Basic Leucine Zipper Protein Nuclear Factor Erythroid 2–related Factor 2 as a Potential Therapeutic Target in Brain Related Disorders

Page: [676 - 691] Pages: 16

  • * (Excluding Mailing and Handling)

Abstract

Nuclear factor erythroid-2-related factor 2 (Nrf2), an inducible transcription factor in phase II metabolic reactions, as well as xenobiotic response pathway, is referred to as ‘master regulator’ in anti-oxidant, anti-inflammatory, and xenobiotic detoxification processes. The activity of Nrf2 is tightly regulated by KEAP1, which promotes ubiquitination, followed by degradation under homeostatic conditions and also allows Nrf2 to escape ubiquitination, accumulate within the cell, and translocate in the nucleus upon exposure to the stresses. The Nrf2 pathway has shown an intrinsic mechanism of defense against oxidative stress (OS). It emerged as a promising therapeutic target as both inducers and as there is an increasing number of evidence for the protective role of the Nrf2-ARE pathway towards exacerbations of ROS generation as well as OS, mitochondrial dysfunction as well as prolonged neuroinflammation is a prevalent pathophysiological process rooted in brain-related disorders. Elevated concentrations of ROS generation and OS have been linked to the pathophysiology of a diverse array of brain related disorders, including Alzheimer’s disease, Parkinson’s disease, Huntington’s disease, Friedrich’s ataxia, multiple sclerosis, and epilepsy. Further, it not only modulates the articulation of anti-oxidant genes but has often been associated with implicating anti-inflammatory consequences as well as regulating mitochondrial functionalities and biogenesis. Therefore, Nrf2 can be considered a potential therapeutic target for the regimen of various brain-related disorders.

Keywords: Nrf2, oxidative stress, neuroinflammation, ROS, neurodegenerative disease, mitochondrial dysfunctions, biogenesis.

Graphical Abstract

[1]
Alfieri, A.; Srivastava, S.; Siow, R.C.M.; Modo, M.; Fraser, P.A.; Mann, G.E. Targeting the Nrf2-Keap1 antioxidant defence pathway for neurovascular protection in stroke. J. Physiol., 2011, 589(17), 4125-4136.
[http://dx.doi.org/10.1113/jphysiol.2011.210294] [PMID: 21646410]
[2]
Yamamoto, M.; Kensler, T.W.; Motohashi, H. The KEAP1-NRF2 system: A thiol-based sensor-effector apparatus for maintaining redox homeostasis. Physiol. Rev., 2018, 98(3), 1169-1203.
[http://dx.doi.org/10.1152/physrev.00023.2017] [PMID: 29717933]
[3]
Hayes, J.D.; Dinkova-Kostova, A.T. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem. Sci., 2014, 39(4), 199-218.
[http://dx.doi.org/10.1016/j.tibs.2014.02.002] [PMID: 24647116]
[4]
Cuadrado, A.; Rojo, A.I.; Wells, G.; Hayes, J.D.; Cousin, S.P.; Rumsey, W.L.; Attucks, O.C.; Franklin, S.; Levonen, A.L.; Kensler, T.W.; Dinkova-Kostova, A.T. Therapeutic targeting of the NRF2 and KEAP1 partnership in chronic diseases. Nat. Rev. Drug Discov., 2019, 18(4), 295-317.
[http://dx.doi.org/10.1038/s41573-018-0008-x] [PMID: 30610225]
[5]
Nguyen, T.; Nioi, P.; Pickett, C.B. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J. Biol. Chem., 2009, 284(20), 13291-13295.
[http://dx.doi.org/10.1074/jbc.R900010200] [PMID: 19182219]
[6]
Dinkova-Kostova, AT; Abramov, A.Y. The emerging role of Nrf2 in mitochondrial function. Free Radic. Biol. Med., 2015, 88(Pt B), 179-188.
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.04.036]
[7]
Holmström, K.M.; Kostov, R.V.; Dinkova-Kostova, A.T. The multifaceted role of Nrf2 in mitochondrial function. Curr. Opin. Toxicol., 2016, 1, 80-91.
[http://dx.doi.org/10.1016/j.cotox.2016.10.002] [PMID: 28066829]
[8]
Holmström, K.M.; Baird, L.; Zhang, Y.; Hargreaves, I.; Chalasani, A.; Land, J.M.; Stanyer, L.; Yamamoto, M.; Dinkova-Kostova, A.T.; Abramov, A.Y. Nrf2 impacts cellular bioenergetics by controlling substrate availability for mitochondrial respiration. Biol. Open, 2013, 2(8), 761-770.
[http://dx.doi.org/10.1242/bio.20134853] [PMID: 23951401]
[9]
Lo, S.C.; Hannink, M. PGAM5 tethers a ternary complex containing Keap1 and Nrf2 to mitochondria. Exp. Cell Res., 2008, 314(8), 1789-1803.
[http://dx.doi.org/10.1016/j.yexcr.2008.02.014] [PMID: 18387606]
[10]
Jain, A.; Lamark, T.; Sjøttem, E.; Bowitz Larsen, K.; Atesoh Awuh, J.; Øvervatn, A.; McMahon, M.; Hayes, J.D.; Johansen, T. p62/SQSTM1 is a target gene for transcription factor Nrf2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J. Biol. Chem., 2010, 285(29), 22576-22591.
[http://dx.doi.org/10.1074/jbc.M110.118976] [PMID: 20452972]
[11]
Komatsu, M.; Kurokawa, H.; Waguri, S.; Taguchi, K.; Kobayashi, A.; Ichimura, Y.; Sou, Y.S.; Ueno, I.; Sakamoto, A.; Tong, K.I.; Kim, M.; Nishito, Y.; Iemura, S.; Natsume, T.; Ueno, T.; Kominami, E.; Motohashi, H.; Tanaka, K.; Yamamoto, M. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol., 2010, 12(3), 213-223.
[http://dx.doi.org/10.1038/ncb2021] [PMID: 20173742]
[12]
Jain, A.; Rusten, T.E.; Katheder, N.; Elvenes, J.; Bruun, J.A.; Sjøttem, E.; Lamark, T.; Johansen, T. p62/Sequestosome-1, autophagy-related gene 8, and autophagy in drosophila are regulated by nuclear factor erythroid 2-related factor 2 (NRF2), independent of transcription factor TFEB. J. Biol. Chem., 2015, 290(24), 14945-14962.
[http://dx.doi.org/10.1074/jbc.M115.656116] [PMID: 25931115]
[13]
Piantadosi, C.A.; Carraway, M.S.; Babiker, A.; Suliman, H.B. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ. Res., 2008, 103(11), 1232-1240.
[http://dx.doi.org/10.1161/01.RES.0000338597.71702.ad] [PMID: 18845810]
[14]
Merry, T.L.; Ristow, M. Nuclear Factor Erythroid-derived 2-like 2 (NFE2L2, Nrf2) mediates exercise-induced mitochondrial biogenesis and the anti-oxidant response in mice. J. Physiol., 2016, 594(18), 5195-5207.
[http://dx.doi.org/10.1113/JP271957] [PMID: 27094017]
[15]
Navarro, E.; Gonzalez-Lafuente, L.; Pérez-Liébana, I.; Buendia, I.; López-Bernardo, E.; Sánchez-Ramos, C.; Prieto, I.; Cuadrado, A.; Satrustegui, J.; Cadenas, S.; Monsalve, M.; López, M.G. Heme-oxygenase I and PCG1alpha regulate mitochondrial biogenesis via microglial activation of alpha7 nicotinic acetylcholine receptors using PNU282987. Antioxid. Redox Signal., 2017, 27(2), 93-105.
[http://dx.doi.org/10.1089/ars.2016.6698] [PMID: 27554853]
[16]
East, D.A.; Fagiani, F.; Crosby, J.; Georgakopoulos, N.D.; Bertrand, H.; Schaap, M.; Fowkes, A.; Wells, G.; Campanella, M. PMI: A ΔΨm independent pharmacological regulator of mitophagy. Chem. Biol., 2014, 21(11), 1585-1596.
[http://dx.doi.org/10.1016/j.chembiol.2014.09.019] [PMID: 25455860]
[17]
Sandberg, M.; Patil, J.; D’Angelo, B.; Weber, S.G.; Mallard, C. NRF2-regulation in brain health and disease: Implication of cerebral inflammation. Neuropharmacology, 2014, 79, 298-306.
[http://dx.doi.org/10.1016/j.neuropharm.2013.11.004] [PMID: 24262633]
[18]
Buendia, I.; Michalska, P.; Navarro, E.; Gameiro, I.; Egea, J.; León, R. Nrf2–ARE pathway: An emerging target against oxidative stress and neuroinflammation in neurodegenerative diseases. Pharmacol. Ther., 2016, 157, 84-104.
[http://dx.doi.org/10.1016/j.pharmthera.2015.11.003] [PMID: 26617217]
[19]
Hayashi, G.; Jasoliya, M.; Sahdeo, S.; Saccà, F.; Pane, C.; Filla, A.; Marsili, A.; Puorro, G.; Lanzillo, R.; Brescia, M.V.; Cortopassi, G. Dimethyl fumarate mediates Nrf2-dependent mitochondrial biogenesis in mice and humans. Hum. Mol. Genet., 2017, 26(15), 2864-2873.
[http://dx.doi.org/10.1093/hmg/ddx167] [PMID: 28460056]
[20]
Sivandzade, F.; Prasad, S.; Bhalerao, A.; Cucullo, L. Nrf2 and NF-B interplay in cerebrovascular and neurodegenerative disorders: Molecular mechanisms and possible therapeutic approaches. Redox Biol., 2019, 21, 101059.
[http://dx.doi.org/10.1016/j.redox.2018.11.017] [PMID: 30576920]
[21]
Cho, H.Y.; Gladwell, W.; Wang, X.; Chorley, B.; Bell, D.; Reddy, S.P.; Kleeberger, S.R. Nrf2-regulated PPARgamma expression is critical to protection against acute lung injury in mice. Am. J. Respir. Crit. Care Med., 2010, 182(2), 170-182.
[http://dx.doi.org/10.1164/rccm.200907-1047OC] [PMID: 20224069]
[22]
Bellezza, I.; Tucci, A.; Galli, F.; Grottelli, S.; Mierla, A.L.; Pilolli, F.; Minelli, A. Inhibition of NF-κB nuclear translocation via HO-1 activation underlies α-tocopheryl succinate toxicity. J. Nutr. Biochem., 2012, 23(12), 1583-1591.
[http://dx.doi.org/10.1016/j.jnutbio.2011.10.012] [PMID: 22444871]
[23]
Lai, L.; Wang, M.; Martin, O.J.; Leone, T.C.; Vega, R.B.; Han, X.; Kelly, D.P. A role for peroxisome proliferator-activated receptor γ coactivator 1 (PGC-1) in the regulation of cardiac mitochondrial phospholipid biosynthesis. J. Biol. Chem., 2014, 289(4), 2250-2259.
[http://dx.doi.org/10.1074/jbc.M113.523654] [PMID: 24337569]
[24]
Ping, Z.; Zhang, L.; Cui, Y.; Chang, Y.; Jiang, C.; Meng, Z.; Xu, P.; Liu, H.; Wang, D.; Cao, X. The protective effects of salidroside from exhaustive exercise-induced heart injury by enhancing the PGC-1 alpha -NRF1/NRF2 pathway and mitochondrial respiratory function in rats. Oxid. Med. Cell. Longev., 2015, 2015, 1-9.
[http://dx.doi.org/10.1155/2015/876825] [PMID: 26167242]
[25]
Huang, K.; Gao, X.; Wei, W. The crosstalk between Sirt1 and Keap1/Nrf2/ARE anti-oxidative pathway forms a positive feedback loop to inhibit FN and TGF-β1 expressions in rat glomerular mesangial cells. Exp. Cell Res., 2017, 361(1), 63-72.
