Role of oxidative stress in refractory epilepsy: Evidence in patients and experimental models

International Journal of Molecular Sciences

Volumn 14, Issue 1, 2013, Pages 1455-1476

  Cardenas Rodriguez, Noemi ^a   Huerta Gertrudis, Bernardino ^a   Rivera Espinosa, Liliana ^a   Montesinos Correa, Hortencia ^a   Bandala, Cindy ^b   Carmona Aparicio, Liliana ^a   Coballase Urrutia, Elvia ^a  

^a INSTITUTO NACIONAL DE PEDIATRÍA   (Mexico)

^b National Institute of Rehabilitation   (Mexico)

Author keywords

Free radicals; Oxidative stress; Pharmacoresistant epilepsy; Refractory epilepsy

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; ASCORBIC ACID; BILIRUBIN; CATALASE; CATHEPSIN B; COPPER ZINC SUPEROXIDE DISMUTASE; CYSTATIN B; DNA; FREE RADICAL; GLUTATHIONE PEROXIDASE; HYDROPEROXIDE; HYDROXYL RADICAL; MANGANESE SUPEROXIDE DISMUTASE; MIDAZOLAM; MULTIDRUG RESISTANCE PROTEIN; OXYGEN; PEROXY RADICAL; PHENOBARBITAL; PHENYTOIN; PROPOFOL; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; RETINOL; SUPEROXIDE; THIAMYLAL; THIOPENTAL; UNINDEXED DRUG; URIC ACID; VALPROIC ACID; ANTICONVULSIVE AGENT; ANTIOXIDANT;

ADJUVANT THERAPY; ANTIOXIDANT ACTIVITY; ATELECTASIS; BIOCHEMISTRY; BLOOD BRAIN BARRIER; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN SURGERY; DISEASE ASSOCIATION; DNA DAMAGE; DRUG MEGADOSE; DRUG PENETRATION; DRUG RESEARCH; DRUG TREATMENT FAILURE; DRUG WITHDRAWAL; ELECTROENCEPHALOGRAPHY; EPILEPSY; FENTON REACTION; HUMAN; HYPOTENSION; KETOGENIC DIET; KIDNEY FAILURE; LEUKOPENIA; LIVER INJURY; MULTIDRUG RESISTANCE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PROTEIN EXPRESSION; QUALITY OF LIFE; REVIEW; THROMBOPHLEBITIS; ANIMAL; DISEASE MODEL; DRUG RESISTANCE; METABOLISM;

ANIMALS; ANTICONVULSANTS; ANTIOXIDANTS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE; EPILEPSY; HUMANS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84877084552     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14011455     Document Type: Review

References (156)

1. Valko, M.; Rhodes, C.; Moncol, J.; Izakovic, M.; Mazur, M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 2006, 160, 1-40.
2. Halliwell, B.; Gutteridge, M. Free Radicals in Biology and Medicine, 3rd ed.; Oxford University Press: New York, NY, USA, 1999.
3. Valko, M.; Izakovic, M.; Mazur, M.; Rhodes, C.; Telser, J. Role of oxygen radicals in DNA damage and cancer incidence. Mol. Cell. Biochem. 2004, 266, 37-56.
4. Inoue, M.; Sato, E.; Nishikawa, M.; Park, A.; Kira, Y.; Imada, I.; Utsumi, K. Mitochondrial generation of reactive oxygen species and its role in aerobic life. Curr. Med. Chem. 2003, 10, 2495-2505.
5. Winterbourn, C. Superoxide as an intracellular radical sink. Free Radic. Biol. Med. 1993, 14, 85-90.
6. Bae, Y.S.; Oh, H.; Rhee, S.G.; Yoo, Y.D. Regulation of reactive oxygen species generation in cell signaling. Mol. Cells. 2011, 32, 491-509.
7. Vandelle, E.; Delledonne, M. Peroxynitrite formation and function in plants. Plant. Sci. 2011, 181, 534-539.
8. Knowles, R.; Moncada, S. Nitric oxide synthases in mammals. Biochem. J. 1994, 298, 249-258.
9. Alderton, W.; Cooper, C.; Knowles, R. Nitric oxide synthases: Structure, function and inhibition. Biochem. J. 2001, 357, 593-615.
10. Van der Veen, B.S.; de Winther, M.P.; Heeringa, P. Myeloperoxidase: Molecular mechanisms of action and their relevance to human health and disease. Antioxid. Redox Signal. 2009, 11, 2899-2937.
11. Burke, K.E.; Wei, H. Synergistic damage by UVA radiation and pollutants. Toxicol. Ind. Health 2009, 25, 219-224.
12. Ohta, H.; Adachi, T.; Hirano, K. Internalization of human extracellular-superoxide dismutase by bovine aortic endotelial cells. Free Radic. Biol. Med. 1994, 16, 501-507.
