob Agents Chemother. 2009;53(10):4080–4085. doi:10.1128/AAC.00088-0919651911
  • PrudhommeJ, McDanielE, PontsN, et al. Marine actinomycetes: a new source of compounds against the human malaria parasite. PLoS One. 2008;3(6):e2335. doi:10.1371/journal.pone.000233518523554
  • LiH, O’DonoghueAJ, van der LindenWA, et al. Structure- and function-based design of Plasmodium-selective proteasome inhibitors. Nature. 2016;530(7589):233–236. doi:10.1038/nature1693626863983
  • ZhanW, VisoneJ, OuelletteT, et al. Improvement of asparagine ethylenediamines as anti-malarial plasmodium-selective proteasome inhibitors. J Med Chem. 2019;62(13):6137–6145.31177777
  • Bibo-VerdugoB, WangSC, AlmalitiJ, et al. The proteasome as a drug target in the metazoan pathogen, schistosoma mansoni. ACS Infect Dis. 2019;5(10):1802–1812. doi:10.1021/acsinfecdis.9b0023731355632
  • LaMonteGM, AlmalitiJ, Bibo-VerdugoB, et al. Development of a potent inhibitor of the plasmodium proteasome with reduced mammalian toxicity. J Med Chem. 2017;60(15):6721–6732. doi:10.1021/acs.jmedchem.7b0067128696697
  • WyllieS, BrandS, ThomasM, et al. Preclinical candidate for the treatment of visceral leishmaniasis that acts through proteasome inhibition. Proc Natl Acad Sci U S A. 2019;116(19):9318–9323. doi:10.1073/pnas.182017511630962368
  • SaxenaAK, SinghA. Mycobacterial tuberculosis enzyme targets and their inhibitors. Curr Top Med Chem. 2019;19(5):337–355. doi:10.2174/156802661966619021910572230806318
  • OrganizationWH. Global Tuberculosis Report. 2018.
  • LinG, HuG, TsuC, et al. Mycobacterium tuberculosis prcBA genes encode a gated proteasome with broad oligopeptide specificity. Mol Microbiol. 2006;59(5):1405–1416. doi:10.1111/j.1365-2958.2005.05035.x16468985
  • HuG, LinG, WangM, et al. Structure of the Mycobacterium tuberculosis proteasome and mechanism of inhibition by a peptidyl boronate. Mol Microbiol. 2006;59(5):1417–1428. doi:10.1111/j.1365-2958.2005.05036.x16468986
  • DarwinKH, LinG, ChenZ, LiH, NathanCF. Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue. Mol Microbiol. 2005;55(2):561–571. doi:10.1111/j.1365-2958.2004.04403.x15659170
  • DarwinKH, EhrtS, Gutierrez-RamosJC, WeichN, NathanCF. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science. 2003;302(5652):1963–1966. doi:10.1126/science.109117614671303
  • LinG, TsuC, DickL, ZhouXK, NathanC. Distinct specificities of Mycobacterium tuberculosis and mammalian proteasomes for N-acetyl tripeptide substrates. J Biol Chem. 2008;283(49):34423–34431. doi:10.1074/jbc.M80532420018829465
  • WH Organization. Global Tuberculosis Report. 2015.
  • KoulA, ArnoultE, LounisN, GuillemontJ, AndriesK. The challenge of new drug discovery for tuberculosis. Nature. 2011;469(7331):483–490.21270886
  • Mc CormackT, BaumeisterW, GrenierL, et al. Active site-directed inhibitors of Rhodococcus 20 S proteasome. Kinetics and mechanism. J Biol Chem. 1997;272(42):26103–26109. doi:10.1074/jbc.272.42.261039334174
  • LinG, LiD, de CarvalhoLP, et al. Inhibitors selective for mycobacterial versus human proteasomes. Nature. 2009;461(7264):621–626.19759536
  • TotaroKA, BarthelmeD, SimpsonPT, et al. Rational design of selective and bioactive inhibitors of the mycobacterium tuberculosis proteasome. ACS Infect Dis. 2017;3(2):176–181. doi:10.1021/acsinfecdis.6b0017228183185
  • RussoF, GisingJ, ÅkerbladhL, et al. Optimization and evaluation of 5-styryl-oxathiazol-2-one mycobacterium tuberculosis proteasome inhibitors as potential antitubercular agents. ChemistryOpen. 2015;4(3):342–362. doi:10.1002/open.20150000126246997
  • TotaroK, BarthelmeD, SimpsonP, et al. Rational design of selective and bioactive inhibitors of the mycobacterium tuberculosis proteasome. ACS Infect Dis. 2016;3.27622944