[http://dx.doi.org/10.1016/j.yexcr.2017.09.042] [PMID: 28986066]
[26]
Song, N.Y.; Lee, Y.H.; Na, H.K.; Baek, J.H.; Surh, Y.J. Leptin induces SIRT1 expression through activation of NF-E2-related factor 2: Implications for obesity-associated colon carcinogenesis. Biochem. Pharmacol., 2018, 153, 282-291.
[http://dx.doi.org/10.1016/j.bcp.2018.02.001] [PMID: 29427626]
[27]
Cai, W.; Yang, T.; Liu, H.; Han, L.; Zhang, K.; Hu, X.; Zhang, X.; Yin, K.J.; Gao, Y.; Bennett, M.V.L.; Leak, R.K.; Chen, J. Peroxisome Proliferator-Activated Receptor γ (PPARγ): A master gatekeeper in CNS injury and repair. Prog. Neurobiol., 2018, 163-164, 27-58.
[http://dx.doi.org/10.1016/j.pneurobio.2017.10.002] [PMID: 29032144]
[28]
Lee, C. Collaborative power of Nrf2 and PPARgamma activators against metabolic and drug-induced oxidative injury. Oxid. Med. Cell. Longev., 2017, 2017, 1-14.
[http://dx.doi.org/10.1155/2017/1378175] [PMID: 28928902]
[29]
Dinkova-Kostova, A.T.; Holtzclaw, W.D.; Cole, R.N.; Itoh, K.; Wakabayashi, N.; Katoh, Y.; Yamamoto, M.; Talalay, P. Direct evidence that sulfhydryl groups of KEAP1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc. Natl. Acad. Sci., 2002, 99(18), 11908-11913.
[http://dx.doi.org/10.1073/pnas.172398899] [PMID: 12193649]
[30]
Baird, L.; Llères, D.; Swift, S.; Dinkova-Kostova, A.T. Regulatory flexibility in the Nrf2-mediated stress response is conferred by conformational cycling of the KEAP1-Nrf2 protein complex. Proc. Natl. Acad. Sci., 2013, 110(38), 15259-15264.
[http://dx.doi.org/10.1073/pnas.1305687110] [PMID: 23986495]
[31]
Kobayashi, A.; Kang, M.I.; Watai, Y.; Tong, K.I.; Shibata, T.; Uchida, K.; Yamamoto, M. Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Mol. Cell. Biol., 2006, 26(1), 221-229.
[http://dx.doi.org/10.1128/MCB.26.1.221-229.2006] [PMID: 16354693]
[32]
Sykiotis, G.P.; Habeos, I.G.; Samuelson, A.V.; Bohmann, D. The role of the antioxidant and longevity-promoting Nrf2 pathway in metabolic regulation. Curr. Opin. Clin. Nutr. Metab. Care, 2011, 14(1), 41-48.
[http://dx.doi.org/10.1097/MCO.0b013e32834136f2] [PMID: 21102319]
[33]
Esteras, N.; Dinkova-Kostova, A.T.; Abramov, A.Y. Nrf2 activation in the treatment of neurodegenerative diseases: A focus on its role in mitochondrial bioenergetics and function. Biol. Chem., 2016, 397(5), 383-400.
[http://dx.doi.org/10.1515/hsz-2015-0295] [PMID: 26812787]
[34]
Johnson, D.A.; Johnson, J.A. Nrf2 a therapeutic target for the treatment of neurodegenerative diseases. Free Radic. Biol. Med., 2015, 88(Pt B), 253-267.
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.07.147] [PMID: 26281945]
[35]
Jarrott, B.; Williams, S.J. Chronic brain inflammation: The neurochemical basis for drugs to reduce inflammation. Neurochem. Res., 2016, 41(3), 523-533.
[http://dx.doi.org/10.1007/s11064-015-1661-7] [PMID: 26177578]
[36]
Hoenen, C.; Gustin, A.; Birck, C.; Kirchmeyer, M.; Beaume, N.; Felten, P.; Grandbarbe, L.; Heuschling, P.; Heurtaux, T. Alpha-synuclein proteins promote proinflammatory cascades in microglia: Stronger effects of the A53T mutant. PLoS One, 2016, 11(9), e0162717.
[http://dx.doi.org/10.1371/journal.pone.0162717] [PMID: 27622765]
[37]
Kumar, H.; Lim, H.W.; More, S.V.; Kim, B.W.; Koppula, S.; Kim, I.S.; Choi, D.K. The role of free radicals in the aging brain and Parkinson’s disease: Convergence and parallelism. Int. J. Mol. Sci., 2012, 13(8), 10478-10504.
[http://dx.doi.org/10.3390/ijms130810478] [PMID: 22949875]
[38]
Yamazaki, H.; Tanji, K.; Wakabayashi, K.; Matsuura, S.; Itoh, K. Role of the Keap1/Nrf2 pathway in neurodegenerative diseases. Pathol. Int., 2015, 65(5), 210-219.
[http://dx.doi.org/10.1111/pin.12261] [PMID: 25707882]
[39]
Goris, A.; Williams-Gray, C.H.; Clark, G.R.; Foltynie, T.; Lewis, S.J.G.; Brown, J.; Ban, M.; Spillantini, M.G.; Compston, A.; Burn, D.J.; Chinnery, P.F.; Barker, R.A.; Sawcer, S.J. Tau and α-synuclein in susceptibility to, and dementia in, Parkinson’s disease. Ann. Neurol., 2007, 62(2), 145-153.
[http://dx.doi.org/10.1002/ana.21192] [PMID: 17683088]
[40]
Tufekci, K.U.; Civi Bayin, E.; Genc, S.; Genc, K. The Nrf2/ARE pathway: A promising target to counteract mitochondrial dysfunction in Parkinson’s disease. Parkinsons Dis., 2011, 2011, 1-14.
[http://dx.doi.org/10.4061/2011/314082] [PMID: 21403858]
[41]
Bhat, S.; Acharya, U.R.; Hagiwara, Y.; Dadmehr, N.; Adeli, H. Parkinson’s disease: Cause factors, measurable indicators, and early diagnosis. Comput. Biol. Med., 2018, 102, 234-241.
[http://dx.doi.org/10.1016/j.compbiomed.2018.09.008] [PMID: 30253869]
[42]
Navarro, A.; Boveris, A. Brain mitochondrial dysfunction and oxidative damage in Parkinson’s disease. J. Bioenerg. Biomembr., 2009, 41(6), 517-521.
[http://dx.doi.org/10.1007/s10863-009-9250-6] [PMID: 19915964]
[43]
Di Filippo, M.; Chiasserini, D.; Tozzi, A.; Picconi, B.; Calabresi, P. Mitochondria and the link between neuroinflammation and neurodegeneration. J. Alzheimers Dis., 2010, 20(s2), S369-S379.
[http://dx.doi.org/10.3233/JAD-2010-100543] [PMID: 20463396]
[44]
Wei, Z.; Li, X.; Li, X.; Liu, Q.; Cheng, Y. Oxidative stress in Parkinson’s disease: A systematic review and metaanalysis. Front. Mol. Neurosci., 2018, 11, 236.
[http://dx.doi.org/10.3389/fnmol.2018.00236] [PMID: 30026688]
[45]
Dzamko, N.; Geczy, C.L.; Halliday, G.M. Inflammation is genetically implicated in Parkinson’s disease. Neuroscience, 2015, 302, 89-102.
[http://dx.doi.org/10.1016/j.neuroscience.2014.10.028] [PMID: 25450953]
[46]
Hirsch, E.C.; Vyas, S.; Hunot, S. Neuroinflammation in Parkinson’s disease. Parkinsonism Relat. Disord., 2012, 18(Suppl. 1), S210-S212.
[http://dx.doi.org/10.1016/S1353-8020(11)70065-7] [PMID: 22166438]
[47]
Aarsland, D.; Andersen, K.; Larsen, J.P.; Lolk, A.; Kragh-Sørensen, P. Prevalence and characteristics of dementia in Parkinson’s disease: An 8-year prospective study. Arch. Neurol., 2003, 60(3), 387-392.
[http://dx.doi.org/10.1001/archneur.60.3.387] [PMID: 12633150]
[48]
Fereshtehnejad, S.M.; Lökk, J. Active aging for individuals with Parkinson’s disease: Definitions, literature review, and models. Parkinsons Dis., 2014, 2014, 1-8.
[http://dx.doi.org/10.1155/2014/739718] [PMID: 25225618]
[49]
Ramsey, C.P.; Glass, C.A.; Montgomery, M.B.; Lindl, K.A.; Ritson, G.P.; Chia, L.A.; Hamilton, R.L.; Chu, C.T.; Jordan-Sciutto, K.L. Expression of Nrf2 in neurodegenerative diseases. J. Neuropathol. Exp. Neurol., 2007, 66(1), 75-85.
[http://dx.doi.org/10.1097/nen.0b013e31802d6da9] [PMID: 17204939]
[50]
Prestera, T.; Talalay, P.; Alam, J.; Ahn, Y.I.; Lee, P.J.; Choi, A.M.K. Parallel induction of heme oxygenase-1 and chemoprotective phase 2 enzymes by electrophiles and antioxidants: Regulation by upstream Antioxidant-Responsive Elements (ARE). Mol. Med., 1995, 1(7), 827-837.
[http://dx.doi.org/10.1007/BF03401897] [PMID: 8612205]
[51]
Wang, B.; Williamson, G. Detection of a nuclear protein which binds specifically to the antioxidant responsive element (ARE) of the human NAD(P)H: Quinone oxidoreductase gene. Biochim. Biophys. Acta Gene Struct. Expr., 1994, 1219(3), 645-652.
[http://dx.doi.org/10.1016/0167-4781(94)90223-2] [PMID: 7948021]
[52]
Zhou, L.; Wang, W.; Hoppel, C.; Liu, J.; Zhu, X. Parkinson’s disease-associated pathogenic VPS35 mutation causes complex I deficits. Biochim. Biophys. Acta Mol. Basis Dis., 2017, 1863(11), 2791-2795.
[http://dx.doi.org/10.1016/j.bbadis.2017.07.032] [PMID: 28765075]
[53]
Sun, J.; Ren, X.; Simpkins, J.W. Sequential upregulation of superoxide dismutase 2 and heme oxygenase 1 by tert-butylhydroquinone protects mitochondria during oxidative stress. Mol. Pharmacol., 2015, 88(3), 437-449.
[http://dx.doi.org/10.1124/mol.115.098269] [PMID: 26082377]
[54]
Miyamoto, N.; Izumi, H.; Miyamoto, R.; Kondo, H.; Tawara, A.; Sasaguri, Y.; Kohno, K. Quercetin induces the expression of peroxiredoxins 3 and 5 via the Nrf2/NRF1 transcription pathway. Invest. Ophthalmol. Vis. Sci., 2011, 52(2), 1055-1063.
[http://dx.doi.org/10.1167/iovs.10-5777] [PMID: 21051700]
[55]
Rushmore, T.H.; Pickett, C.B. Transcriptional regulation of the rat glutathione S-transferase Ya subunit gene. Characterization of a xenobiotic-responsive element controlling inducible expression by phenolic antioxidants. J. Biol. Chem., 1990, 265(24), 14648-14653.
[http://dx.doi.org/10.1016/S0021-9258(18)77351-1] [PMID: 2387873]
[56]
Mulcahy, R.T.; Gipp, J.J. Identification of a putative antioxidant response element in the 5′-flanking region of the human gamma-glutamylcysteine synthetase heavy subunit gene. Biochem. Biophys. Res. Commun., 1995, 209(1), 227-233.
[http://dx.doi.org/10.1006/bbrc.1995.1493] [PMID: 7726839]
[57]
Nakamura, K.; Wang, W.; Kang, U.J. The role of glutathione in dopaminergic neuronal survival. J. Neurochem., 1997, 69(5), 1850-1858.