13. Marklund, S.; Westman, N.; Lundgren, E.; Ross, G. Copper-and zinc-containing superooxide dismutase, manganese-containing superoxide dismutase, catalase, and glutathione peroxidase in normal and neoplastic human cell lines and normal human tissues. Cancer Res. 1982, 42, 1955-1961.
14. Cheng, L.; Kellog, E.; Packer, L. Photoinactivation of catalase. Photochem. Photobiol. 1981, 34, 125-129.
15. Savaskan, N.E.; Ufer, C.; Kühn, H.; Borchert, A. Molecular biology of glutathione peroxidase 4: From genomic structure to developmental expression and neural function. Biol. Chem. 2007, 388, 1007-1017.
16. Brigelius-Flohe, R. Tissue-Specific functions of individual glutathione peroxidases. Free Radic. Biol. Med. 1999, 27, 951-965.
17. Chu, F.; Esworthy, R.; Doroshow, J. Role of se-dependent glutathione peroxidases in gastrointestinal inflammation and cancer. Free Radic. Biol. Med. 2004, 36, 1481-1495.
18. Comhair, S.; Erzurum, S. The regulation and role of extracellular glutathione peroxidase. Antioxid. Redox Signal 2005, 1, 72-79.
19. Hirotaka, I.; Yasuhito, N. Biological significance of phospholipid hydroperoxide gluathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic. Biol. Med. 2003, 2, 145-169.
20. Untucht-Grau, R.; Schirmer, R.H.; Schirmer, I.; Krauth-Siegel, R.L. Glutathione reductase from human erythrocytes: Amino-Acid sequence of the structurally known FAD-binding domain. Eur. J. Biochem. 1981, 120, 407-419.
21. Harris, D. Regulation of antioxidant enzymes. FASEB J. 1992, 6, 2675-2683.
22. Sharma, R.; Yang, Y.; Sharma, A.; Awasthi, S.; Awasthi, Y. Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stress-mediated apoptosis. Antiox. Redox Signal. 2004, 6, 289-291.
23. Higgins, L.G.; Hayes, J.D. Mechanisms of induction of cytosolic and microsomal glutathione transferase (GST) genes by xenobiotics and pro-inflammatory agents. Drug Metab. Rev. 2011, 43, 92-137.
24. Oakley, A. Glutathione transferases: a structural perspective. Drug Metab. Rev. 2011, 43, 138-151.
25. Collet, J.F.; Messens, J. Structure, function, and mechanism of thioredoxin proteins. Antioxid. Redox Signal. 2010, 13, 1205-1216.
26. Nordberg, J.; Arner, E. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic. Biol. Med. 2001, 31, 1287-1312.
27. Hirotsu, S.; Abe, Y.; Okada, K.; Nagahara, N.; Hori, H.; Nishino, T.; Hakoshima, T. Cristal structure of multifunctional 2-Cys peroxiredoxin heme-binding protein 23 kDa/proliferation-associated gene product. Proc. Natl. Acad. Sci. USA 1999, 96, 12333-12338.
28. Aran, M.; Ferrero, D.S.; Pagano, E.; Wolosiuk, R.A. Typical 2-Cys peroxiredoxins-Modulation by covalent transformations and noncovalent interactions. FEBS J. 2009, 276, 2478-2493.
29. Riccioni, G.; D'Orazio, N.; Salvatore, C.; Franceschelli, S.; Pesce, M.; Speranza, L. Carotenoids and vitamins C and E in the prevention of cardiovascular disease. Int. J. Vitam. Nutr. Res. 2012, 82, 15-26.
30. Da Costa, L.A.; Badawi, A.; El-Sohemy, A. Nutrigenetics and modulation of oxidative stress. Ann. Nutr. Metab. 2012, 60, 27-36.
31. Cos, P.; Ying, L.; Calomme, M.; Hu, J.P.; Cimanga, K.; Van Poel, B.; Pieters, L.; Vlietinck, A.J.; Vanden, B.D. Structure-Activity relationship and classification of flavonoids as inhibitors of xanthine oxidase and superoxide scavengers. J. Nat. Prod. 1998, 61, 71-76.
32. Spencer, J.P. Beyond antioxidants: The cellular and molecular interactions of flavonoids and how these underpin their actions on the brain. Proc. Nutr. Soc. 2010, 69, 244-260.
33. Spencer, J.P. Flavonoids: Modulators of brain function? Br. J. Nutr. 2008, 99, ES60-ES77.
34. Steffen, Y.; Gruber, C.; Schewe, T.; Sies, H. Mono-O-Methylated flavanols and other flavonoids as inhibitors of endothelial NADPH oxidase. Arch. Biochem. Biophys. 2008, 469, 209-219.
