Pathophysiological processes in multiple sclerosis: focus on nuclear factor erythroid-2-related factor 2 and emerging pathways

References

• LucchinettiCBruckWParisiJScheithauerBRodriguezMLassmannHHeterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelinationAnn Neurol200047670771710852536
   PubMed Web of Science ®Google Scholar
• BjartmarCTrappBDAxonal degeneration and progressive neurologic disability in multiple sclerosisNeurotox Res200351–215716412832230
   PubMed Web of Science ®Google Scholar
• KuhlmannTLingfeldGBitschASchuchardtJBruckWAcute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over timeBrain2002125Pt 102202221212244078
   PubMed Web of Science ®Google Scholar
• FergusonBMatyszakMKEsiriMMPerryVHAxonal damage in acute multiple sclerosis lesionsBrain1997120Pt 33933999126051
   PubMed Web of Science ®Google Scholar
• SimonJMagnetic resonance imaging in the diagnosis of multiple sclerosis, elucidation of disease, course, and determining prognosisBurksJSJohnsonKPMultiple Sclerosis: Diagnosis, Medical Management, and RehabilitationNew YorkDemos Medical Publishing200099126
   Google Scholar
• BarnettMHPrineasJWRelapsing and remitting multiple sclerosis: pathology of the newly forming lesionAnn Neurol200455445846815048884
   PubMed Web of Science ®Google Scholar
• GonsetteRENeurodegeneration in multiple sclerosis: the role of oxidative stress and excitotoxicityJ Neurol Sci20082741–2485318684473
   PubMed Web of Science ®Google Scholar
• DevasagayamTPTilakJCBoloorKKSaneKSGhaskadbiSSLeleRDFree radicals and antioxidants in human health: current status and future prospectsJ Assoc Physicians India20045279480415909857
   PubMedGoogle Scholar
• MaQTranscriptional responses to oxidative stress: pathological and toxicological implicationsPharmacol Ther2010125337639319945483
   PubMed Web of Science ®Google Scholar
• FinkelTSignal transduction by mitochondrial oxidantsJ Biol Chem201228774434444021832045
   PubMed Web of Science ®Google Scholar
• BoverisADetermination of the production of superoxide radicals and hydrogen peroxide in mitochondriaMethods Enzymol19841054294356328196
   PubMed Web of Science ®Google Scholar
• ChanceBSiesHBoverisAHydroperoxide metabolism in mammalian organsPhysiol Rev197959352760537532
   PubMed Web of Science ®Google Scholar
• HansfordRGHogueBAMildazieneVDependence of H2O2 formation by rat heart mitochondria on substrate availability and donor ageJ Bioenerg Biomembr199729189959067806
   PubMed Web of Science ®Google Scholar
• TurrensJFBoverisAGeneration of superoxide anion by the NADH dehydrogenase of bovine heart mitochondriaBiochem J198019124214276263247
   PubMed Web of Science ®Google Scholar
• ShigenagaMKHagenTMAmesBNOxidative damage and mitochondrial decay in agingProc Natl Acad Sci U S A1994912310771107787971961
   PubMed Web of Science ®Google Scholar
• CadenasEDaviesKJMitochondrial free radical generation, oxidative stress, and agingFree Radic Biol Med2000293–422223011035250
   PubMed Web of Science ®Google Scholar
• BoverisACadenasEMitochondrial production of hydrogen peroxide regulation by nitric oxide and the role of ubisemiquinoneIUBMB Life2000504–524525011327317
   PubMed Web of Science ®Google Scholar
• MaQRole of Nrf2 in oxidative stress and toxicityAnnu Rev Pharmacol Toxicol20135340142623294312
   PubMed Web of Science ®Google Scholar
• BedardKKrauseKHThe NOX family of ROS-generating NADPH oxidases: physiology and pathophysiologyPhysiol Rev200787124531317237347
   PubMed Web of Science ®Google Scholar
• LoveSOxidative stress in brain ischemiaBrain Pathol1999911191319989455
   PubMed Web of Science ®Google Scholar
• LuSCRegulation of glutathione synthesisCurr Top Cell Regul2000369511610842748
   PubMedGoogle Scholar
• BiewengaGPHaenenGRBastAThe pharmacology of the antioxidant lipoic acidGen Pharmacol19972933153319378235
   PubMedGoogle Scholar
• PackerLWittEHTritschlerHJalpha-Lipoic acid as a biological antioxidantFree Radic Biol Med19951922272507649494
   PubMed Web of Science ®Google Scholar