[http://dx.doi.org/10.1046/j.1471-4159.1997.69051850.x] [PMID: 9349527]
[58]
Cook, A.L.; Vitale, A.M.; Ravishankar, S.; Matigian, N.; Sutherland, G.T.; Shan, J.; Sutharsan, R.; Perry, C.; Silburn, P.A.; Mellick, G.D.; Whitelaw, M.L.; Wells, C.A.; Mackay-Sim, A.; Wood, S.A. Nrf2 activation restores disease related metabolic deficiencies in olfactory neurosphere-derived cells from patients with sporadic Parkinson’s disease. PLoS One, 2011, 6(7), e21907.
[http://dx.doi.org/10.1371/journal.pone.0021907] [PMID: 21747966]
[59]
Puschmann, A. Monogenic Parkinson’s disease and parkinsonism: Clinical phenotypes and frequencies of known mutations. Parkinsonism Relat. Disord., 2013, 19(4), 407-415.
[http://dx.doi.org/10.1016/j.parkreldis.2013.01.020] [PMID: 23462481]
[60]
Onyango, I.G.; Khan, S.M.; Bennett, J.P. Jr. Mitochondria in the pathophysiology of Alzheimer’s and Parkinson’s diseases. Front. Biosci., 2017, 22(5), 854-872.
[http://dx.doi.org/10.2741/4521] [PMID: 27814651]
[61]
Olanow, C.W. The pathogenesis of cell death in Parkinson’s disease – 2007. Mov. Disord., 2007, 22(S17), S335-S342.
[http://dx.doi.org/10.1002/mds.21675] [PMID: 18175394]
[62]
Yacoubian, T.A.; Standaert, D.G. Targets for neuroprotection in Parkinson’s disease. Biochim. Biophys. Acta Mol. Basis Dis., 2009, 1792(7), 676-687.
[http://dx.doi.org/10.1016/j.bbadis.2008.09.009] [PMID: 18930814]
[63]
Wang, Q.; Li, W.X.; Dai, S.X.; Guo, Y.C.; Han, F.F.; Zheng, J.J.; Li, G.H.; Huang, J.F. Meta-analysis of Parkinson’s disease and Alzheimer’s disease revealed commonly impaired pathways and dysregulation of Nrf2-dependent genes. J. Alzheimers Dis., 2017, 56(4), 1525-1539.
[http://dx.doi.org/10.3233/JAD-161032] [PMID: 28222515]
[64]
Schipper, H.M.; Liberman, A.; Stopa, E.G. Neural heme oxygenase-1 expression in idiopathic Parkinson’s disease. Exp. Neurol., 1998, 150(1), 60-68.
[http://dx.doi.org/10.1006/exnr.1997.6752] [PMID: 9514830]
[65]
Li, Y.; Sun, H.; Chen, Z.; Xu, H.; Bu, G.; Zheng, H. Implications of GABAergic neurotransmission in Alzheimer’s disease. Front. Aging Neurosci., 2016, 8, 31.
[http://dx.doi.org/10.3389/fnagi.2016.00031] [PMID: 26941642]
[66]
Alzheimer’s Association 2017 Alzheimer’s disease facts and figures. Alzheimers Dement., 2017, 13(4), 325-373.
[http://dx.doi.org/10.1016/j.jalz.2017.02.001]
[67]
Alzheimer’s Association Alzheimer’s disease facts and figures. Alzheimers Dement., 2018, 14(3), 367-429.
[http://dx.doi.org/10.1016/j.jalz.2018.02.001]
[68]
Lin, M.T.; Beal, M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature, 2006, 443(7113), 787-795.
[http://dx.doi.org/10.1038/nature05292] [PMID: 17051205]
[69]
Jo, D.G.; Arumugam, T.V.; Woo, H.N.; Park, J.S.; Tang, S.C.; Mughal, M.; Hyun, D.H.; Park, J.H.; Choi, Y.H.; Gwon, A.R.; Camandola, S.; Cheng, A.; Cai, H.; Song, W.; Markesbery, W.R.; Mattson, M.P. Evidence that γ-secretase mediates oxidative stress-induced β-secretase expression in Alzheimer’s disease. Neurobiol. Aging, 2010, 31(6), 917-925.
[http://dx.doi.org/10.1016/j.neurobiolaging.2008.07.003] [PMID: 18687504]
[70]
Bonda, D.J.; Wang, X.; Perry, G.; Nunomura, A.; Tabaton, M.; Zhu, X.; Smith, M.A. Oxidative stress in Alzheimer’s disease: A possibility for prevention. Neuropharmacology, 2010, 59(4-5), 290-294.
[http://dx.doi.org/10.1016/j.neuropharm.2010.04.005] [PMID: 20394761]
[71]
Gwon, A.R.; Park, J.S.; Arumugam, T.V.; Kwon, Y.K.; Chan, S.L.; Kim, S.H.; Baik, S.H.; Yang, S.; Yun, Y.K.; Choi, Y.; Kim, S.; Tang, S.C.; Hyun, D.H.; Cheng, A.; Dann, C.E., III; Bernier, M.; Lee, J.; Markesbery, W.R.; Mattson, M.P.; Jo, D.G. Oxidative lipid modification of nicastrin enhances amyloidogenic γ-secretase activity in Alzheimer’s disease. Aging Cell, 2012, 11(4), 559-568.
[http://dx.doi.org/10.1111/j.1474-9726.2012.00817.x] [PMID: 22404891]
[72]
Liu, Z.; Zhou, T.; Ziegler, A.C.; Dimitrion, P.; Zuo, L. Oxidative stress in neurodegenerative diseases: From molecular mechanisms to clinical applications. Oxid. Med. Cell. Longev., 2017, 2017, 1-11.
[http://dx.doi.org/10.1155/2017/2525967] [PMID: 28785371]
[73]
Müller, W.E.; Eckert, A.; Kurz, C.; Eckert, G.P.; Leuner, K. Mitochondrial dysfunction: Common final pathway in brain aging and Alzheimer’s disease-therapeutic aspects. Mol. Neurobiol., 2010, 41(2-3), 159-171.
[http://dx.doi.org/10.1007/s12035-010-8141-5] [PMID: 20461558]
[74]
Galasko, D.; Montine, T.J. Biomarkers of oxidative damage and inflammation in Alzheimer’s disease. Biomarkers Med., 2010, 4(1), 27-36.
[http://dx.doi.org/10.2217/bmm.09.89] [PMID: 20383271]
[75]
Smith, J.A.; Das, A.; Ray, S.K.; Banik, N.L. Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res. Bull., 2012, 87(1), 10-20.
[http://dx.doi.org/10.1016/j.brainresbull.2011.10.004] [PMID: 22024597]
[76]
Giraldo, E. Lloret, A.; Fuchsberger, T.; Viña, J. Aβ and tau toxicities in Alzheimer’s are linked via oxidative stress-induced p38 activation: Protective role of vitamin E. Redox Biol., 2014, 2, 873-877.
[http://dx.doi.org/10.1016/j.redox.2014.03.002] [PMID: 25061569]
[77]
Uttara, B.; Singh, A.; Zamboni, P.; Mahajan, R. Oxidative stress and neurodegenerative diseases: A review of upstream and downstream antioxidant therapeutic options. Curr. Neuropharmacol., 2009, 7(1), 65-74.
[http://dx.doi.org/10.2174/157015909787602823] [PMID: 19721819]
[78]
Feng, Y.; Wang, X. Antioxidant therapies for Alzheimer’s disease. Oxid. Med. Cell. Longev., 2012, 2012, 1-17.
[http://dx.doi.org/10.1155/2012/472932] [PMID: 22888398]
[79]
Woo, H.N.; Park, J.S.; Gwon, A.R.; Arumugam, T.V.; Jo, D.G. Alzheimer’s disease and notch signaling. Biochem. Biophys. Res. Commun., 2009, 390(4), 1093-1097.
[http://dx.doi.org/10.1016/j.bbrc.2009.10.093] [PMID: 19853579]
[80]
Zhang, Y.; Thompson, R.; Zhang, H.; Xu, H. APP processing in Alzheimer’s disease. Mol. Brain, 2011, 4(1), 3.
[http://dx.doi.org/10.1186/1756-6606-4-3] [PMID: 21214928]
[81]
Bona, D.; Scapagnini, G.; Candore, G.; Castiglia, L.; Colonna-Romano, G.; Duro, G.; Nuzzo, D.; Iemolo, F.; Lio, D.; Pellicanò, M.; Scafidi, V.; Caruso, C.; Vasto, S. Immune-inflammatory responses and oxidative stress in Alzheimer’s disease: Therapeutic implications. Curr. Pharm. Des., 2010, 16(6), 684-691.
[http://dx.doi.org/10.2174/138161210790883769] [PMID: 20388078]
[82]
Lovell, M.A.; Markesbery, W.R. Oxidative damage in mild cognitive impairment and early Alzheimer’s disease. J. Neurosci. Res., 2007, 85(14), 3036-3040.
[http://dx.doi.org/10.1002/jnr.21346] [PMID: 17510979]
[83]
Gubandru, M.; Margina, D.; Tsitsimpikou, C.; Goutzourelas, N.; Tsarouhas, K.; Ilie, M.; Tsatsakis, A.M.; Kouretas, D. Alzheimer’s disease treated patients showed different patterns for oxidative stress and inflammation markers. Food Chem. Toxicol., 2013, 61, 209-214.
[http://dx.doi.org/10.1016/j.fct.2013.07.013] [PMID: 23871825]
[84]
Schrag, M.; Mueller, C.; Zabel, M.; Crofton, A.; Kirsch, W.M.; Ghribi, O.; Squitti, R.; Perry, G. Oxidative stress in blood in Alzheimer’s disease and mild cognitive impairment: A meta-analysis. Neurobiol. Dis., 2013, 59, 100-110.
[http://dx.doi.org/10.1016/j.nbd.2013.07.005] [PMID: 23867235]
[85]
Zabel, M.; Nackenoff, A.; Kirsch, W.M.; Harrison, F.E.; Perry, G.; Schrag, M. Markers of oxidative damage to lipids, nucleic acids and proteins and antioxidant enzymes activities in Alzheimer’s disease brain: A meta-analysis in human pathological specimens. Free Radic. Biol. Med., 2018, 115, 351-360.
[http://dx.doi.org/10.1016/j.freeradbiomed.2017.12.016] [PMID: 29253591]
[86]
Kanninen, K.; Heikkinen, R.; Malm, T.; Rolova, T.; Kuhmonen, S.; Leinonen, H.; Ylä-Herttuala, S.; Tanila, H.; Levonen, A.L.; Koistinaho, M.; Koistinaho, J. Intrahippocampal injection of a lentiviral vector expressing Nrf2 improves spatial learning in a mouse model of Alzheimer’s disease. Proc. Natl. Acad. Sci. USA, 2009, 106(38), 16505-16510.
[http://dx.doi.org/10.1073/pnas.0908397106] [PMID: 19805328]
[87]
Caesar, I.; Jonson, M.; Nilsson, K.P.R. Curcumin promotes a-beta fibrillation and reduces neurotoxicity in transgenic Drosophila. PLoS One 7, 2012, 7(2), 31424.
[88]
Kitani, K.; Osawa, T.; Yokozawa, T. The effects of tetrahydrocurcumin and green tea polyphenol on the survival of male C57BL/6 mice. Biogerontology, 2007, 8(5), 567-573.
[http://dx.doi.org/10.1007/s10522-007-9100-z] [PMID: 17516143]
[89]
Du, L.L.; Xie, J.Z.; Cheng, X.S.; Li, X.H.; Kong, F.L.; Jiang, X.; Ma, Z.W.; Wang, J.Z.; Chen, C.; Zhou, X.W. Activation of sirtuin 1 attenuates cerebral ventricular streptozotocin-induced tau hyperphosphorylation and cognitive injuries in rat hippocampi. Age, 2014, 36(2), 613-623.