35. Park, S.S.; Bae, I.; Lee, Y.J. Flavonoids-Induced accumulation of hypoxia-inducible factor (HIF)-1alpha/2alpha is mediated through chelation of iron. J. Cell. Biochem. 2008, 103, 989-998.
36. Spencer, J.P. Flavonoids and brain health: Multiple effects underpinned by common mechanisms. Genes Nutr. 2009, 4, 243-250.
37. Lai, H.C.; Wu, M.J.; Chen, P.Y.; Sheu, T.T.; Chiu, S.P.; Lin, M.H.; Ho, C.T.; Yen, J.H. Neurotrophic effect of citrus 5-hydroxy-3,6,7,8,3′,4′-hexamethoxyflavone: Promotion of neurite outgrowth via cAMP/PKA/CREB pathway in PC12 cells. PLoS One 2011, 6, e28280.
38. Naseer, M.I.; Ullah, I.; Ullah, N.; Lee, H.Y.; Cheon, E.W.; Chung, J.; Kim, M.O. Neuroprotective effect of vitamin C against PTZ induced apoptotic neurodegeneration in adult rat brain. Pak. J. Pharm. Sci. 2011, 24, 263-268.
39. Floyd, R.; Carney, J. Free radical damage to protein and DNA: Mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann. Neurol. 1992, 32, S22-S27.
40. Kosiakov, K.S. Blood catalase activity in brain tumors during the postoperative period. Vop. Neirokthir. 1975, 6, 41-44.
41. Henchcliffe, C.; Beal, M.F. Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nat. Clin. Pract. Neurol. 2008, 4, 600-609.
42. Wood-Kaczmar, A.; Gandhi, S.; Wood, N.W. Understanding the molecular causes of Parkinson's disease. Trends Mol. Med. 2006, 12, 521-528.
43. Dexter, D.T.; Holley, A.E.; Flitter, W.D.; Slater, T.F.; Wells, F.R.; Daniel, S.E.; Lees, A.J.; Jenner, P.; Marsden, C.D. Increased levels of lipid hydroperoxides in the parkinsonian substantia nigra: An HPLC and ESR study. Mov. Disord. 1994, 9, 92-97.
44. Sanyal, J.; Bandyopadhyay, S.K.; Banerjee, T.K.; Mukherjee, S.C.; Chakraborty, D.P.; Ray, B.C.; Rao, V.R. Plasma levels of lipid peroxides in patients with Parkinson's disease. Eur. Rev. Med. Pharmacol. Sci. 2009, 13, 129-132.
45. Bolner, A.; Pilleri, M.; de Riva, V.; Nordera, G.P. Plasma and urinary HPLC-ED determination of the ratio of 8-OHdG/2-dG in Parkinson's disease. Clin. Lab. 2011, 57, 859-866.
46. Gencer, M.; Dasdemir, S.; Cakmakoglu, B.; Cetinkaya, Y.; Varlibas, F.; Tireli, H.; Kucukali, C.I.; Ozkok, E.; Aydin, M. DNA repair genes in Parkinson's disease. Genet. Test Mol. Biomark. 2012, 16, 504-507.
47. Maetzler, W.; Schmid, S.P.; Wurster, I.; Liepelt, I.; Gaenslen, A.; Gasser, T.; Berg, D. Reduced but not oxidized cerebrospinal fluid glutathione levels are lowered in Lewy body diseases. Mov. Disord. 2011, 26, 176-181.
48. Sofic, E.; Lange, K.W.; Jellinger, K.; Riederer, P. Reduced and oxidized glutathione in the substantia nigra of patients with Parkinson's disease. Neurosci. Lett. 1992, 17, 128-130.
49. Saggu, H.; Cooksey, J.; Dexter, D.; Wells, F.R.; Lees, A.; Jenner, P.; Marsden, C.D. A selective increase in particulate superoxide dismutase activity in parkinsonian substantia nigra. J. Neurochem. 1989, 53, 692-697.
50. Kushleika, J.; Checkoway, H.; Woods, J.S.; Moon, J.D.; Smith-Weller, T.; Franklin, G.M.; Swanson, P.D. Selegiline and lymphocyte superoxide dismutase activities in Parkinson's disease. Ann. Neurol. 1996, 39, 378-381.
51. Tang, S.C.; Lathia, J.D.; Selvaraj, P.K.; Jo, D.G.; Mughal, M.R.; Cheng, A.; Siler, D.A.; Markesbery, W.R.; Arumugam, T.V.; Mattson, M.P. Toll-Like receptor-4 mediates neuronal apoptosis induced by amyloidbeta-peptide and the membrane lipid peroxidation product 4-hydroxynonenal. Exp. Neurol. 2008, 213, 114-121.