• van HorssenJWitteMESchreibeltGde VriesHERadical changes in multiple sclerosis pathogenesisBiochim Biophys Acta20111812214115020600869
   PubMed Web of Science ®Google Scholar
• HendriksJJAlblasJvan der PolSMvan TolEADijkstraCDde VriesHEFlavonoids influence monocytic GTPase activity and are protective in experimental allergic encephalitisJ Exp Med2004200121667167215611292
   PubMed Web of Science ®Google Scholar
• SmithKJKapoorRFeltsPADemyelination: the role of reactive oxygen and nitrogen speciesBrain Pathol19999169929989453
   PubMed Web of Science ®Google Scholar
• van MeeterenMEHendriksJJDijkstraCDvan TolEADietary compounds prevent oxidative damage and nitric oxide production by cells involved in demyelinating diseaseBiochem Pharmacol200467596797515104250
   PubMed Web of Science ®Google Scholar
• Aboul-EneinFRauschkaHKornekBPreferential loss of myelin-associated glycoprotein reflects hypoxia-like white matter damage in stroke and inflammatory brain diseasesJ Neuropathol Exp Neurol2003621253312528815
   PubMed Web of Science ®Google Scholar
• HaiderLFischerMTFrischerJMOxidative damage in multiple sclerosis lesionsBrain2011134Pt 71914192421653539
   PubMed Web of Science ®Google Scholar
• NaidooRKnappMLStudies of lipid peroxidation products in cerebrospinal fluid and serum in multiple sclerosis and other conditionsClin Chem19923812244924541458583
   PubMed Web of Science ®Google Scholar
• van HorssenJSchreibeltGDrexhageJSevere oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expressionFree Radic Biol Med200845121729173718930811
   PubMed Web of Science ®Google Scholar
• GrayEThomasTLBetmouniSScoldingNLoveSElevated myeloperoxidase activity in white matter in multiple sclerosisNeurosci Lett2008444219519818723077
   PubMed Web of Science ®Google Scholar
• GrayEThomasTLBetmouniSScoldingNLoveSElevated activity and microglial expression of myeloperoxidase in demyelinated cerebral cortex in multiple sclerosisBrain Pathol2008181869518042261
   PubMed Web of Science ®Google Scholar
• MarikCFeltsPABauerJLassmannHSmithKJLesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity?Brain2007130Pt 112800281517956913
   PubMed Web of Science ®Google Scholar
• CrossAHManningPTKeelingRMSchmidtREMiskoTPPeroxynitrite formation within the central nervous system in active multiple sclerosisJ Neuroimmunol1998881–245569688323
   PubMed Web of Science ®Google Scholar
• LiuJSZhaoMLBrosnanCFLeeSCExpression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesionsAm J Pathol200115862057206611395383
   PubMed Web of Science ®Google Scholar
• SmithKJLassmannHThe role of nitric oxide in multiple sclerosisLancet Neurol20021423224112849456
   PubMed Web of Science ®Google Scholar
• VetoSAcsPBauerJInhibiting poly(ADP-ribose) polymerase: a potential therapy against oligodendrocyte deathBrain2010133Pt 382283420157013
   PubMed Web of Science ®Google Scholar
• WitteMEBoLRodenburgRJEnhanced number and activity of mitochondria in multiple sclerosis lesionsJ Pathol2009219219320419591199
   PubMed Web of Science ®Google Scholar
• DuttaRMcDonoughJYinXMitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patientsAnn Neurol200659347848916392116
   PubMed Web of Science ®Google Scholar
• DuttaRTrappBDMechanisms of neuronal dysfunction and degeneration in multiple sclerosisProg Neurobiol201193111220946934
   PubMed Web of Science ®Google Scholar
• MahadDZiabrevaILassmannHTurnbullDMitochondrial defects in acute multiple sclerosis lesionsBrain2008131Pt 71722173518515320
   PubMed Web of Science ®Google Scholar
• ZamboninJLZhaoCOhnoNIncreased mitochondrial content in remyelinated axons: implications for multiple sclerosisBrain2011134Pt 71901191321705418
   PubMed Web of Science ®Google Scholar
• MahadDJZiabrevaICampbellGMitochondrial changes within axons in multiple sclerosisBrain2009132Pt 51161117419293237
   PubMed Web of Science ®Google Scholar
• NikicIMerklerDSorbaraCA reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosisNat Med201117449549921441916
   PubMed Web of Science ®Google Scholar