[http://dx.doi.org/10.1007/s11357-013-9592-1] [PMID: 24142524]
[90]
Porquet, D.; Casadesús, G.; Bayod, S.; Vicente, A.; Canudas, A.M.; Vilaplana, J.; Pelegrí, C.; Sanfeliu, C.; Camins, A.; Pallàs, M.; del Valle, J. Dietary resveratrol prevents Alzheimer’s markers and increases life span in SAMP8. Age, 2013, 35(5), 1851-1865.
[http://dx.doi.org/10.1007/s11357-012-9489-4] [PMID: 23129026]
[91]
Lee, C.; Park, G.H.; Lee, S.R.; Jang, J.H. Attenuation of β-amyloid-induced oxidative cell death by sulforaphane via activation of NF-E2-related factor 2. Oxid. Med. Cell. Longev., 2013, 2013, 1-12.
[http://dx.doi.org/10.1155/2013/313510] [PMID: 23864927]
[92]
Egea, J.; Buendia, I.; Parada, E.; Navarro, E.; Rada, P.; Cuadrado, A.; López, M.G.; García, A.G.; León, R. Melatonin-sulforaphane hybrid ITH12674 induces neuroprotection in oxidative stress conditions by a ‘drug-prodrug’ mechanism of action. Br. J. Pharmacol., 2015, 172(7), 1807-1821.
[http://dx.doi.org/10.1111/bph.13025] [PMID: 25425158]
[93]
Xie, G.; Tian, W.; Wei, T.; Liu, F. The neuroprotective effects of β-hydroxybutyrate on β-injected rat hippocampus in vivo and in Aβ-treated PC-12 cells in vitro. Free Radic. Res., 2015, 49(2), 139-150.
[http://dx.doi.org/10.3109/10715762.2014.987274] [PMID: 25410532]
[94]
Yu, L.; Wang, S.; Chen, X.; Yang, H.; Li, X.; Xu, Y.; Zhu, X. Orientin alleviates cognitive deficits and oxidative stress in Aβ1–42-induced mouse model of Alzheimer’s disease. Life Sci., 2015, 121, 104-109.
[http://dx.doi.org/10.1016/j.lfs.2014.11.021] [PMID: 25497709]
[95]
Chang, W.H.; Chen, M.C.; Cheng, I.H. Antroquinonol lowers brain amyloid-β levels and improves spatial learning and memory in a transgenic mouse model of Alzheimer’s disease. Sci. Rep., 2015, 5(1), 15067.
[http://dx.doi.org/10.1038/srep15067] [PMID: 26469245]
[96]
Fragoulis, A.; Siegl, S.; Fendt, M.; Jansen, S.; Soppa, U.; Brandenburg, L.O.; Pufe, T.; Weis, J.; Wruck, C.J. Oral administration of methysticin improves cognitive deficits in a mouse model of Alzheimer’s disease. Redox Biol., 2017, 12, 843-853.
[http://dx.doi.org/10.1016/j.redox.2017.04.024] [PMID: 28448946]
[97]
Stack, C.; Jainuddin, S.; Elipenahli, C.; Gerges, M.; Starkova, N.; Starkov, A.A.; Jové, M.; Portero-Otin, M.; Launay, N.; Pujol, A.; Kaidery, N.A.; Thomas, B.; Tampellini, D.; Beal, M.F.; Dumont, M. Methylene blue upregulates Nrf2/ARE genes and prevents tau-related neurotoxicity. Hum. Mol. Genet., 2014, 23(14), 3716-3732.
[http://dx.doi.org/10.1093/hmg/ddu080] [PMID: 24556215]
[98]
Jimenez-Sanchez, M.; Licitra, F.; Underwood, B.R.; Rubinsztein, D.C. Huntington’s disease: Mechanisms of pathogenesis and therapeutic strategies. Cold Spring Harb. Perspect. Med., 2017, 7(7), a024240.
[http://dx.doi.org/10.1101/cshperspect.a024240] [PMID: 27940602]
[99]
Ayala-Peña, S. Role of oxidative DNA damage in mitochondrial dysfunction and Huntington’s disease pathogenesis. Free Radic. Biol. Med., 2013, 62, 102-110.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.04.017] [PMID: 23602907]
[100]
Zielonka, D.; Mielcarek, M.; Landwehrmeyer, G.B. Update on Huntington’s disease: Advances in care and emerging therapeutic options. Parkinsonism Relat. Disord., 2015, 21(3), 169-178.
[http://dx.doi.org/10.1016/j.parkreldis.2014.12.013] [PMID: 25572500]
[101]
Chen, C.M.; Wu, Y.R.; Cheng, M.L.; Liu, J.L.; Lee, Y.M.; Lee, P.W.; Soong, B.W.; Chiu, D.T.Y. Increased oxidative damage and mitochondrial abnormalities in the peripheral blood of Huntington’s disease patients. Biochem. Biophys. Res. Commun., 2007, 359(2), 335-340.
[http://dx.doi.org/10.1016/j.bbrc.2007.05.093] [PMID: 17543886]
[102]
Klepac, N.; Relja, M.; Klepac, R. Hećimović S.; Babić T.; Trkulja, V. Oxidative stress parameters in plasma of Huntington’s disease patients, asymptomatic Huntington’s disease gene carriers and healthy subjects. J. Neurol., 2007, 254(12), 1676-1683.
[http://dx.doi.org/10.1007/s00415-007-0611-y] [PMID: 17990062]
[103]
Browne, S.E.; Beal, M.F. Oxidative damage in Huntington’s disease pathogenesis. Antioxid. Redox Signal., 2006, 8(11-12), 2061-2073.
[http://dx.doi.org/10.1089/ars.2006.8.2061] [PMID: 17034350]
[104]
Sorolla, M.A.; Reverter-Branchat, G.; Tamarit, J.; Ferrer, I.; Ros, J.; Cabiscol, E. Proteomic and oxidative stress analysis in human brain samples of Huntington’s disease. Free Radic. Biol. Med., 2008, 45(5), 667-678.
[http://dx.doi.org/10.1016/j.freeradbiomed.2008.05.014] [PMID: 18588971]
[105]
Duran, R.; Barrero, F.J.; Morales, B.; Luna, J.D.; Ramirez, M.; Vives, F. Oxidative stress and plasma aminopeptidase activity in Huntington’s disease. J. Neural Transm., 2010, 117(3), 325-332.
[http://dx.doi.org/10.1007/s00702-009-0364-0] [PMID: 20094738]
[106]
Johri, A.; Beal, M.F. Antioxidants in Huntington’s disease. Biochim. Biophys. Acta Mol. Basis Dis., 2012, 1822(5), 664-674.
[http://dx.doi.org/10.1016/j.bbadis.2011.11.014] [PMID: 22138129]
[107]
Prasad, K.N.; Bondy, S.C. Inhibition of early biochemical defects in prodromal Huntington’s disease by simultaneous activation of Nrf2 and elevation of multiple micronutrients. Curr. Aging Sci., 2016, 9(1), 61-70.
[http://dx.doi.org/10.2174/1874609809666151124231127] [PMID: 26601664]
[108]
Dalrymple, A.; Wild, E.J.; Joubert, R.; Sathasivam, K.; Björkqvist, M.; Petersén, Å.; Jackson, G.S.; Isaacs, J.D.; Kristiansen, M.; Bates, G.P.; Leavitt, B.R.; Keir, G.; Ward, M.; Tabrizi, S.J. Proteomic profiling of plasma in Huntington’s disease reveals neuroinflammatory activation and biomarker candidates. J. Proteome Res., 2007, 6(7), 2833-2840.
[http://dx.doi.org/10.1021/pr0700753] [PMID: 17552550]
[109]
Silvestroni, A.; Faull, R.L.M.; Strand, A.D.; Möller, T. Distinct neuroinflammatory profile in post-mortem human Huntington’s disease. Neuroreport, 2009, 20(12), 1098-1103.
[http://dx.doi.org/10.1097/WNR.0b013e32832e34ee] [PMID: 19590393]
[110]
Sapp, E.; Kegel, K.B.; Aronin, N.; Hashikawa, T.; Uchiyama, Y.; Tohyama, K.; Bhide, P.G.; Vonsattel, J.P.; Difiglia, M. Early and progressive accumulation of reactive microglia in the Huntington disease brain. J. Neuropathol. Exp. Neurol., 2001, 60(2), 161-172.
[http://dx.doi.org/10.1093/jnen/60.2.161] [PMID: 11273004]
[111]
Björkqvist, M.; Wild, E.J.; Thiele, J.; Silvestroni, A.; Andre, R.; Lahiri, N.; Raibon, E.; Lee, R.V.; Benn, C.L.; Soulet, D.; Magnusson, A.; Woodman, B.; Landles, C.; Pouladi, M.A.; Hayden, M.R.; Khalili-Shirazi, A.; Lowdell, M.W.; Brundin, P.; Bates, G.P.; Leavitt, B.R.; Möller, T.; Tabrizi, S.J. A novel pathogenic pathway of immune activation detectable before clinical onset in Huntington’s disease. J. Exp. Med., 2008, 205(8), 1869-1877.
[http://dx.doi.org/10.1084/jem.20080178] [PMID: 18625748]
[112]
Wild, E.; Magnusson, A.; Lahiri, N.; Krus, U.; Orth, M.; Tabrizi, S.J.; Björkqvist, M. Abnormal peripheral chemokine profile in Huntington’s disease. PLoS Curr., 2011, 3, RRN1231.
[http://dx.doi.org/10.1371/currents.RRN1231] [PMID: 21826115]
[113]
Möller, T. Neuroinflammation in Huntington’s disease. J. Neural Transm., 2010, 117(8), 1001-1008.
[http://dx.doi.org/10.1007/s00702-010-0430-7] [PMID: 20535620]
[114]
Pavese, N.; Gerhard, A.; Tai, Y.F.; Ho, A.K.; Turkheimer, F.; Barker, R.A.; Brooks, D.J.; Piccini, P. Microglial activation correlates with severity in Huntington’s disease: A clinical and PET study. Neurology, 2006, 66(11), 1638-1643.
[http://dx.doi.org/10.1212/01.wnl.0000222734.56412.17] [PMID: 16769933]
[115]
Tai, Y.F.; Pavese, N.; Gerhard, A.; Tabrizi, S.J.; Barker, R.A.; Brooks, D.J.; Piccini, P. Imaging microglial activation in Huntington’s disease. Brain Res. Bull., 2007, 72(2-3), 148-151.
[http://dx.doi.org/10.1016/j.brainresbull.2006.10.029] [PMID: 17352938]
[116]
Frank-Cannon, T.C.; Alto, L.T.; McAlpine, F.E.; Tansey, M.G. Does neuroinflammation fan the flame in neurodegenerative diseases? Mol. Neurodegener., 2009, 4(1), 47.
[http://dx.doi.org/10.1186/1750-1326-4-47] [PMID: 19917131]
[117]
Politis, M.; Pavese, N.; Tai, Y.F.; Kiferle, L.; Mason, S.L.; Brooks, D.J.; Tabrizi, S.J.; Barker, R.A.; Piccini, P. Microglial activation in regions related to cognitive function predicts disease onset in Huntington’s disease: A multimodal imaging study. Hum. Brain Mapp., 2011, 32(2), 258-270.
[http://dx.doi.org/10.1002/hbm.21008] [PMID: 21229614]
[118]
Ribeiro, M.; Rosenstock, T.R.; Oliveira, A.M.; Oliveira, C.R.; Rego, A.C. Insulin and IGF-1 improve mitochondrial function in a PI-3K/Akt-dependent manner and reduce mitochondrial generation of reactive oxygen species in Huntington’s disease knock-in striatal cells. Free Radic. Biol. Med., 2014, 74, 129-144.