52. Esterbauer, H.; Schaur, R.J.; Zollner, H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 1991, 11, 81-128.
53. Markesbery, W.R.; Lovell, M.A. 4-Hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol. Aging 1998, 19, 33-36.
54. Montine, K.S.; Olson, S.J.; Amarnath, V.; Whetsell, W.O.; Graham, D.G., Jr.; Montine, T.J. Immunohistochemical detection of 4-hydroxy-2-nonenal adducts in Alzheimer's disease is associated with inheritance of APOE4. Am. J. Pathol. 1997, 150, 437-443.
55. Maragakis, N.J.; Rothstein, J.D. Glutamate transporters in neurologic disease. Arch. Neurol. 2001, 58, 365-370.
56. Rothstein, J.D. Excitotoxic mechanisms in the pathogenesis of amyotrophic lateral sclerosis. Adv. Neurol. 1995, 68, 7-20.
57. Wood, J.D.; Beaujeux, T.P.; Shaw, P.J. Protein aggregation in motor neurone disorders. Neuropathol. Appl. Neurobiol. 2003, 29, 529-545.
58. Lariviere, R.C.; Julien, J.P. Functions of intermediate filaments in neuronal development and disease. J. Neurobiol. 2004, 58, 131-148.
59. Aga, J.; Durham, H. Relevance of oxidative injury in the pathogenesis of motor neuron diseases. Amyotroph Lateral Scler. Other Motor Neuron. Disord. 2003, 4, 232-242.
60. Xu, Z.; Jung, C.; Higgins, C.; Levine, J.; Kong, J. Mitochondrial degeneration in amyotrophic lateral sclerosis. J. Bioenerg. Biomembr. 2004, 36, 395-399.
61. Benedusi, V.; Martorana, F.; Brambilla, L.; Maggi, A.; Rossi, D. The Peroxisome Proliferator-Activated Receptor γ (PPARγ) controls natural protective mechanisms against lipid peroxidation in Amyotrophic Lateral Sclerosis. J. Biol. Chem. 2012, in press.
62. Cova, E.; Bongioanni, P.; Cereda, C.; Metelli, M.R.; Salvaneschi, L.; Bernuzzi, S.; Guareschi, S.; Rossi, B.; Ceroni, M. Time course of oxidant markers and antioxidant defenses in subgroups of amyotrophic lateral sclerosis patients. Neurochem. Int. 2010, 56, 687-693.
63. Engel, J.J. Concepts of Epilepsy. Epilepsia 1995, 36, S23-S29.
64. Hauser, A.W.; Annegers, F.J.; Kurland, T.L. Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota. Epilepsia 1993, 34, 453-468.
65. Dichter, M.A. Emerging insights into mechanisms of epilepsy: Implications for new anmtiepileptic drug development. Epilepsia 1994, 35, S51-S57.
66. Newton, C.R.; Garcia, H.H. Epilepsy in poor regions of the world. Lancet 2012, 29, 1193-1201.
67. Neligan, A.; Hauser, W.A.; Sander, J.W. The epidemiology of the epilepsies. Handb. Clin. Neurol. 2012, 107, 113-133.
68. Téllez-Zenteno, J.F.; Hernández-Roquillo, L. A review of the epidemiology of temporal lobe epilepsy. Epilepsy Res. Treat. 2012, in press.
69. Berg, A.T. Classification and epilepsy: The future awaits. Epilepsy Curr. 2011, 11, 138-140.
70. Fisher, R.S.; Frost, J. Epilepsy. J. Nucl. Med. 1991, 32, 651-659.
71. Davidson, P.N.; Davidson, K.A. Electroencephalography in the elderly. Neurodiagn. J. 2012, 52, 3-19.
72. Engel, J.J.; Starkman, S. Overview of seizures. Emerg. Med. Clin. North Am. 1994, 12, 895-923.
73. Engel, J.J.; Pedley, A.T. Introduction to the epilepsies. In Epilepsy, A Comprehensive Textbook, 1st ed.; Lippincott-Raven, Ed.; Philadelphia, PA, USA, 1997; pp. 765-772.
74. Annergers, J.F.; Grabow, J.D.; Groover, R.V. Seizures after head trauma: A population study. Neurology 1980, 30, 683-689.
75. ILAE. Commision on classification and terminology of the international league against epilepsy: Proposal for revised classification and electroencephalographic classification of epileptic seizures. Epilepsia 1981, 22, 489-501.
76. ILAE. Commision on classification and termnology of the international league against epilepsy: Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 1989, 30, 389-399.
77. Berg, A.T.; Cross, J.H. Classification of epilepsies and seizures: Historical perspective and future directions. Handb. Clin. Neurol. 2012, 107, 99-111.
78. Cavanna, A.E.; Rickards, H.; Ali, F. What makes a simple partial seizure complex? Epilepsy Behav. 2011, 22, 651-658.
79. Bergamini, L.; Broglia, S.; Riccio, A.; Franchini, V. Favorable results of ACTH therapy in different types of epilepsy resistant to all classical drug therapy (21 cases followed-up for more than 6 months). Riv. Neurol. 1966, 36, 49-62.
