Targeting crosstalk between Nuclear factor (erythroid-derived 2)-like 2 and Nuclear factor kappa beta pathway by Nrf2 activator dimethyl fumarate in epileptogenesis

References

• Fisher RS, Acevedo C, Arzimanoglou A, et al. ILAE Official Report: a practical clinical definition of epilepsy. Epilepsia. 2014;55:475–482. doi:10.1111/epi.12550.
   PubMed Web of Science ®Google Scholar
• Behr C, Goltzene MA, Kosmalski G, et al. Epidemiology of epilepsy. Rev Neurol (Paris). 2016;172:27–36. doi:10.1016/J.NEUROL.2015.11.003.
   PubMed Web of Science ®Google Scholar
• Bromfield EB, Cavazos JE. I. J.I.S.J. Chapter 1. Basic mechanisms underlying seizures and epilepsy. In: An introduction to epilepsy. West Hartford (CT): American Epilepsy Society; 2006. p. 1–26.
   Google Scholar
• Maguire J. Epileptogenesis: More than just the latent period. Epilepsy Curr. 2016;16:31–33. doi:10.5698/1535-7597-16.1.31.
   PubMed Web of Science ®Google Scholar
• Pauletti A, Terrone ÃG, Shekh-ahmad ÃT, et al. Targeting oxidative stress improves disease outcomes in a rat model of acquired epilepsy. Brain. 2017;140:1885–1899. doi:10.1093/brain/awx117.
   Google Scholar
• Treiman DM. GABAergic mechanisms in epilepsy. Epilepsia. 2001;42(Suppl 3):8–12.
   PubMed Web of Science ®Google Scholar
• Martinc B, Grabnar I, Vovk T. The role of reactive species in epileptogenesis and influence of antiepileptic drug therapy on oxidative stress. Curr Neuropharmacol. 2012;10:328–343. doi:10.2174/157015912804143504.
   PubMed Web of Science ®Google Scholar
• Vezzani A, French J, Bartfai T, et al. The role of inflammation in epilepsy. Nat Rev Neurol. 2011;7:31–40. doi:10.1038/nrneurol.2010.178.
   PubMed Web of Science ®Google Scholar
• Cuadrado A. NRF2 in neurodegenerative diseases. Curr Opin Toxicol. 2016;1:46–53. doi:10.1016/J.COTOX.2016.09.004.
   Google Scholar
• Guo Y, Zhang Y, Wen D, et al. The modest impact of transcription factor Nrf2 on the course of disease in an ALS animal model. Lab Invest. 2013;93:825–833. doi:10.1038/labinvest.2013.73.
   PubMed Web of Science ®Google Scholar
• Sandberg M, Patil J, D'Angelo B, et al. NRF2-regulation in brain health and disease: implication of cerebral inflammation. Neuropharmacology. 2014;79:298–306. doi:10.1016/j.neuropharm.2013.11.004.
   PubMed Web of Science ®Google Scholar
• Wardyn JD, Ponsford AH, Sanderson CM. Dissecting molecular cross-talk between Nrf2 and NF-κB response pathways. Biochem Soc Trans. 2015;43:621–626. doi:10.1042/BST20150014.
   PubMed Web of Science ®Google Scholar
• Cuadrado A, Martín-Moldes Z, Ye J, et al. Transcription factors NRF2 and NF-κB are coordinated effectors of the Rho family, GTP-binding protein RAC1 during inflammation. J Biol Chem. 2014;289:15244–15258. doi:10.1074/jbc.M113.540633.
   PubMed Web of Science ®Google Scholar
• Albrecht P, Bouchachia I, Zimmermann C, et al. Effects of dimethyl fumarate on neuroprotection and immunomodulation. J Neuroinflammation. 2012;9:163. doi:10.1186/1742-2094-9-163.
   PubMed Web of Science ®Google Scholar
• Schmidt MM, Dringen R. Fumaric acid diesters deprive cultured primary astrocytes rapidly of glutathione. Neurochem Int. 2010;57:460–467. doi:10.1016/j.neuint.2010.01.006.
   PubMed Web of Science ®Google Scholar
• Kunze R, Urrutia A, Hoffmann A, et al. Dimethyl fumarate attenuates cerebral edema formation by protecting the blood-brain barrier integrity. Exp Neurol. 2015;266:99–111. doi:10.1016/j.expneurol.2015.02.022.