[http://dx.doi.org/10.1016/j.freeradbiomed.2014.06.023] [PMID: 24992836]
[119]
Browne, P.; Chandraratna, D.; Angood, C.; Tremlett, H.; Baker, C.; Taylor, B.V.; Thompson, A.J. Atlas of multiple sclerosis 2013: A growing global problem with widespread inequity. Neurology, 2014, 83(11), 1022-1024.
[http://dx.doi.org/10.1212/WNL.0000000000000768] [PMID: 25200713]
[120]
Frohman, E.M.; Racke, M.K.; Raine, C.S. Multiple sclerosis-the plaque and its pathogenesis. N. Engl. J. Med., 2006, 354(9), 942-955.
[http://dx.doi.org/10.1056/NEJMra052130] [PMID: 16510748]
[121]
Wootla, B.; Eriguchi, M.; Rodriguez, M. Is multiple sclerosis an autoimmune disease? Autoimmune Dis., 2012, 2012, 1-12.
[http://dx.doi.org/10.1155/2012/969657] [PMID: 22666554]
[122]
Compston, A.; Coles, A. Multiple sclerosis. Lancet, 2008, 372(9648), 1502-1517.
[http://dx.doi.org/10.1016/S0140-6736(08)61620-7] [PMID: 18970977]
[123]
Lassmann, H. Axonal and neuronal pathology in multiple sclerosis: What have we learnt from animal models. Exp. Neurol., 2010, 225(1), 2-8.
[http://dx.doi.org/10.1016/j.expneurol.2009.10.009] [PMID: 19840788]
[124]
Lassmann, H.; Brück, W.; Lucchinetti, C.F. The immunopathology of multiple sclerosis: An overview. Brain Pathol., 2007, 17(2), 210-218.
[http://dx.doi.org/10.1111/j.1750-3639.2007.00064.x] [PMID: 17388952]
[125]
Jäger, A.; Kuchroo, V.K. Effector and regulatory T-cell subsets in autoimmunity and tissue inflammation. Scand. J. Immunol., 2010, 72(3), 173-184.
[http://dx.doi.org/10.1111/j.1365-3083.2010.02432.x] [PMID: 20696013]
[126]
Łyszczarz, A.; Szczuciński, A.; Pawlak, M.A.; Losy, J. Clinical study on CXCL13, CCL17, CCL20 and IL-17 as immune cell migration navigators in relapsing-remitting multiple sclerosis patients. J. Neurol. Sci., 2011, 300(1-2), 81-85.
[http://dx.doi.org/10.1016/j.jns.2010.09.026] [PMID: 20947098]
[127]
Khaibullin, T.; Ivanova, V.; Martynova, E.; Cherepnev, G.; Khabirov, F.; Granatov, E.; Rizvanov, A.; Khaiboullina, S. Elevated levels of proinflammatory cytokines in cerebrospinal fluid of multiple sclerosis patients. Front. Immunol., 2017, 8, 531.
[http://dx.doi.org/10.3389/fimmu.2017.00531] [PMID: 28572801]
[128]
Smith, K.J.; Kapoor, R.; Felts, P.A. Demyelination: The role of reactive oxygen and nitrogen species. Brain Pathol., 1999, 9(1), 69-92.
[http://dx.doi.org/10.1111/j.1750-3639.1999.tb00212.x] [PMID: 9989453]
[129]
Mahad, D.; Ziabreva, I.; Lassmann, H.; Turnbull, D. Mitochondrial defects in acute multiple sclerosis lesions. Brain, 2008, 131(7), 1722-1735.
[http://dx.doi.org/10.1093/brain/awn105] [PMID: 18515320]
[130]
Witte, M.E.; Geurts, J.J.G.; De Vries, H.E.; Van Der Valk, P.; Van Horssen, J. Mitochondrial dysfunction: A potential link between neuroinflammation and neurodegeneration? Mitochondrion, 2010, 10(5), 411-418.
[http://dx.doi.org/10.1016/j.mito.2010.05.014] [PMID: 20573557]
[131]
Lassmann, H.; Van Horssen, J. The molecular basis of neurodegeneration in multiple sclerosis. FEBS Lett., 2011, 585(23), 3715-3723.
[http://dx.doi.org/10.1016/j.febslet.2011.08.004] [PMID: 21854776]
[132]
Haider, L.; Fischer, M.T.; Frischer, J.M.; Bauer, J.; Höftberger, R.; Botond, G.; Esterbauer, H.; Binder, C.J.; Witztum, J.L.; Lassmann, H. Oxidative damage in multiple sclerosis lesions. Brain, 2011, 134(7), 1914-1924.
[http://dx.doi.org/10.1093/brain/awr128] [PMID: 21653539]
[133]
Van Horssen, J.; Drexhage, J.A.R.; Flor, T.; Gerritsen, W.; Van Der Valk, P.; De Vries, H.E. Nrf2 and DJ1 are consistently upregulated in inflammatory multiple sclerosis lesions. Free Radic. Biol. Med., 2010, 49(8), 1283-1289.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.07.013] [PMID: 20673799]
[134]
Hirotani, M.; Maita, C.; Niino, M.; Iguchi-Ariga, S.M.; Hamada, S.; Ariga, H.; Sasaki, H. Correlation between DJ-1 levels in the cerebrospinal fluid and the progression of disabilities in multiple sclerosis patients. Mult. Scler., 2008, 14(8), 1056-1060.
[http://dx.doi.org/10.1177/1352458508093616] [PMID: 18632777]
[135]
Van Horssen, J.; Schreibelt, G.; Drexhage, J.; Hazes, T.; Dijkstra, C.D.; Van Der Valk, P.; De Vries, H.E. Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic. Biol. Med., 2008, 45(12), 1729-1737.
[http://dx.doi.org/10.1016/j.freeradbiomed.2008.09.023] [PMID: 18930811]
[136]
Van Horssen, J.; Witte, M.E.; Schreibelt, G.; De Vries, H.E. Radical changes in multiple sclerosis pathogenesis. Biochim. Biophys. Acta Mol. Basis Dis., 2011, 1812(2), 141-150.
[http://dx.doi.org/10.1016/j.bbadis.2010.06.011] [PMID: 20600869]
[137]
Qi, X.; Lewin, A.S.; Sun, L.; Hauswirth, W.W.; Guy, J. Mitochondrial protein nitration primes neurodegeneration in experimental autoimmune encephalomyelitis. J. Biol. Chem., 2006, 281(42), 31950-31962.
[http://dx.doi.org/10.1016/S0021-9258(19)84109-1] [PMID: 16920708]
[138]
Sadeghian, M.; Mastrolia, V.; Rezaei Haddad, A.; Mosley, A.; Mullali, G.; Schiza, D.; Sajic, M.; Hargreaves, I.; Heales, S.; Duchen, M.R.; Smith, K.J. Mitochondrial dysfunction is an important cause of neurological deficits in an inflammatory model of multiple sclerosis. Sci. Rep., 2016, 6(1), 1-14.
[http://dx.doi.org/10.1038/srep33249] [PMID: 27624721]
[139]
Wang, L.; Li, B.; Quan, M.Y.; Li, L.; Chen, Y.; Tan, G.J.; Zhang, J.; Liu, X.P.; Guo, L. Mechanism of oxidative stress p38MAPK-SGK1 signaling axis in experimental autoimmune encephalo-] myelitis (EAE). Oncotarget, 2017, 8(26), 42808-42816.
[http://dx.doi.org/10.18632/oncotarget.17057] [PMID: 28467798]
[140]
Schulze-Topphoff, U.; Varrin-Doyer, M.; Pekarek, K.; Spencer, C.M.; Shetty, A.; Sagan, S.A.; Cree, B.A.C.; Sobel, R.A.; Wipke, B.T.; Steinman, L.; Scannevin, R.H.; Zamvil, S.S. Dimethyl fumarate treatment induces adaptive and innate immune modulation independent of Nrf2. Proc. Natl. Acad. Sci., 2016, 113(17), 4777-4782.
[http://dx.doi.org/10.1073/pnas.1603907113] [PMID: 27078105]
[141]
Yang, Z.B.; Chen, W.W.; Chen, H.P.; Cai, S.X.; Lin, J.D.; Qiu, L.Z. MiR-155 aggravated septic liver injury by oxidative stress-mediated ER stress and mitochondrial dysfunction via targeting Nrf-2. Exp. Mol. Pathol., 2018, 105(3), 387-394.
[http://dx.doi.org/10.1016/j.yexmp.2018.09.003] [PMID: 30218645]
[142]
Noh, H.; Jeon, J.; Seo, H. Systemic injection of LPS induces region-specific neuroinflammation and mitochondrial dysfunction in normal mouse brain. Neurochem. Int., 2014, 69, 35-40.
[http://dx.doi.org/10.1016/j.neuint.2014.02.008] [PMID: 24607701]
[143]
Johnson, D.A.; Amirahmadi, S.; Ward, C.; Fabry, Z.; Johnson, J.A. The absence of the pro-antioxidant transcription factor Nrf2 exacerbates experimental autoimmune encephalomyelitis. Toxicol. Sci., 2010, 114(2), 237-246.
[http://dx.doi.org/10.1093/toxsci/kfp274] [PMID: 19910389]
[144]
Larabee, C.M.; Desai, S.; Agasing, A.; Georgescu, C.; Wren, J.D.; Axtell, R.C.; Plafker, S.M. Loss of Nrf2 exacerbates the visual deficits and optic neuritis elicited by experimental autoimmune encephalomyelitis. Mol. Vis., 2016, 22, 1503-1513.
[PMID: 28050123]
[145]
Chen, W.J.; Du, J.K.; Hu, X.; Yu, Q.; Li, D.X.; Wang, C.N.; Zhu, X.Y.; Liu, Y.J. Protective effects of resveratrol on mitochondrial function in the hippocampus improves inflammation-induced depressive-like behavior. Physiol. Behav., 2017, 182, 54-61.
[http://dx.doi.org/10.1016/j.physbeh.2017.09.024] [PMID: 28964807]
[146]
Khan, A.; Ali, T.; Rehman, S.U.; Khan, M.S.; Alam, S.I.; Ikram, M.; Muhammad, T.; Saeed, K.; Badshah, H.; Kim, M.O. Neuroprotective effect of quercetin against the detrimental effects of LPS in the adult mouse brain. Front. Pharmacol., 2018, 9, 1383.
[http://dx.doi.org/10.3389/fphar.2018.01383] [PMID: 30618732]
[147]
Rehman, S.U.; Ali, T.; Alam, S.I.; Ullah, R.; Zeb, A.; Lee, K.W.; Rutten, B.P.F.; Kim, M.O. Ferulic acid rescues LPS-induced neurotoxicity via modulation of the TLR4 receptor in the mouse hippocampus. Mol. Neurobiol., 2019, 56(4), 2774-2790.
[http://dx.doi.org/10.1007/s12035-018-1280-9] [PMID: 30058023]
[148]
Wang, J.; Zou, Q.; Suo, Y.; Tan, X.; Yuan, T.; Liu, Z.; Liu, X. Lycopene ameliorates systemic inflammation-induced synaptic dysfunction via improving insulin resistance and mitochondrial dysfunction in the liver–brain axis. Food Funct., 2019, 10(4), 2125-2137.
[http://dx.doi.org/10.1039/C8FO02460J] [PMID: 30924473]
[149]
Linker, R.A.; Lee, D.H.; Ryan, S.; Van Dam, A.M.; Conrad, R.; Bista, P.; Zeng, W.; Hronowsky, X.; Buko, A.; Chollate, S.; Ellrichmann, G.; Brück, W.; Dawson, K.; Goelz, S.; Wiese, S.; Scannevin, R.H.; Lukashev, M.; Gold, R. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain, 2011, 134(3), 678-692.