80. Falconer, M.A.; Taylor, D.C. Surgical treatment of drug-resistant epilepsy due to mesial temporal sclerosis. Etiology and significance. Arch. Neurol. 1968, 19, 353-361.
81. Brandt, S. Resistant transitory epilepsy in children. Acta Neurol. Scand. 1976, 53, 119-127.
82. Chayasirisobhon, S. The mechanisms of medically refractory temporal lobe epilepsy. Acta Neurol. Taiwan 2009, 18, 155-160.
83. Zambrano, M.T.; Támara, E.C.; Ballestas, J.M.C. Resistencia farmacológica en epilepsia. Acta Neurol. Colomb. 2007, 23, 278-285.
84. Beleza, P. Refractory Epilepsy: A Clinically Oriented Review. Eur. Neurol. 2009, 62, 65-71.
85. Bachelard, H.S.; Thompson, M.F.; Polkey, C.E. Kinetic properties of hexokinase in resected temporal lobes of patients with drug-resistant epilepsy. Epilepsia 1975, 16, 431-437.
86. Zaccara, G.; Galli, A.; Rossi, L.; Zappoli, R.; Zatelli, L.; Amaducci, L. Plasma levels of diphenylhydantoin (DPH) and phenobarbitone (PB) in epileptic patients resistant to drug treatment (author's translation). Riv. Patol. Nerv. Ment. 1977, 98, 363-375.
87. Broeker, H.; Müller, D.; Müller, J.; Walther, H. Serum anticonvulsant levels in therapy-resistant epileptics. Psychiatr. Neurol. Med. Psychol. (Leipz) 1980, 32, 541-549.
88. Alvarez, J.C.S.; Castro, P.J.S.; Fernández, J.M.S. Clinical implications of mechanisms of resistance to antiepileptic drugs. Neurologist 2007, 13, S38-S46.
89. Rambeck, B.; Jürgens, U.H.; May, T.W.; Pannek, H.W.; Behne, F.; Ebner, A.; Gorji, A.; Straub, H.; Speckmann, E.J.; Pohlmann-Eden, B.; Löscher, W. Comparison of brain extracellular fluid, brain tissue, cerebrospinal fluid, and serum concentrations of antiepileptic drugs measured intraoperatively in patients with intractable epilepsy. Epilepsia 2006, 47, 681-694.
90. Höcht, C.; Lazarowski, A.; Gonzalez, N.N.; Auzmendi, J.; Opezzo, J. A; Bramuglia, G.F.; Taira, C.A.; Girardi, E. Nimodipine restores the altered hippocampal phenytoin pharmacokinetics in a refractory epileptic model. Neurosci. Lett. 2007, 413, 168-172.
91. Löscher, W.; Potschka, H. Role of multidrug transporters in pharmacoresistance to antiepileptic drugs. J. Pharmacol. Exp. Ther. 2002, 301, 7-14.
92. Löscher, W. Mechanisms of drug resistance. Epileptic Disord. 2005, 7, S3-S9.
93. Ban, J.J.; Jung, K.H.; Chu, K.; Lee, S.T.; Jeon, D.; Park, K.I.; Moon, H.J.; Kim, H.; Kim, S.; Lee, S.K.; Roh, J.K. Profiles of multidrug resistance protein-1 in the peripheral blood mononuclear cells of patients with refractory epilepsy. PLoS One 2012, 7, e36985.
94. Lazarowski, A.; Czornyj, L. Potential role of multidrug resistant proteins in refractory epilepsy and antiepileptic drugs interactions. Drug Metabol. Drug Interact. 2011, 26, 21-26.
95. Robey, R.W.; Lazarowski, A.; Bates, S.E. P-Glycoprotein-A clinical target in drug-refractory epilepsy? Mol. Pharmacol. 2008, 73, 1343-1346.
96. Volk, H.A.; Löscher, W. Multidrug resistance in epilepsy: Rats with drug-resistant seizures exhibit enhanced brain expression of P-glycoprotein compared with rats with drug-responsive seizures. Brain 2005, 128, 1358-1368.
97. Schmidt, D.; Löscher, W. New developments in antiepileptic drug resistance: An integrative view. Epilepsy Curr. 2009, 9, 47-52.
98. Choi, B.H. Oxygen, antioxidants and brain dysfunction. Yonsei Med. J. 1993, 34, 1-10.
99. Bondy, S.C. The relation of oxidative stress and hyperexcitation to neurological disease. Proc. Soc. Exp. Biol. Med. 1995, 208, 337-345.
100. Dalton, T.; Pazdernik, T.L.; Wagner, J.; Samson, F.; Andrews, G.K. Temporal spatial patterns of expression of metallothionein-I and-III and other stress related genes in rat brain after kainic acid-induced seizures. Neurochem. Int. 1995, 27, 59-71.