   PubMed Web of Science ®Google Scholar
• Longo D, Fauci A, Kasper D, et al. Chapter 193, Seizures and epilepsy. In: Longo D, Fauci A, Kasper D, et al. , editors. Harrison's Manual of Internal Medicine. 18th ed. New York (NY): McGraw-Hill Companies, Inc.; 2013. p. 1199–1212.
   Google Scholar
• Mazzuferi M, Kumar G, van Eyll J, et al. Nrf2 defense pathway: experimental evidence for its protective role in epilepsy. Ann Neurol. 2013;74:560–568. doi:10.1002/ana.23940.
   PubMed Web of Science ®Google Scholar
• Carmona-Aparicio L, Pérez-Cruz C, Zavala-Tecuapetla C, et al. Overview of Nrf2 as therapeutic target in epilepsy. Int J Mol Sci. 2015;16:18348–18367. doi:10.3390/ijms160818348.
   PubMed Web of Science ®Google Scholar
• Chodobski A, Zink BJ, Szmydynger-Chodobska J. Blood-brain barrier pathophysiology in traumatic brain injury. Transl Stroke Res. 2011;2:492–516. doi:10.1007/s12975-011-0125-x.
   PubMed Web of Science ®Google Scholar
• Dumuis A, Sebben M, Haynes L, et al. NMDA receptors activate the arachidonic acid cascade system in striatal neurons. Nature. 1988;336:68–70. doi:10.1038/336068a0.
   PubMed Web of Science ®Google Scholar
• Mertsch K, Blasig I, Grune T. 4-Hydroxynonenal impairs the permeability of an in vitro rat blood–brain barrier. Neuroscience Letters. 2001;314:135–138. doi:10.1016/S0304-3940(01)02299-6.
   PubMed Web of Science ®Google Scholar
• Rahal A, Kumar A, Singh V, et al. Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int. 2014; 2014:1–19. doi:10.1155/2014/761264.
   Web of Science ®Google Scholar
• Uttara B, Singh AV, Zamboni P, et al. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol. 2009;7:65–74. doi:10.2174/157015909787602823.
   PubMed Web of Science ®Google Scholar
• Braughler JM, Hall ED. Central nervous system trauma and stroke. I. Biochemical considerations for oxygen radical formation and lipid peroxidation. Free Radic Biol Med. 1989;6:289–301. doi:10.1016/0891-5849(89)90056-7.
   PubMed Web of Science ®Google Scholar
• Oh SM, Betz AL. Interaction between free radicals and excitatory amino acids in the formation of ischemic brain edema in rats. Stroke. 1991;22:915–921.
   PubMed Web of Science ®Google Scholar
• Waldbaum S, Patel M. Mitochondrial dysfunction and oxidative stress: a contributing link to acquired epilepsy? J Bioenerg Biomembr. 2010;42:449–455. doi:10.1007/s10863-010-9320-9.
   PubMed Web of Science ®Google Scholar
• Wang W, Wang WP, Zhang GL, et al. Activation of Nrf2-ARE signal pathway in hippocampus of amygdala kindling rats. Neurosci Lett. 2013;543:58–63. doi:10.1016/j.neulet.2013.03.038.
   PubMed Web of Science ®Google Scholar
• Ramsey CP, Glass CA, Montgomery MB, et al. Expression of Nrf2 in neurodegenrative disease. J Neuropathol Exp Neurol. NIHpublic access. 2008;66:75–85.
   Google Scholar
• Ellrichmann G, Petrasch-Parwez E, Lee DH, et al. Efficacy of fumaric acid esters in the R6/2 and YAC128 models of huntington's disease. PLoS One. 2011;6:1–11. doi:10.1371/journal.pone.0016172.
   Web of Science ®Google Scholar
• Löscher W, Brandt C. Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol Rev. 2010;62:668–700. doi:10.1124/pr.110.003046.668.
   PubMed Web of Science ®Google Scholar
• Sun Z, Wu T, Zhao F, et al. KPNA6 (Importin a7)-mediated nuclear import of Keap1 represses the Nrf2-dependent antioxidant response. Mol Cell Biol. 2011;31:1800–1811. doi:10.1128/MCB.05036-11.
   PubMed Web of Science ®Google Scholar
• Linker RA, Lee DH, Ryan S, et al. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain. 2011;134:678–692. doi:10.1093/brain/awq386.