• VolterraATrottiDTrombaCFloridiSRacagniGGlutamate uptake inhibition by oxygen free radicals in rat cortical astrocytesJ Neurosci1994145 Pt 1292429327910203
   PubMed Web of Science ®Google Scholar
• MatuteCSanchez-GomezMVMartinez-MillanLMilediRGlutamate receptor-mediated toxicity in optic nerve oligodendrocytesProc Natl Acad Sci U S A19979416883088359238063
   PubMed Web of Science ®Google Scholar
• MatuteCCharacteristics of acute and chronic kainate excitotoxic damage to the optic nerveProc Natl Acad Sci U S A1998951710229102349707629
   PubMed Web of Science ®Google Scholar
• McDonaldJWAlthomsonsSPHyrcKLChoiDWGoldbergMPOligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicityNat Med1998432912979500601
   PubMed Web of Science ®Google Scholar
• NoseworthyJHLucchinettiCRodriguezMWeinshenkerBGMultiple sclerosisN Engl J Med20003431393895211006371
   PubMed Web of Science ®Google Scholar
• CuiWBaiYLuoPMiaoLCaiLPreventive and therapeutic effects of MG132 by activating Nrf2-ARE signaling pathway on oxidative stress-induced cardiovascular and renal injuryOxid Med Cell Longev2013201330607323533688
   PubMed Web of Science ®Google Scholar
• HayesJDMcMahonMNRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancerTrends Biochem Sci200934417618819321346
   PubMed Web of Science ®Google Scholar
• AlamJKilleenEGongPHeme activates the heme oxygenase-1 gene in renal epithelial cells by stabilizing Nrf2Am J Physiol Renal Physiol20032844F743F75212453873
   PubMed Web of Science ®Google Scholar
• StewartDKilleenENaquinRAlamSAlamJDegradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmiumJ Biol Chem200327842396240212441344
   PubMed Web of Science ®Google Scholar
• Dinkova-KostovaATHoltzclawWDColeRNDirect evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidantsProc Natl Acad Sci U S A20029918119081191312193649
   PubMed Web of Science ®Google Scholar
• ItohKWakabayashiNKatohYKeap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domainGenes Dev199913176869887101
   PubMed Web of Science ®Google Scholar
• ItohKWakabayashiNKatohYIshiiTO’ConnorTYamamotoMKeap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophilesGenes Cells20038437939112653965
   PubMed Web of Science ®Google Scholar
• HirotsuYKatsuokaFFunayamaRNrf2-MafG heterodimers contribute globally to antioxidant and metabolic networksNucleic Acids Res20124020102281023922965115
   PubMed Web of Science ®Google Scholar
• LeeJMLiJJohnsonDANrf2, a multi-organ protector?FASEB J20051991061106615985529
   PubMed Web of Science ®Google Scholar
• TrappBDStysPKVirtual hypoxia and chronic necrosis of demyelinated axons in multiple sclerosisLancet Neurol20098328029119233038
   PubMed Web of Science ®Google Scholar
• FilippiniGBrusaferriFSibleyWACorticosteroids or ACTH for acute exacerbations in multiple sclerosisCochrane Database Syst Rev20004CD00133111034713
   PubMedGoogle Scholar
• WeinerHLDauPCKhatriBODouble-blind study of true vs sham plasma exchange in patients treated with immunosuppression for acute attacks of multiple sclerosisNeurology1989399114311492549450
   PubMed Web of Science ®Google Scholar
• WeinshenkerBGO’BrienPCPettersonTMA randomized trial of plasma exchange in acute central nervous system inflammatory demyelinating diseaseAnn Neurol199946687888610589540
   PubMed Web of Science ®Google Scholar
• KieseierBCThe mechanism of action of interferon-beta in relapsing multiple sclerosisCNS Drugs201125649150221649449
   PubMed Web of Science ®Google Scholar
• JohnsonKPBrooksBRCohenJACopolymer 1 reduces relapse rate and improves disability in relapsing-remitting multiple sclerosis: results of a phase III multicenter, double-blind placebo-controlled trial. The Copolymer 1 Multiple Sclerosis Study GroupNeurology1995457126812767617181
   PubMed Web of Science ®Google Scholar
• ChenPCVargasMRPaniAKNrf2-mediated neuroprotection in the MPTP mouse model of Parkinson’s disease: critical role for the astrocyteProc Natl Acad Sci U S A200910682933293819196989
   PubMed Web of Science ®Google Scholar