101. Ziegler, D.R.; Ribeiro, L.C.; Hagenn, M.; Siqueira, I.R.; Araújo, E.; Torres, I.L.; Gottfried, C.; Netto, C.A.; Gonçalves, C.A. Ketogenic diet increases glutathione peroxidase activity in rat hippocampus. Neurochem. Res. 2003, 28, 1793-1797.
102. Lehtinen, M.K.; Tegelberg, S.; Schipper, H.; Su, H.; Zukor, H.; Manninen, O.; Kopra, O.; Joensuu, T.; Hakala, P.; Bonni, A.; Lehesjoki, A.E. Cystatin B deficiency sensitizes neurons to oxidative stress in progressive myoclonus epilepsy, EPM1. J. Neurosci. 2009, 29, 5910-5915.
103. Ben-Menachem, E.; Kyllerman, M.; Marklund, S. Superoxide dismutase and glutathione peroxidase function in progressive myoclonus epilepsies. Epilepsy Res. 2000, 40, 33-39.
104. Shiihará, T.; Kato, M.; Ichiyama, T.; Takahashi, Y.; Tanuma, N.; Miyata, R.; Hayasaka, K. Acute encephalopathy with refractory status epilepticus: Bilateral mesial temporal and claustral lesions, associated with a peripheral marker of oxidative DNA damage. J. Neurol. Sci. 2006, 250, 159-161.
105. Hayashi, M.; Tanuma, N.; Miyata, R. The involvement of oxidative stress in epilepsy. In Handbook of Free Radicals: Formation, Types and Effects, Kozyrev, D., Slutsky, V., Eds.; Nova Science Publishers: New York, NY, USA, 2010; pp. 305-318.
106. López, J.; González, M.E.; Lorigados, L.; Morales, L.; Riverón, G.; Bauzá, J.Y. Oxidative stress markers in surgically treated patients with refractory epilepsy. Clin. Biochem. 2007, 40, 292-298.
107. Faust, K.; Gehrke, S., Yang, Y.; Yang, L.; Beal, F.; Lu, B. Neuroprotective effects of compounds with antioxidant and anti-inflammatory properties in a Drosophila model of Parkinson's disease. BMC Neurosci. 2009, 10, 109-121.
108. Löscher, W. Animal models of epilepsy for the development of antiepileptogenic and disease-modifying drugs. A comparison of the pharmacology of kindling and post-status epilepticus models of temporal lobe epilepsy. Epilepsy Res. 2002, 50, 105-123.
109. Pitkänen, A. Drug-Mediated neuroprotection and antiepileptogenesis: Animal data. Neurology 2002, 59, S27-S33.
110. Engel, J., Jr.; Wilson, C.; Bragin, A. Advances in understanding the process of epileptogenesis based on patient material: What can the patient tell us? Epilepsia 2003, 44, 60-71.
111. Majores, M.; Schoch, S.; Lie, A.; Becker, A.J. Molecular neuropathology of temporal lobe epilepsy: Complementary approaches in animal models and human disease tissue. Epilepsia 2007, 48, 4-12.
112. Nanjo, F.; Goto, K.; Seto, R.; Suzuki, M.; Sakai, M.; Hara, Y. Scavenging effects of tea catechins and their derivatives on 1,1-diphenyl-2-picrylhydrazyl radical. Free Radic. Biol. Med. 1996, 21, 895-902.
113. Panickar, K.S.; Polansky, M.M.; Anderson, R.A. Green tea polyphenols attenuate glial swelling and mitochondrial dysfunction following oxygen-glucose deprivation in cultures. Nutr. Neurosci. 2009, 12, 105-113.
114. Abdin, A.A.; Hamouda, H.E. Mechanism of the neuroprotective role of coenzyme Q10 with or without L-dopa in rotenone-induced parkinsonism. Neuropharmacology 2008, 55, 1340-1346.
115. Kooncumchoo, P.; Sharma, S.; Porter, J.; Govitrapong, P.; Ebadi, M. Coenzyme Q(10) provides neuroprotection in iron-induced apoptosis in dopaminergic neurons. J. Mol. Neurosci. 2006, 28, 125-141.
116. Sen, C.K.; Khanna, S.; Roy, S. Tocotrienol: The natural vitamin E to defend the nervous system? Ann. N. Y. Acad. Sci. 2004, 1031, 127-142.
117. Saito, Y.; Nishio, K.; Akazawa, Y.O.; Yamanaka, K.; Miyama, A.; Yoshida, Y.; Noguchi, N.; Niki, E. Cytoprotective effects of vitamin E homologues against glutamate-induced cell death in immature primary cortical neuron cultures: Tocopherols and tocotrienols exert similar effects by antioxidant function. Free Radic. Biol. Med. 2010, 49, 1542-1549.