  • LinG, ChidawanyikaT, TsuC, et al. N,C-Capped dipeptides with selectivity for mycobacterial proteasome over human proteasomes: role of S3 and S1 binding pockets. J Am Chem Soc. 2013;135(27):9968–9971. doi:10.1021/ja400021x23782398
  • HsuHC, SinghPK, FanH, et al. Structural basis for the species-selective binding of N,C-capped dipeptides to the mycobacterium tuberculosis proteasome. Biochemistry. 2017;56(1):324–333. doi:10.1021/acs.biochem.6b0110727976853
  • ZhanW, HsuHC, MorganT, et al. Selective phenylimidazole-based inhibitors of the mycobacterium tuberculosis proteasome. J Med Chem. 2019;62(20):9246–9253. doi:10.1021/acs.jmedchem.9b0118731560200
  • ParryDM. Closing the loop: developing an integrated design, make, and test platform for discovery. ACS Med Chem Lett. 2019;10(6):848–856. doi:10.1021/acsmedchemlett.9b0009531223437
  • PantSM, MukonoweshuroA, DesaiB, et al. Design, synthesis, and testing of potent, selective hepsin inhibitors via application of an automated closed-loop optimization platform. J Med Chem. 2018;61(10):4335–4347. doi:10.1021/acs.jmedchem.7b0169829701962
  • RamjeeMK, PatelS. Continuous-flow injection microfluidic thrombin assays: the effect of binding kinetics on observed enzyme inhibition. Anal Biochem. 2017;528:38–46. doi:10.1016/j.ab.2017.04.01628456636
  • DesaiB, DixonK, FarrantE, et al. Rapid discovery of a novel series of Abl kinase inhibitors by application of an integrated microfluidic synthesis and screening platform. J Med Chem. 2013;56(7):3033–3047. doi:10.1021/jm400099d23441572
  • CzechtizkyW, DedioJ, DesaiB, et al. Integrated synthesis and testing of substituted xanthine based dpp4 inhibitors: application to drug discovery. ACS Med Chem Lett. 2013;4(8):768–772. doi:10.1021/ml400171b24900744
  • OgorevcE, SchiffrerES, SosicI, GobecS. A patent review of immunoproteasome inhibitors. Expert Opin Ther Pat. 2018;28(7):517–540. doi:10.1080/13543776.2018.148490429865878
  • EskandariSK, SeelenMAJ, LinG, AzziJR. The immunoproteasome: an old player with a novel and emerging role in alloimmunity. 2017;17(12):3033–3039.
  • EttariR, ZappalaM, GrassoS, MusolinoC, InnaoV, AllegraA. Immunoproteasome-selective and non-selective inhibitors: a promising approach for the treatment of multiple myeloma. Pharmacol Ther. 2018;182:176–192. doi:10.1016/j.pharmthera.2017.09.00128911826
  • IchikawaHT, ConleyT, MuchamuelT, et al. Beneficial effect of novel proteasome inhibitors in murine lupus via dual inhibition of type I interferon and autoantibody-secreting cells. 64(2):493–503.
  • LiuRT, ZhangP, YangCL, et al. ONX-0914, a selective inhibitor of immunoproteasome, ameliorates experimental autoimmune myasthenia gravis by modulating humoral response. J Neuroimmunol. 2017;311:71–78. doi:10.1016/j.jneuroim.2017.08.00528844501
  • JohnsonHWB, LoweE, AnderlJL, et al. Required Immunoproteasome Subunit Inhibition Profile for Anti-Inflammatory Efficacy and Clinical Candidate KZR-616 ((2 S,3 R)- N-((S)-3-(Cyclopent-1-en-1-yl)-1-((R)-2-methyloxiran-2-yl)-1-oxopropan-2-yl)-3-hydroxy-3-(4-methoxyphenyl)-2-((S)-2-(2-morpholinoacetamido)propanamido)propenamide). J Med Chem. 2018;61(24):11127–11143.30380863
  • KevinSP, McNaughtCWO, BarryH, IsacsonO, JennerP. Failure of the ubiquitin–proteasomesystem in Parkinson’s disease. NAT REV. 2001;2:589–593. doi:10.1038/35086067
  • DasS, RamakrishnaS, KimKS. Critical Roles Of Deubiquitinating Enzymes In The Nervous System And Neurodegenerative Disorders. Mol Cells. 2020;43(3):203–214.32133826
  • GadhaveK, KumarP, KapugantiS, UverskyV, GiriR. Unstructured biology of proteins from ubiquitin-proteasome system: roles in cancer and neurodegenerative diseases. Biomolecules. 2020;10:796. doi:10.3390/biom10050796
  • LeeB-H, LeeMJ, ParkS, et al. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature. 2010;467(7312):179–184. doi:10.1038/nature0929920829789