[http://dx.doi.org/10.1093/brain/awq386] [PMID: 21354971]
[150]
Bomprezzi, R. Dimethyl fumarate in the treatment of relapsing–remitting multiple sclerosis: An overview. Ther. Adv. Neurol. Disord., 2015, 8(1), 20-30.
[http://dx.doi.org/10.1177/1756285614564152] [PMID: 25584071]
[151]
Gopal, S.; Mikulskis, A.; Gold, R.; Fox, R.J.; Dawson, K.T.; Amaravadi, L. Evidence of activation of the Nrf2 pathway in multiple sclerosis patients treated with delayed-release dimethyl fumarate in the Phase 3 DEFINE and CONFIRM studies. Mult. Scler., 2017, 23(14), 1875-1883.
[http://dx.doi.org/10.1177/1352458517690617] [PMID: 28156185]
[152]
Blair, H.A. Dimethyl fumarate: A review in moderate to severe plaque psoriasis. Drugs, 2018, 78(1), 123-130.
[http://dx.doi.org/10.1007/s40265-017-0854-6] [PMID: 29236231]
[153]
Ahuja, M.; Ammal Kaidery, N.; Yang, L.; Calingasan, N.; Smirnova, N.; Gaisin, A.; Gaisina, I.N.; Gazaryan, I.; Hushpulian, D.M.; Kaddour-Djebbar, I.; Bollag, W.B.; Morgan, J.C.; Ratan, R.R.; Starkov, A.A.; Beal, M.F.; Thomas, B. Distinct Nrf2 signaling mechanisms of fumaric acid esters and their role in neuroprotection against 1‐Methyl‐4‐Phenyl‐1,2,3,6‐tetrahydropyridine‐induced experimental Parkinson’s-like disease. J. Neurosci., 2016, 36(23), 6332-6351.
[http://dx.doi.org/10.1523/JNEUROSCI.0426-16.2016] [PMID: 27277809]
[154]
Paupe, V.; Dassa, E.P.; Goncalves, S.; Auchère, F.; Lönn, M.; Holmgren, A.; Rustin, P. Impaired nuclear Nrf2 translocation undermines the oxidative stress response in Friedreich ataxia. PLoS One, 2009, 4(1), e4253.
[http://dx.doi.org/10.1371/journal.pone.0004253] [PMID: 19158945]
[155]
Li, K.; Besse, E.K.; Ha, D.; Kovtunovych, G.; Rouault, T.A. Iron-dependent regulation of frataxin expression: Implications for treatment of Friedreich ataxia. Hum. Mol. Genet., 2008, 17(15), 2265-2273.
[http://dx.doi.org/10.1093/hmg/ddn127] [PMID: 18424449]
[156]
Aranca, T.V.; Jones, T.M.; Shaw, J.D.; Staffetti, J.S.; Ashizawa, T.; Kuo, S.H.; Fogel, B.L.; Wilmot, G.R.; Perlman, S.L.; Onyike, C.U.; Ying, S.H.; Zesiewicz, T.A. Emerging therapies in Friedreich’s ataxia. Neurodegener. Dis. Manag., 2016, 6(1), 49-65.
[http://dx.doi.org/10.2217/nmt.15.73] [PMID: 26782317]
[157]
Polek, B.; Roach, M.J.; Andrews, W.T.; Ehling, M.; Salek, S. Burden of Friedreich’s ataxia to the patients and healthcare systems in the United States and Canada. Front. Pharmacol., 2013, 4, 66.
[http://dx.doi.org/10.3389/fphar.2013.00066] [PMID: 23734128]
[158]
Vankan, P. Prevalence gradients of Friedreich’s Ataxia and R1b haplotype in Europe co-localize, suggesting a common Palaeolithic origin in the Franco-Cantabrian ice age refuge. J. Neurochem., 2013, 126, 11-20.
[http://dx.doi.org/10.1111/jnc.12215] [PMID: 23859338]
[159]
Santos, R.; Lefevre, S.; Sliwa, D.; Seguin, A.; Camadro, J.M.; Lesuisse, E. Friedreich ataxia: Molecular mechanisms, redox considerations, and therapeutic opportunities. Antioxid. Redox Signal., 2010, 13(5), 651-690.
[http://dx.doi.org/10.1089/ars.2009.3015] [PMID: 20156111]
[160]
Nickel, A.; Kohlhaas, M.; Maack, C. Mitochondrial reactive oxygen species production and elimination. J. Mol. Cell. Cardiol., 2014, 73, 26-33.
[http://dx.doi.org/10.1016/j.yjmcc.2014.03.011] [PMID: 24657720]
[161]
Anzovino, A.; Chiang, S.; Brown, B.E.; Hawkins, C.L.; Richardson, D.R.; Huang, M.L.H. Molecular alterations in a mouse cardiac model of Friedreich ataxia: An impaired Nrf2 response mediated via upregulation of Keap1 and activation of the Gsk3beta axis. Am. J. Pathol., 2017, 187(12), 2858-2875.
[http://dx.doi.org/10.1016/j.ajpath.2017.08.021] [PMID: 28935570]
[162]
La Rosa, P.; Russo, M.; D’Amico, J.; Petrillo, S.; Aquilano, K.; Lettieri-Barbato, D.; Turchi, R.; Bertini, E.S.; Piemonte, F. Nrf2 induction re-establishes a proper neuronal differentiation program in Friedreich’s ataxia neural stem cells. Front. Cell. Neurosci., 2019, 13, 356.
[http://dx.doi.org/10.3389/fncel.2019.00356] [PMID: 31417369]
[163]
Petrillo, S.; Piermarini, E.; Pastore, A.; Vasco, G.; Schirinzi, T.; Carrozzo, R.; Bertini, E.; Piemonte, F. Nrf2- inducers counteract neurodegeneration in frataxin-silenced motor neurons: Disclosing new therapeutic targets for Friedreich’s ataxia. Int. J. Mol. Sci., 2017, 18(10), 2173.
[http://dx.doi.org/10.3390/ijms18102173] [PMID: 29057804]
[164]
Abeti, R.; Baccaro, A.; Esteras, N.; Giunti, P. Novel Nrf2-inducer prevents mitochondrial defects and oxidative stress in Friedreich’s ataxia models. Front. Cell. Neurosci., 2018, 12, 188.
[http://dx.doi.org/10.3389/fncel.2018.00188] [PMID: 30065630]
[165]
Abeti, R.; Uzun, E.; Renganathan, I.; Honda, T.; Pook, M.A.; Giunti, P. Targeting lipid peroxidation and mitochondrial imbalance in Friedreich’s ataxia. Pharmacol. Res., 2015, 99, 344-350.
[http://dx.doi.org/10.1016/j.phrs.2015.05.015] [PMID: 26141703]
[166]
Sahdeo, S.; Scott, B.D.; McMackin, M.Z.; Jasoliya, M.; Brown, B.; Wulff, H.; Perlman, S.L.; Pook, M.A.; Cortopassi, G.A. Dyclonine rescues frataxin deficiency in animal models and buccal cells of patients with Friedreich’s ataxia. Hum. Mol. Genet., 2014, 23(25), 6848-6862.
[http://dx.doi.org/10.1093/hmg/ddu408] [PMID: 25113747]
[167]
Engel, J., Jr Concepts of epilepsy. Epilepsia, 1995, 36(S1), 23-29.
[http://dx.doi.org/10.1111/j.1528-1157.1995.tb01648.x] [PMID: 23057107]
[168]
Bralowsky, S. Algunas definiciones. Epilepsia, Enfermedad Sagrada del Cerebro; Secretaría de Educación Publica: México, 1999, pp. 1-125.
[169]
Devinsky, O.; Vezzani, A.; O’Brien, T.J.; Jette, N.; Scheffer, I.E.; De Curtis, M.; Perucca, P. Epilepsy. Nat. Rev. Dis. Primers, 2018, 4(1), 18024.
[http://dx.doi.org/10.1038/nrdp.2018.24] [PMID: 29722352]
[170]
Klein, P.; Dingledine, R.; Aronica, E.; Bernard, C.; Blümcke, I.; Boison, D.; Brodie, M.J.; Brooks-Kayal, A.R.; Engel, J., Jr; Forcelli, P.A.; Hirsch, L.J.; Kaminski, R.M.; Klitgaard, H.; Kobow, K.; Lowenstein, D.H.; Pearl, P.L.; Pitkänen, A.; Puhakka, N.; Rogawski, M.A.; Schmidt, D.; Sillanpää, M.; Sloviter, R.S.; Steinhäuser, C.; Vezzani, A.; Walker, M.C.; Löscher, W. Commonalities in epileptogenic processes from different acute brain insults: Do they translate? Epilepsia, 2018, 59(1), 37-66.
[http://dx.doi.org/10.1111/epi.13965] [PMID: 29247482]
[171]
Vezzani, A.; Balosso, S.; Ravizza, T. Neuroinflammatory pathways as treatment targets and biomarkers in epilepsy. Nat. Rev. Neurol., 2019, 15(8), 459-472.
[http://dx.doi.org/10.1038/s41582-019-0217-x] [PMID: 31263255]
[172]
Kobayashi, A.; Kang, M.I.; Okawa, H.; Ohtsuji, M.; Zenke, Y.; Chiba, T.; Igarashi, K.; Yamamoto, M. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol., 2004, 24(16), 7130-7139.
[http://dx.doi.org/10.1128/MCB.24.16.7130-7139.2004] [PMID: 15282312]
[173]
Kaspar, J.W.; Niture, S.K.; Jaiswal, A.K. Antioxidant-induced INrf2 (Keap1) tyrosine 85 phosphorylation controls the nuclear export and degradation of the INrf2–Cul3–Rbx1 complex to allow normal Nrf2 activation and repression. J. Cell Sci., 2012, 125(4), 1027-1038.
[http://dx.doi.org/10.1242/jcs.097295] [PMID: 22448038]
[174]
Kaspar, J.W.; Jaiswal, A.K. Tyrosine phosphorylation controls nuclear export of Fyn, allowing Nrf2 activation of cytoprotective gene expression. FASEB J., 2011, 25(3), 1076-1087.
[http://dx.doi.org/10.1096/fj.10-171553] [PMID: 21097520]
[175]
Kaspar, J.W.; Jaiswal, A.K. Antioxidant-induced phosphorylation of tyrosine 486 leads to rapid nuclear export of Bach1 that allows Nrf2 to bind to the antioxidant response element and activate defensive gene expression. J. Biol. Chem., 2010, 285(1), 153-162.
[http://dx.doi.org/10.1074/jbc.M109.040022] [PMID: 19897490]
[176]
Clements, C.M.; McNally, R.S.; Conti, B.J.; Mak, T.W.; Ting, J.P.Y. DJ-1, a cancer and Parkinson’s disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proc. Natl. Acad. Sci., 2006, 103(41), 15091-15096.
[http://dx.doi.org/10.1073/pnas.0607260103] [PMID: 17015834]
[177]
Van Roon-Mom, W.M.C.; Pepers, B.A.; ’t Hoen, P.A.C.; Verwijmeren, C.A.C.M.; Den Dunnen, J.T.; Dorsman, J.C.; Van Ommen, G.B. Mutant huntingtin activates Nrf2-responsive genes and impairs dopamine synthesis in a PC12 model of Huntington’s disease. BMC Mol. Biol., 2008, 9(1), 84.
[http://dx.doi.org/10.1186/1471-2199-9-84] [PMID: 18844975]
[178]
Rowley, S.; Patel, M. Mitochondrial involvement and oxidative stress in temporal lobe epilepsy. Free Radic. Biol. Med., 2013, 62, 121-131.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.02.002] [PMID: 23411150]
[179]
Wang, W.; Wu, Y.; Zhang, G.; Fang, H.; Wang, H.; Zang, H.; Xie, T.; Wang, W. Activation of Nrf2-ARE signal pathway protects the brain from damage induced by epileptic seizure. Brain Res., 2014, 1544, 54-61.