• EllrichmannGPetrasch-ParwezELeeDHEfficacy of fumaric acid esters in the R6/2 and YAC128 models of Huntington’s diseasePloS One201161e1617221297955
   PubMed Web of Science ®Google Scholar
• KapposLGoldRMillerDHEffect of BG-12 on contrast-enhanced lesions in patients with relapsing – remitting multiple sclerosis: subgroup analyses from the phase 2b studyMult Scler201218331432121878455
   PubMed Web of Science ®Google Scholar
• KapposLGoldRMillerDHEfficacy and safety of oral fumarate in patients with relapsing-remitting multiple sclerosis: a multicentre, randomised, double-blind, placebo-controlled phase IIb studyLancet200837296481463147218970976
   PubMed Web of Science ®Google Scholar
• BittnerSMeuthSGGobelKTASK1 modulates inflammation and neurodegeneration in autoimmune inflammation of the central nervous systemBrain2009132Pt 92501251619570851
   PubMed Web of Science ®Google Scholar
• KhodagholiFEftekharzadehBMaghsoudiNRezaeiPFChitosan prevents oxidative stress-induced amyloid beta formation and cytotoxicity in NT2 neurons: involvement of transcription factors Nrf2 and NF-kappaBMol Cell Biochem20103371–2395119844776
   PubMed Web of Science ®Google Scholar
• LewerenzJAlbrechtPTienMLInduction of Nrf2 and xCT are involved in the action of the neuroprotective antibiotic ceftriaxone in vitroJ Neurochem2009111233234319694903
   PubMed Web of Science ®Google Scholar
• RachakondaGXiongYSekharKRStamerSLLieblerDCFreemanMLCovalent modification at Cys151 dissociates the electrophile sensor Keap1 from the ubiquitin ligase CUL3Chem Res Toxicol200821370571018251510
   PubMed Web of Science ®Google Scholar
• ThiessenASchmidtMMDringenRFumaric acid dialkyl esters deprive cultured rat oligodendroglial cells of glutathione and upregulate the expression of heme oxygenase 1Neurosci Lett20104751566020347008
   PubMed Web of Science ®Google Scholar
• KavanaghGMBurtonJLDonnellVOEffects of dithranol on neutrophil superoxide generation in patients with psoriasisBr J Dermatol199613422342378746335
   PubMed Web of Science ®Google Scholar
• LitjensNHBurggraafJvan StrijenEPharmacokinetics of oral fumarates in healthy subjectsBr J of Clin Pharmacol200458442943215373936
   PubMed Web of Science ®Google Scholar
• FoxRJMillerDHPhillipsJTPlacebo-controlled phase 3 study of oral BG-12 or glatiramer in multiple sclerosisN Engl J Med2012367121087109722992072
   PubMed Web of Science ®Google Scholar
• GoldRKapposLArnoldDLPlacebo-controlled phase 3 study of oral BG-12 for relapsing multiple sclerosisN Engl J Med2012367121098110722992073
   PubMed Web of Science ®Google Scholar
• ScannevinRHChollateSJungMYFumarates promote cytoprotection of central nervous system cells against oxidative stress via the nuclear factor (erythroid-derived 2)-like 2 pathwayJ Pharmacol Exp Ther2012341127428422267202
   PubMed Web of Science ®Google Scholar
• LeeDHGoldRLinkerRAMechanisms of oxidative damage in multiple sclerosis and neurodegenerative diseases: therapeutic modulation via fumaric acid estersInt J Mol Sci2012139117831180323109883
   PubMed Web of Science ®Google Scholar
• SchmidtMMDringenRFumaric acid diesters deprive cultured primary astrocytes rapidly of glutathioneNeurochem Int201057446046720096739
   PubMed Web of Science ®Google Scholar
• ChauhanDCatleyLLiGA novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from BortezomibCancer Cell20058540741916286248
   PubMed Web of Science ®Google Scholar
• FelingRHBuchananGOMincerTJKauffmanCAJensenPRFenicalWSalinosporamide A: a highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus salinosporaAngew Chem Int Ed Engl200342335535712548698
   PubMed Web of Science ®Google Scholar
• PottsBCAlbitarMXAndersonKCMarizomib, a proteasome inhibitor for all seasons: preclinical profile and a framework for clinical trialsCurr Cancer Drug Targets201111325428421247382
   PubMed Web of Science ®Google Scholar
• MengLMohanRKwokBHElofssonMSinNCrewsCMEpoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activityProc Natl Acad Sci U S A19999618104031040810468620
   PubMed Web of Science ®Google Scholar