   PubMed Web of Science ®Google Scholar
• Becher B, Prat A, Antel JP. Brain-immune connection: immuno-regulatory properties of CNS-resident cells. Glia. 2000;29:293–304.
   PubMed Web of Science ®Google Scholar
• Walker L, Sills GJ. Inflammation and epilepsy: the foundations for a new therapeutic approach in epilepsy? Epilepsy Curr. 2012;12:8–12. doi:10.5698/1535-7511-12.1.8.
   PubMed Web of Science ®Google Scholar
• Mattson MP. NF-kB in the survival and plasticity of neurons. Neurochem Res. 2005;30:883–893. doi:10.1007/s11064-005-6961-x.
   PubMed Web of Science ®Google Scholar
• O'Mahony A, Raber J, Montano M, et al. NF-κB/Rel regulates inhibitory and excitatory neuronal function and synaptic plasticity. Mol Cell Biol. 2006;26:7283–7298. doi:10.1128/MCB.00510-06.
   PubMed Web of Science ®Google Scholar
• Latimer M, Ernst MK, Dunn LL, et al. The N-terminal domain of I kappa B alpha masks the nuclear localization signal of p50 and c-Rel homodimers. Mol Cell Biol. 1998;18:2640–2649. doi:10.1128/MCB.18.5.2640.
   PubMed Web of Science ®Google Scholar
• Lubin FD, Ren Y, Xu X, et al. Nuclear factor-κB regulates seizure threshold and gene transcription following convulsant stimulation. J Neurochem. 2007;103:1381–1395. doi:10.1111/j.1471-4159.2007.04863.x.
   PubMed Web of Science ®Google Scholar
• Yu N, Di Q, Liu H, et al. Nuclear factor-kappa B activity regulates brain expression of P-glycoprotein in the kainic acid-induced seizure rats. Mediators Inflamm. 2011;670613. doi:10.1155/2011/670613.
   PubMed Web of Science ®Google Scholar
• Rong Y, Baudry M. Seizure activity results in a rapid induction of Nuclear factor-κB in adult but not juvenile rat limbic structures. J Neurochem. 2002;67:662–668. doi:10.1046/j.1471-4159.1996.67020662.x.
   Google Scholar
• Zhang H, Chu X, Fu T, et al. Inhibitory effect of interleukin-1β antibody for NLRP3 inflammasome on epilepsy rat model. Int J Clin Exp Pathol. 2017;10:1847–1853.
   Web of Science ®Google Scholar
• Zhang JM, Hong Y, Yan W, et al. The role of Nrf2 signaling in the regulation of antioxidants and detoxifying enzymes after traumatic brain injury in rats and mice. Acta Pharmacol Sin. 2010;31:1421–1430. doi:10.1038/aps.2010.101.
   PubMed Web of Science ®Google Scholar
• Pan H, Wang H, Wang X, et al. The absence of Nrf2 enhances NF-κB-dependent inflammation following scratch injury in mouse primary cultured astrocytes. Mediators Inflamm. 2012;2012:1–9. doi:10.1155/2012/217580.
   Web of Science ®Google Scholar
• Thimmulappa RK, Lee H, Rangasamy T, et al. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest. 2006;116:984–995. doi:10.1172/JCI25790.984.
   PubMed Web of Science ®Google Scholar
• Soares MP, Seldon MP, Gregoire IP, et al. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol. 2004;172:3553–3563. doi:10.4049/JIMMUNOL.172.6.3553.
   PubMed Web of Science ®Google Scholar
• Kim JE, You DJ, Lee C, et al. Suppression of NF-κB signaling by Keap1 regulation of IKKβ activity through autophagic degradation and inhibition of phosphorylation. Cell Signal. 2010;22:1645–1654. doi:10.1016/j.cellsig.2010.06.004.
   PubMed Web of Science ®Google Scholar
• Liu GH, Qu J, Shen X. NF-κB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochim Biophys Acta - Mol Cell Res. 2008;1783:713–727. doi:10.1016/j.bbamcr.2008.01.002.
   PubMed Web of Science ®Google Scholar
• Kraft AD, Lee JM, Johnson DA, et al. Neuronal sensitivity to kainic acid is dependent on the Nrf2-mediated actions of the antioxidant response element. J Neurochem. 2006;98:1852–1865. doi:10.1111/j.1471-4159.2006.04019.x.