[http://dx.doi.org/10.1016/j.brainres.2013.12.004] [PMID: 24333359]
[180]
Patel, M. Nrf2 to the rescue. Epilepsy Curr., 2015, 15(1), 39-40.
[http://dx.doi.org/10.5698/1535-7597-15.1.39] [PMID: 25678888]
[181]
Milder, J.; Patel, M. Modulation of oxidative stress and mitochondrial function by the ketogenic diet. Epilepsy Res., 2012, 100(3), 295-303.
[http://dx.doi.org/10.1016/j.eplepsyres.2011.09.021] [PMID: 22078747]
[182]
Lozano, R.; Naghavi, M.; Foreman, K.; Lim, S.; Shibuya, K.; Aboyans, V.; Abraham, J.; Adair, T.; Aggarwal, R.; Ahn, S.Y.; AlMazroa, M.A.; Alvarado, M.; Anderson, H.R.; Anderson, L.M.; Andrews, K.G.; Atkinson, C.; Baddour, L.M.; Barker-Collo, S.; Bartels, D.H.; Bell, M.L.; Benjamin, E.J.; Bennett, D.; Bhalla, K.; Bikbov, B.; Abdulhak, A.B.; Birbeck, G.; Blyth, F.; Bolliger, I.; Boufous, S.; Bucello, C.; Burch, M.; Burney, P.; Carapetis, J.; Chen, H.; Chou, D.; Chugh, S.S.; Coffeng, L.E.; Colan, S.D.; Colquhoun, S.; Colson, K.E.; Condon, J.; Connor, M.D.; Cooper, L.T.; Corriere, M.; Cortinovis, M.; de Vaccaro, K.C.; Couser, W.; Cowie, B.C.; Criqui, M.H.; Cross, M.; Dabhadkar, K.C.; Dahodwala, N.; De Leo, D.; Degenhardt, L.; Delossantos, A.; Denenberg, J.; Des Jarlais, D.C.; Dharmaratne, S.D.; Dorsey, E.R.; Driscoll, T.; Duber, H.; Ebel, B.; Erwin, P.J.; Espindola, P.; Ezzati, M.; Feigin, V.; Flaxman, A.D.; Forouzanfar, M.H.; Fowkes, F.G.R.; Franklin, R.; Fransen, M.; Freeman, M.K.; Gabriel, S.E.; Gakidou, E.; Gaspari, F.; Gillum, R.F.; Gonzalez-Medina, D.; Halasa, Y.A.; Haring, D.; Harrison, J.E.; Havmoeller, R.; Hay, R.J.; Hoen, B.; Hotez, P.J.; Hoy, D.; Jacobsen, K.H.; James, S.L.; Jasrasaria, R.; Jayaraman, S.; Johns, N.; Karthikeyan, G.; Kassebaum, N.; Keren, A.; Khoo, J-P.; Knowlton, L.M.; Kobusingye, O.; Koranteng, A.; Krishnamurthi, R.; Lipnick, M.; Lipshultz, S.E.; Ohno, S.L.; Mabweijano, J.; MacIntyre, M.F.; Mallinger, L.; March, L.; Marks, G.B.; Marks, R.; Matsumori, A.; Matzopoulos, R.; Mayosi, B.M.; McAnulty, J.H.; McDermott, M.M.; McGrath, J.; Memish, Z.A.; Mensah, G.A.; Merriman, T.R.; Michaud, C.; Miller, M.; Miller, T.R.; Mock, C.; Mocumbi, A.O.; Mokdad, A.A.; Moran, A.; Mulholland, K.; Nair, M.N.; Naldi, L.; Narayan, K.M.V.; Nasseri, K.; Norman, P.; O’Donnell, M.; Omer, S.B.; Ortblad, K.; Osborne, R.; Ozgediz, D.; Pahari, B.; Pandian, J.D.; Rivero, A.P.; Padilla, R.P.; Perez-Ruiz, F.; Perico, N.; Phillips, D.; Pierce, K.; Pope, C.A., III; Porrini, E.; Pourmalek, F.; Raju, M.; Ranganathan, D.; Rehm, J.T.; Rein, D.B.; Remuzzi, G.; Rivara, F.P.; Roberts, T.; De León, F.R.; Rosenfeld, L.C.; Rushton, L.; Sacco, R.L.; Salomon, J.A.; Sampson, U.; Sanman, E.; Schwebel, D.C.; Segui-Gomez, M.; Shepard, D.S.; Singh, D.; Singleton, J.; Sliwa, K.; Smith, E.; Steer, A.; Taylor, J.A.; Thomas, B.; Tleyjeh, I.M.; Towbin, J.A.; Truelsen, T.; Undurraga, E.A.; Venketasubramanian, N.; Vijayakumar, L.; Vos, T.; Wagner, G.R.; Wang, M.; Wang, W.; Watt, K.; Weinstock, M.A.; Weintraub, R.; Wilkinson, J.D.; Woolf, A.D.; Wulf, S.; Yeh, P.H.; Yip, P.; Zabetian, A.; Zheng, Z.J.; Lopez, A.D.; Murray, C.J.L. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: A systematic analysis for the global burden of disease study 2010. Lancet, 2012, 380(9859), 2095-2128.
[http://dx.doi.org/10.1016/S0140-6736(12)61728-0] [PMID: 23245604]
[183]
Murray, C.J.L.; Vos, T.; Lozano, R.; Naghavi, M.; Flaxman, A.D.; Michaud, C.; Ezzati, M.; Shibuya, K.; Salomon, J.A.; Abdalla, S.; Aboyans, V.; Abraham, J.; Ackerman, I.; Aggarwal, R.; Ahn, S.Y.; Ali, M.K.; AlMazroa, M.A.; Alvarado, M.; Anderson, H.R.; Anderson, L.M.; Andrews, K.G.; Atkinson, C.; Baddour, L.M.; Bahalim, A.N.; Barker-Collo, S.; Barrero, L.H.; Bartels, D.H.; Basáñez, M-G.; Baxter, A.; Bell, M.L.; Benjamin, E.J.; Bennett, D.; Bernabé, E.; Bhalla, K.; Bhandari, B.; Bikbov, B.; Abdulhak, A.B.; Birbeck, G.; Black, J.A.; Blencowe, H.; Blore, J.D.; Blyth, F.; Bolliger, I.; Bonaventure, A.; Boufous, S.; Bourne, R.; Boussinesq, M.; Braithwaite, T.; Brayne, C.; Bridgett, L.; Brooker, S.; Brooks, P.; Brugha, T.S.; Bryan-Hancock, C.; Bucello, C.; Buchbinder, R.; Buckle, G.; Budke, C.M.; Burch, M.; Burney, P.; Burstein, R.; Calabria, B.; Campbell, B.; Canter, C.E.; Carabin, H.; Carapetis, J.; Carmona, L.; Cella, C.; Charlson, F.; Chen, H.; Cheng, A.T-A.; Chou, D.; Chugh, S.S.; Coffeng, L.E.; Colan, S.D.; Colquhoun, S.; Colson, K.E.; Condon, J.; Connor, M.D.; Cooper, L.T.; Corriere, M.; Cortinovis, M.; de Vaccaro, K.C.; Couser, W.; Cowie, B.C.; Criqui, M.H.; Cross, M.; Dabhadkar, K.C.; Dahiya, M.; Dahodwala, N.; Damsere-Derry, J.; Danaei, G.; Davis, A.; Leo, D.D.; Degenhardt, L.; Dellavalle, R.; Delossantos, A.; Denenberg, J.; Derrett, S.; Des Jarlais, D.C.; Dharmaratne, S.D.; Dherani, M.; Diaz-Torne, C.; Dolk, H.; Dorsey, E.R.; Driscoll, T.; Duber, H.; Ebel, B.; Edmond, K.; Elbaz, A.; Ali, S.E.; Erskine, H.; Erwin, P.J.; Espindola, P.; Ewoigbokhan, S.E.; Farzadfar, F.; Feigin, V.; Felson, D.T.; Ferrari, A.; Ferri, C.P.; Fèvre, E.M.; Finucane, M.M.; Flaxman, S.; Flood, L.; Foreman, K.; Forouzanfar, M.H.; Fowkes, F.G.R.; Fransen, M.; Freeman, M.K.; Gabbe, B.J.; Gabriel, S.E.; Gakidou, E.; Ganatra, H.A.; Garcia, B.; Gaspari, F.; Gillum, R.F.; Gmel, G.; Gonzalez-Medina, D.; Gosselin, R.; Grainger, R.; Grant, B.; Groeger, J.; Guillemin, F.; Gunnell, D.; Gupta, R.; Haagsma, J.; Hagan, H.; Halasa, Y.A.; Hall, W.; Haring, D.; Haro, J.M.; Harrison, J.E.; Havmoeller, R.; Hay, R.J.; Higashi, H.; Hill, C.; Hoen, B.; Hoffman, H.; Hotez, P.J.; Hoy, D.; Huang, J.J.; Ibeanusi, S.E.; Jacobsen, K.H.; James, S.L.; Jarvis, D.; Jasrasaria, R.; Jayaraman, S.; Johns, N.; Jonas, J.B.; Karthikeyan, G.; Kassebaum, N.; Kawakami, N.; Keren, A.; Khoo, J-P.; King, C.H.; Knowlton, L.M.; Kobusingye, O.; Koranteng, A.; Krishnamurthi, R.; Laden, F.; Lalloo, R.; Laslett, L.L.; Lathlean, T.; Leasher, J.L.; Lee, Y.Y.; Leigh, J.; Levinson, D.; Lim, S.S.; Limb, E.; Lin, J.K.; Lipnick, M.; Lipshultz, S.E.; Liu, W.; Loane, M.; Ohno, S.L.; Lyons, R.; Mabweijano, J.; MacIntyre, M.F.; Malekzadeh, R.; Mallinger, L.; Manivannan, S.; Marcenes, W.; March, L.; Margolis, D.J.; Marks, G.B.; Marks, R.; Matsumori, A.; Matzopoulos, R.; Mayosi, B.M.; McAnulty, J.H.; McDermott, M.M.; McGill, N.; McGrath, J.; Medina-Mora, M.E.; Meltzer, M.; Memish, Z.A.; Mensah, G.A.; Merriman, T.R.; Meyer, A.C.; Miglioli, V.; Miller, M.; Miller, T.R.; Mitchell, P.B.; Mock, C.; Mocumbi, A.O.; Moffitt, T.E.; Mokdad, A.A.; Monasta, L.; Montico, M.; Moradi-Lakeh, M.; Moran, A.; Morawska, L.; Mori, R.; Murdoch, M.E.; Mwaniki, M.K.; Naidoo, K.; Nair, M.N.; Naldi, L.; Narayan, K.M.V.; Nelson, P.K.; Nelson, R.G.; Nevitt, M.C.; Newton, C.R.; Nolte, S.; Norman, P.; Norman, R.; O’Donnell, M.; O’Hanlon, S.; Olives, C.; Omer, S.B.; Ortblad, K.; Osborne, R.; Ozgediz, D.; Page, A.; Pahari, B.; Pandian, J.D.; Rivero, A.P.; Patten, S.B.; Pearce, N.; Padilla, R.P.; Perez-Ruiz, F.; Perico, N.; Pesudovs, K.; Phillips, D.; Phillips, M.R.; Pierce, K.; Pion, S.; Polanczyk, G.V.; Polinder, S.; Pope, C.A., III; Popova, S.; Porrini, E.; Pourmalek, F.; Prince, M.; Pullan, R.L.; Ramaiah, K.D.; Ranganathan, D.; Razavi, H.; Regan, M.; Rehm, J.T.; Rein, D.B.; Remuzzi, G.; Richardson, K.; Rivara, F.P.; Roberts, T.; Robinson, C.; De Leòn, F.R.; Ronfani, L.; Room, R.; Rosenfeld, L.C.; Rushton, L.; Sacco, R.L.; Saha, S.; Sampson, U.; Sanchez-Riera, L.; Sanman, E.; Schwebel, D.C.; Scott, J.G.; Segui-Gomez, M.; Shahraz, S.; Shepard, D.S.; Shin, H.; Shivakoti, R.; Silberberg, D.; Singh, D.; Singh, G.M.; Singh, J.A.; Singleton, J.; Sleet, D.A.; Sliwa, K.; Smith, E.; Smith, J.L.; Stapelberg, N.J.C.; Steer, A.; Steiner, T.; Stolk, W.A.; Stovner, L.J.; Sudfeld, C.; Syed, S.; Tamburlini, G.; Tavakkoli, M.; Taylor, H.R.; Taylor, J.A.; Taylor, W.J.; Thomas, B.; Thomson, W.M.; Thurston, G.D.; Tleyjeh, I.M.; Tonelli, M.; Towbin, J.A.; Truelsen, T.; Tsilimbaris, M.K.; Ubeda, C.; Undurraga, E.A.; Van Der Werf, M.J.; Van Os, J.; Vavilala, M.S.; Venketasubramanian, N.; Wang, M.; Wang, W.; Watt, K.; Weatherall, D.J.; Weinstock, M.A.; Weintraub, R.; Weisskopf, M.G.; Weissman, M.M.; White, R.A.; Whiteford, H.; Wiebe, N.; Wiersma, S.T.; Wilkinson, J.D.; Williams, H.C.; Williams, S.R.M.; Witt, E.; Wolfe, F.; Woolf, A.D.; Wulf, S.; Yeh, P-H.; Zaidi, A.K.M.; Zheng, Z-J.; Zonies, D.; Lopez, A.D. Disability-Adjusted Life Years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: A systematic analysis for the global burden of disease study 2010. Lancet, 2012, 380(9859), 2197-2223.