  • NagDK, FinleyD. A small-molecule inhibitor of deubiquitinating enzyme USP14 inhibits Dengue virus replication. Virus Res. 2012;165(1):103–106. doi:10.1016/j.virusres.2012.01.00922306365
  • ZhouH, ShaoM, GuoB, et al. Tetramethylpyrazine analogue T-006 promotes the clearance of alpha-synuclein by enhancing proteasome activity in parkinson’s disease models. Neurotherapeutics. 2019;16(4):1225–1236.31313223
  • ChenHY, XuDP, TanGL, et al. A potent multi-functional neuroprotective derivative of tetramethylpyrazine. J Mol Neurosci. 2015;56(4):977–987. doi:10.1007/s12031-015-0566-x25982925
  • VeggianiG, GerpeMCR, SidhuSS, ZhangW. Emerging drug development technologies targeting ubiquitination for cancer therapeutics. Pharmacol Ther. 2019;199:139–154.30851297
  • FonovićM, BogyoM. Activity based probes as a tool for functional proteomic analysis of proteases. Expert Rev Proteomics. 2008;5:721–730. doi:10.1586/14789450.5.5.72118937562
  • BeksacG. The safety of bortezomib for the treatment of multiple myeloma. Expert Opin Drug Saf. 2018;17:953–962. doi:10.1080/14740338.2018.151348730118610
  • WertzIE, WangX. From discovery to bedside: targeting the ubiquitin system. Cell Chem Biol. 2019;26(2):156–177. doi:10.1016/j.chembiol.2018.10.02230554913
  • ThibaudeauTA, SmithDM, PracticalA. Review of proteasome pharmacology. Pharmacol Rev. 2019;71(2):170–197. doi:10.1124/pr.117.01537030867233
  • DemoSD, KirkCJ, AujayMA, et al. Antitumor activity of PR-171, a novel irreversible inhibitor of the proteasome. Cancer Res. 2007;67(13):6383–6391. doi:10.1158/0008-5472.CAN-06-408617616698
  • Correction: evaluation of the Proteasome Inhibitor MLN9708 in Preclinical Models of Human Cancer. Cancer Res. 2010;70(9):3852–3853.
  • RothP JR, GorliaT, DhermainF, et al. A phase III trial of marizomib in combination with standard temozolomide-based radiochemotherapy versus standard temozolomid-based radiochemotherapy alone in patients with newly diagnosed glioblastoma. Neuro-Oncology. 2019;21:iii98. doi:10.1093/neuonc/noz126.359
  • ZhuH, WangT, XinZ, et al. An oral second-generation proteasome inhibitor oprozomib significantly inhibits lung cancer in a p53 independent manner in vitro. Acta Biochim Biophys Sin (Shanghai). 2019;51(10):1034–1040. doi:10.1093/abbs/gmz09331518420
  • IsonoM, SatoA, AsanoT, OkuboK, AsanoT. Delanzomib Interacts with Ritonavir Synergistically to Cause Endoplasmic Reticulum Stress in Renal Cancer Cells. Anticancer Res. 2018;38(6):3493–3500. doi:10.21873/anticanres.1262029848702
  • TrivediHL, TerasakiPI, FerozA, et al. Abrogation of anti-HLA antibodies via proteasome inhibition. Transplantation. 2009;87(10):1555–1561. doi:10.1097/TP.0b013e3181a4b91b19461494
  • WilliamsAJ, DaveJR, TortellaFC. Neuroprotection with the proteasome inhibitor MLN519 in focal ischemic brain injury: relation to nuclear factor kappaB (NF-kappaB), inflammatory gene expression, and leukocyte infiltration. Neurochem Int. 2006;49(2):106–112. doi:10.1016/j.neuint.2006.03.01816759750
  • ShuklaSK, RafiqK. Proteasome biology and therapeutics in cardiac diseases. Transl Res. 2019;205:64–76. doi:10.1016/j.trsl.2018.09.00330342797
  • WangS, LiuH, ZuX, et al. The ubiquitin-proteasome system is essential for the productive entry of Japanese encephalitis virus. Virology. 2016;498:116–127. doi:10.1016/j.virol.2016.08.01327567260
  • VriendJ, ReiterRJ. Melatonin, bone regulation and the ubiquitin-proteasome connection: A review. Life Sci. 2016;145:152–160. doi:10.1016/j.lfs.2015.12.03126706287
  • HusebyNE, RavuriC, MoensU. The proteasome inhibitor lactacystin enhances GSH synthesis capacity by increased expression of antioxidant components in an Nrf2-independent, but p38 MAPK-dependent manner in rat colorectal carcinoma cells. Free Radic Res. 2016;50(1):1–13. doi:10.3109/10715762.2015.110073026530909