118. Khanna, S.; Roy, S.; Parinandi, N.L.; Maurer, M.; Sen, C.K. Characterization of the potent neuroprotective properties of the natural vitamin E alpha-tocotrienol. J. Neurochem. 2006, 98, 1474-1486.
119. Tomé Ada, R.; Ferreira, P.M.; Freitas, R.M. Inhibitory action of antioxidants (ascorbic acid or alpha-tocopherol) on seizures and brain damage induced by pilocarpine in rats. Arq. Neuropsiquiatr. 2010, 68, 355-361.
120. Santos, I.M.; Tomé Ada, R.; Saldanha, G.B.; Ferreira, P.M.; Militão, G.C.; Freitas, R.M. Oxidative stress in the hippocampus during experimental seizures can be ameliorated with the antioxidant ascorbic acid. Oxid. Med. Cell Longev. 2009, 2, 214-221.
121. Zaidi, S.M.; Banu, N. Antioxidant potential of vitamins A, E and C in modulating oxidative stress in rat brain. Clin. Chim. Acta 2004, 340, 229-233.
122. +-ATPase activities and glutathione-reduced levels in rat hippocampus after pilocarpine-induced seizures. Cell Mol. Neurobiol. 2010, 30, 381-387.
123. Pence, S.; Erkutlu, I.; Kurtul, N.; Bosnak, M.; Alptekin, M.; Tan, U. Antiepileptogenic effects of glutathione against increased brain ADA in PTZ-induced epilepsy. Int. J. Neurosci. 2009, 119, 616-629.
124. Chung, S.Y.; Han, S.H. Melatonin attenuates kainic acid-induced hippocampal neurodegeneration and oxidative stress through microglial inhibition. J. Pineal Res. 2003, 34, 95-102.
125. Giusti, P.; Lipartiti, M.; Franceschini, D.; Schiavo, N.; Floreani, M.; Manev, H. Neuroprotection by melatonin from kainate-induced excitotoxicity in rats. FASEB J. 1996, 10, 891-896.
126. Bochyńska, A.; Lipczyńska-Łojkowska, W.; Gugała-Iwaniuk, M.; Lechowicz, W.; Restel, M.; Graban, A.; Lipska, B.; Ryglewicz, D. The effect of vitamin B supplementation on homocysteine metabolism and clinical state of patients with chronic epilepsy treated with carbamazepine and valproic acid. Seizure 2012, 21, 276-281.
127. Belcastro, V.; Striano, P. Vitamin B12, folate and hyperhomocysteinemia in patients with epilepsy. Ann. Neurol. 2011, 69, 1067-1068.
128. Ohtahara, S.; Yamatogi, Y.; Ohtsuka, Y. Vitamin B(6) treatment of intractable seizures. Brain Dev. 2011, 33, 783-789.
129. Rabie, T.; Mühlhofer, W.; Bruckner, T.; Schwab, A.; Bauer. A.T.; Zimmermann, M.; Bonke, D.; Marti, H.H.; Schenkel, J. Transient protective effect of B-vitamins in experimental epilepsy in the mouse brain. J. Mol. Neurosci. 2010, 41, 74-79.
130. Bacman, S.R.; Williams, S.L.; Hernandez, D.; Moraes, C.T. Modulating mtDNA heteroplasmy by mitochondria-targeted restriction endonucleases in a-differential multiple cleavage-site{norm of matrix} model. Gene Ther. 2007, 14, 1309-1318.
131. Chuang, Y.C. Mitochondrial dysfunction and oxidative stress in seizure-induced neuronal cell death. Acta Neurol. Taiwan 2010, 19, 3-15.
132. Lim, S.T.; Airavaara, M.; Harvey, B.K. Viral vectors for neurotrophic factor delivery: A gene therapy approach for neurodegenerative diseases of the CNS. Pharmacol. Res. 2010, 61, 14-26.
133. Murphy, M.P.; Smith, R.A. Drug delivery to mitochondria: The key to mitochondrial medicine. Adv. Drug Deliv. Rev. 2000, 41, 235-250.
134. Gruber, J.; Fong, S.; Chen, C.B.; Yoon, S.; Pastorin, G.; Schaffer, S.; Cheah, I.; Halliwell, B. Mitochondria-Targeted antioxidants and metabolic modulators as pharmacological interventions to slow. Ageing Biotechnol. Adv. 2012, in press.
135. Rocha, M.; Hernandez-Mijares, A.; Garcia-Malpartida, K.; Bañuls, C.; Bellod, L.; Victor, V.M. Mitochondria-Targeted antioxidant peptides. Curr. Pharm. Des. 2010, 16, 3124-3131.
136. Camara, A.K.; Lesnefsky, E.J.; Stowe, D.F. Potential therapeutic benefits of strategies directed to mitochondria. Antioxid. Redox Signal 2010, 13, 279-347.