[http://dx.doi.org/10.1016/S0140-6736(12)61689-4] [PMID: 23245608]
[184]
Jauch, E.C.; Saver, J.L.; Adams, H.P., Jr; Bruno, A.; Connors, J.J.B.; Demaerschalk, B.M.; Khatri, P.; McMullan, P.W., Jr; Qureshi, A.I.; Rosenfield, K.; Scott, P.A.; Summers, D.R.; Wang, D.Z.; Wintermark, M.; Yonas, H. Guidelines for the early management of patients with acute ischemic stroke: A guideline for healthcare professionals from the American Heart Association/American stroke association. Stroke, 2013, 44(3), 870-947.
[http://dx.doi.org/10.1161/STR.0b013e318284056a] [PMID: 23370205]
[185]
Ding, Y.; Ren, D.; Xu, H.; Liu, W.; Liu, T.; Li, L.; Li, J.; Li, Y.; Wen, A. Antioxidant and pro-angiogenic effects of corilagin in rat cerebral ischemia via Nrf2 activation. Oncotarget, 2017, 8(70), 114816-114828.
[http://dx.doi.org/10.18632/oncotarget.22023] [PMID: 29383122]
[186]
Lo, E.H.; Dalkara, T.; Moskowitz, M.A. Mechanisms, challenges and opportunities in stroke. Nat. Rev. Neurosci., 2003, 4(5), 399-414.
[http://dx.doi.org/10.1038/nrn1106] [PMID: 12728267]
[187]
Shih, A.Y.; Li, P.; Murphy, T.H. A small-molecule-inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J. Neurosci., 2005, 25(44), 10321-10335. [b]
[http://dx.doi.org/10.1523/JNEUROSCI.4014-05.2005] [PMID: 16267240]
[188]
Li, L.; Zhang, X.; Cui, L.; Wang, L.; Liu, H.; Ji, H.; Du, Y. Ursolic acid promotes the neuroprotection by activating Nrf2 pathway after cerebral ischemia in mice. Brain Res., 2013, 1497, 32-39.
[http://dx.doi.org/10.1016/j.brainres.2012.12.032] [PMID: 23276496]
[189]
Kaisar, M.A.; Villalba, H.; Prasad, S.; Liles, T.; Sifat, A.E.; Sajja, R.K.; Abbruscato, T.J.; Cucullo, L. Offsetting the impact of smoking and e-cigarette vaping on the cerebrovascular system and stroke injury: Is Metformin a viable countermeasure? Redox Biol., 2017, 13, 353-362.
[http://dx.doi.org/10.1016/j.redox.2017.06.006] [PMID: 28646795]
[190]
Zhao, J.; Moore, A.N.; Redell, J.B.; Dash, P.K. Enhancing expression of Nrf2-driven genes protects the blood brain barrier after brain injury. J. Neurosci., 2007, 27(38), 10240-10248.
[http://dx.doi.org/10.1523/JNEUROSCI.1683-07.2007] [PMID: 17881530]
[191]
Liu, Q.; Jin, Z.; Xu, Z.; Yang, H.; Li, L.; Li, G.; Li, F.; Gu, S.; Zong, S.; Zhou, J.; Cao, L.; Wang, Z.; Xiao, W. Antioxidant effects of ginkgolides and bilobalide against cerebral ischemia injury by activating the Akt/Nrf2 pathway in vitro and in vivo. Cell Stress Chaperones, 2019, 24(2), 441-452.
[http://dx.doi.org/10.1007/s12192-019-00977-1] [PMID: 30815818]
[192]
Daga, M.K. Madhuchhanda; Mishra, T.K.; Mohan, A. Lipid peroxide, beta-carotene and alpha-tocopherol in ischaemic stroke and effect of exogenous vitamin E supplementation on outcome. J. Assoc. Physicians India, 1997, 45(11), 843-846.
[PMID: 11229181]
[193]
Cook, N.R.; Albert, C.M.; Gaziano, J.M.; Zaharris, E.; MacFadyen, J.; Danielson, E.; Buring, J.E.; Manson, J.E. A randomized factorial trial of vitamins C and E and beta carotene in the secondary prevention of cardiovascular events in women: Results from the women’s antioxidant cardiovascular study. Arch. Intern. Med., 2007, 167(15), 1610-1618.
[http://dx.doi.org/10.1001/archinte.167.15.1610] [PMID: 17698683]
[194]
Elshazly, S.M.; Abd El Motteleb, D.M.; Nassar, N.N. The selective 5-LOX inhibitor 11-keto-β-boswellic acid protects against myocardial ischemia reperfusion injury in rats: Involvement of redox and inflammatory cascades. Naunyn Schmiedebergs Arch. Pharmacol., 2013, 386(9), 823-833.
[http://dx.doi.org/10.1007/s00210-013-0885-9] [PMID: 23771412]
[195]
Wu, A.G.; Yong, Y.Y.; Pan, Y.R.; Zhang, L.; Wu, J.M.; Zhang, Y.; Tang, Y.; Wei, J.; Yu, L.; Law, B.Y.K.; Yu, C.L.; Liu, J.; Lan, C.; Xu, R.X.; Zhou, X.G.; Qin, D.L. Targeting Nrf2-mediated oxidative stress response in traumatic brain injury: Therapeutic perspectives of phytochemicals. Oxid. Med. Cell. Longev., 2022, 2022, 1-24.
[http://dx.doi.org/10.1155/2022/1015791] [PMID: 35419162]
[196]
Sharma, R.; Shultz, S.R.; Robinson, M.J.; Belli, A.; Hibbs, M.L.; O’Brien, T.J.; Semple, B.D. Infections after a traumatic brain injury: The complex interplay between the immune and neurological systems. Brain Behav. Immun., 2019, 79, 63-74.
[http://dx.doi.org/10.1016/j.bbi.2019.04.034] [PMID: 31029794]
[197]
Benady, A.; Freidin, D.; Pick, C.G.; Rubovitch, V. GM1 ganglioside prevents axonal regeneration inhibition and cognitive deficits in a mouse model of traumatic brain injury. Sci. Rep., 2018, 8(1), 13340.
[http://dx.doi.org/10.1038/s41598-018-31623-y] [PMID: 30190579]
[198]
Dong, W.; Yang, B.; Wang, L.; Li, B.; Guo, X.; Zhang, M.; Jiang, Z.; Fu, J.; Pi, J.; Guan, D.; Zhao, R. Curcumin plays neuroprotective roles against traumatic brain injury partly via Nrf2 signaling. Toxicol. Appl. Pharmacol., 2018, 346, 28-36.
[http://dx.doi.org/10.1016/j.taap.2018.03.020] [PMID: 29571711]
[199]
Lu, X.Y.; Wang, H.D.; Xu, J.G.; Ding, K.; Li, T. Deletion of Nrf2 exacerbates oxidative stress after traumatic brain injury in mice. Cell. Mol. Neurobiol., 2015, 35(5), 713-721.
[http://dx.doi.org/10.1007/s10571-015-0167-9] [PMID: 25732597]
[200]
Li, F.; Wang, X.; Zhang, Z.; Zhang, X.; Gao, P. Dexmedetomidine attenuates neuroinflammatory-induced apoptosis after traumatic brain injury via Nrf2 signaling pathway. Ann. Clin. Transl. Neurol., 2019, 6(9), 1825-1835.
[http://dx.doi.org/10.1002/acn3.50878] [PMID: 31478596]
[201]
Prasad, S.; Sajja, R.K.; Kaisar, M.A.; Park, J.H.; Villalba, H.; Liles, T.; Abbruscato, T.; Cucullo, L. Role of Nrf2 and protective effects of metformin against tobacco smoke-induced cerebrovascular toxicity. Redox Biol., 2017, 12, 58-69.
[http://dx.doi.org/10.1016/j.redox.2017.02.007] [PMID: 28212524]
[202]
He, Y.; Yan, H.; Ni, H.; Liang, W.; Jin, W. Expression of nuclear factor erythroid 2-related factor 2 following traumatic brain injury in the human brain. Neuroreport, 2019, 30(5), 344-349.
[http://dx.doi.org/10.1097/WNR.0000000000001205] [PMID: 30724850]
[203]
Zhou, Y.; Tian, M.; Wang, H.D.; Gao, C.C.; Zhu, L.; Lin, Y.X.; Fang, J.; Ding, K. Activation of the Nrf2-ARE signal pathway after blast induced traumatic brain injury in mice. Int. J. Neurosci., 2019, 129(8), 801-807.
[http://dx.doi.org/10.1080/00207454.2019.1569652] [PMID: 30648894]
[204]
Sarlette, A.; Krampfl, K.; Grothe, C.; Neuhoff, N.; Dengler, R.; Petri, S. Nuclear erythroid 2-related factor 2-antioxidative response element signaling pathway in motor cortex and spinal cord in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol., 2008, 67(11), 1055-1062.
[http://dx.doi.org/10.1097/NEN.0b013e31818b4906] [PMID: 18957896]
[205]
Shibata, N.; Nagai, R.; Uchida, K.; Horiuchi, S.; Yamada, S.; Hirano, A.; Kawaguchi, M.; Yamamoto, T.; Sasaki, S.; Kobayashi, M. Morphological evidence for lipid peroxidation and protein glycoxidation in spinal cords from sporadic amyotrophic lateral sclerosis patients. Brain Res., 2001, 917(1), 97-104.
[http://dx.doi.org/10.1016/S0006-8993(01)02926-2] [PMID: 11602233]
[206]
Sivandzade, F.; Alqahtani, F.; Cucullo, L. Impact of chronic smoking on traumatic brain microvascular injury: An in vitro study. J. Cell. Mol. Med., 2021, 25(15), 7122-7134.
[http://dx.doi.org/10.1111/jcmm.16741] [PMID: 34160882]