   PubMed Web of Science ®Google Scholar
• Xu C, Shen G, Chen C, et al. Suppression of NF-kB and NF-kB-regulated gene expression by sulforaphane and PEITC through IkBa, IKK pathway in human prostate cancer PC-3 cells. Oncogene. 2005;24:4486–4495. doi:10.1038/sj.onc.1208656.
   PubMed Web of Science ®Google Scholar
• Keum Y-S, Owuor ED, Kim B-R, et al. Involvement of Nrf2 and JNK1 in the activation of antioxidant responsive element (ARE) by chemopreventive agent phenethyl isothiocyanate (PEITC). Pharm Res. 2003;20:1351–1356.
   PubMed Web of Science ®Google Scholar
• Loewe R, Holnthoner W, Groger M, et al. Dimethylfumarate inhibits TNF-induced nuclear entry of NF- B/p65 in human endothelial cells. J Immunol. 2002;168:4781–4787. doi:10.4049/jimmunol.168.9.4781.
   PubMed Web of Science ®Google Scholar
• Kastrati I, Siklos MA, Calderon-gierszal EL, et al. Dimethyl fumarate inhibits the nuclear factor κB pathway in breast cancer cells by covalent modification of p65. J Biol Chem. 2015;291:3639–3647. doi:10.1074/jbc.M115.679704.
   PubMed Web of Science ®Google Scholar
• Vego H, Sand KL, Høglund RA, et al. Monomethyl fumarate augments NK cell lysis of tumor cells through degranulation and the upregulation of NKp46 and CD107a. Cell Mol Immunol. 2016;13:57–64. doi:10.1038/cmi.2014.114.
   PubMed Web of Science ®Google Scholar
• Ockenfels HM, Schultewolter T, Ockenfels G, et al. The antipsoriatic agent dimethylfumarate immunomodulates T-cell cytokine secretion and inhibits cytokines of the psoriatic cytokine network. Br J Dermatol. 1998;139:390–395. doi:10.1046/j.1365-2133.1998.02400.x.
   PubMed Web of Science ®Google Scholar
• Al-Jaderi Z, Maghazachi AA. Utilization of dimethyl fumarate and related molecules for treatment of multiple sclerosis, cancer, and other diseases. Front Immunol. 2016;7:1–8. doi:10.3389/fimmu.2016.00278.
   PubMed Web of Science ®Google Scholar
• Calkins MJ, Johnson DA, Townsend JA, et al. The Nrf2 /ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Signal. 2009;11:497–508. doi:10.1089/ars.2008.2242.
   PubMed Web of Science ®Google Scholar
• Schulze-Topphoff U, Varrin-Doyer M, Pekarek K, et al. Dimethyl fumarate treatment induces adaptive and innate immune modulation independent of Nrf2. Proc Natl Acad Sci USA. 2016;113:4777–4782. doi:10.1073/pnas.1603907113.
   PubMed Web of Science ®Google Scholar
• Chen H, Assmann JC, Krenz A, et al. Hydroxycarboxylic acid receptor 2 mediates dimethyl fumarate's protective effect in EAE. J Clin Invest. 2014;124:2188–2192. doi:10.1172/JCI72151.
   PubMed Web of Science ®Google Scholar
• Jo C, Gundemir S, Pritchard S, et al. Nrf2 reduces levels of phosphorylated tau protein by inducing autophagy adaptor protein NDP52. Nat Commun. 2014;5:3496. doi:10.1038/ncomms4496.
   Web of Science ®Google Scholar
• Ameen D, Michniak-Kohn B. Transdermal delivery of dimethyl fumarate for Alzheimer's disease: effect of penetration enhancers. Int J Pharm. 2017;529:465–473. doi:10.1016/j.ijpharm.2017.07.031.
   PubMed Web of Science ®Google Scholar
• Ahuja M, Ammal Kaidery N, Yang L, et al. 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;36:6332–6351. doi:10.1523/JNEUROSCI.0426-16.2016.
   PubMed Web of Science ®Google Scholar
• de Paula CZ, Gonçalves BDC, Vieira LB. An overview of potential targets for treating amyotrophic lateral sclerosis and Huntington's disease. Biomed Res Int. 2015;2015:198612. doi:10.1155/2015/198612.
   PubMed Web of Science ®Google Scholar