137. Serviddio, G.; Romano, A.D.; Cassano, T.F.; Altomare, E.; Vendemiale, G. Principles and therapeutic relevance for targeting mitochondria in aging and neurodegenerative diseases. Curr. Pharm. Des. 2011, 17, 2036-2055.
138. Doyl, R.; Chan, C.K. Mitochondrial gene therapy: An evaluation of strategies for the treatment of mitochondrial DNA disorders. Hum. Gene Ther. 2008, 19, 1335-1348.
139. Spencer, S.S. Depth electroencephalography in selection of refractory epilepsy for surgery. Ann. Neurol. 1981, 9, 207-214.
140. Chugani, H.T.; Shewmon, D.A.; Peacock, W.J.; Shields, W.D.; Mazziotta, J.C.; Phelps, M.E. Surgical treatment of intractable neonatal-onset seizures: The role of positron emission tomography. Neurology 1988, 38, 1178-1188.
141. Gorman, D.G.; Shields, W.D.; Shewmon, D.A.; Chugani, H.T.; Finkel, R.; Comair, Y.G.; Peacock, W.J. Neurosurgical treatment of refractory status epilepticus. Epilepsia 1992, 33, 546-549.
142. Burch, J.; Hinde, S.; Palmer, S.; Beyer, F.; Minton, J.; Marson, A.; Wieshmann, U.; Woolacott, N.; Soares, M. The clinical effectiveness and cost-effectiveness of technologies used to visualise the seizure focus in people with refractory epilepsy being considered for surgery: A systematic review and decision-analytical model. Health Technol. Assess. 2012, 16, 1-157.
143. Pérez, R.P.; Cuesta, Z.I.; Meix, A.M.; Gallego, S.A. Evaluation of the effectiveness of the ketogenic diet with medium-chain triglycerides, in the treatment of refractory epilepsy in children. Apropos of a series of cases. An. Esp. Pediatr. 1989, 30, 155-158.
144. Lefevre, F.; Aronson, N. Ketogenic diet for the treatment of refractory epilepsy in children: A systematic review of efficacy. Pediatrics 2000, 105, 1-7.
145. Manso, G.M.; Arellano, M.; Sans, A.; Sanmartí, F.X.; Gómez, L.; Vernet, A.; Campistol, J. A ketogenic diet: Is this a valid alternative in refractory epilepsy. Rev. Neurol. 2001, 33, 1010-1014.
146. Do Kim, Y.; Rho, J.M. The ketogenic diet and epilepsy. Curr. Opin. Clin. Nutr. Metab. Care 2008, 11, 113-120.
147. Banach, M.; Gurdziel, E.; Je{ogonek}drych, M.; Borowicz, K.K. Melatonin in experimental seizures and epilepsy. Pharmacol. Rep. 2011, 63, 1-11.
148. Ogunmekan, A.O.; Hwang, P.A. A randomized, double-blind, placebo-controlled, clinical trial of D-alpha-tocopheryl acetate (vitamin E), as add-on therapy, for epilepsy in children. Epilepsia 1989, 30, 84-89.
149. Ashrafi, M.R.; Shabanian, R.; Abbaskhanian, A.; Nasirian, A.; Ghofrani, M.; Mohammadi, M.; Zamani, G.R.; Kayhanidoost, Z.; Ebrahimi, S.; Pourpak, Z. Selenium and intractable epilepsy: Is there any correlation? Pediatr. Neurol. 2007, 36, 25-29.
150. Ramaekers, V.T.; Calomme, M.; Vanden Berghe, D.; Makropoulos, W. Selenium deficiency triggering intractable seizures. Neuropediatrics 1994, 25, 217-223.
151. Togha, M.; Akhondzadeh, S.; Motamedi, M.; Ahmadi, B.; Razeghi, S. Allopurinol as adjunctive therapy in intractable epilepsy: A double-blind and placebo-controlled trial. Arch. Med. Res. 2007, 38, 313-316.
152. Bazil, C.W.; Short, D.; Crispin, D.; Zheng, W. Patients with intractable epilepsy have low melatonin, which increases following seizures. Neurology 2000, 55, 1746-1748.
153. Peled, N.; Shorer, Z.; Peled, E.; Pillar, G. Melatonin effect on seizures in children with severe neurologic deficit disorders. Epilepsia 2001, 42, 1208-1210.
154. Tada, H.; Morooka, K.; Arimoto, K.; Matsuo, T. Clinical effects of allopurinol on intractable epilepsy. Epilepsia 1991, 32, 279-283.
155. Marrosu, F.; Marrosu, G.; Rachele, M.G.; Masala, C.; Giagheddu, M. Allopurinol add-on treatment in intractable seizures. Neurological 1990, 12, 207-213.
156. Sander, J.W.; Patsalos, P.N. Allopurinol as an add-on drug in the management of intractable epilepsy. Epilepsy Res. 1988, 2, 223-225.