Oxidative stress associated with neuronal apoptosis in experimental models of epilepsy

Oxidative Medicine and Cellular Longevity

Volumn 2014, Issue , 2014, Pages

  Méndez Armenta, Marisela ^a   Nava Ruíz, Concepción ^a   Juárez Rebollar, Daniel ^a   Rodríguez Martínez, Erika ^b   Yescas Gómez, Petra ^a  

^a NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; FREE RADICALS; OXIDATIVE STRESS;

EXPERIMENTAL MODELS; FREE RADICAL PRODUCTIONS; MITOCHONDRIAL FUNCTION; NEUROLOGICAL DISORDERS; NEURONAL APOPTOSIS; NEURONAL DEATH;

NEUROLOGY;

CALCIUM; KAINIC ACID; NITRIC OXIDE; PENTETRAZOLE; PILOCARPINE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

APOPTOSIS; BRAIN MITOCHONDRION; CALCIUM SIGNALING; DNA DAMAGE; EPILEPTOGENESIS; EXCISION REPAIR; EXCITOTOXICITY; EXPERIMENTAL EPILEPSY; GENERALIZED EPILEPSY; LIPID PEROXIDATION; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; REVIEW; ANIMAL; DISEASE MODEL; EPILEPSY; GENETICS; HUMAN; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; DISEASE MODELS, ANIMAL; EPILEPSY; HUMANS; NEURONS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84921296198     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2014/293689     Document Type: Review

References (121)

1. A. K. Ngugi, C. Bottomley, I. Kleinschmidt, J. W. Sander, and C. R. Newton, "Estimation of the burden of active and life-time epilepsy: a meta-analytic approach," Epilepsia, vol. 51, no. 5, pp. 883-890, 2010.
2. R. S. Fisher, W. van Emde Boas, W. Blume et al., "Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE)," Epilepsia, vol. 46, no. 4, pp. 470-472, 2005.
3. Y.-C. Chuang, "Mitochondrial dysfunction and oxidative stress in seizure-induced neuronal cell death," Acta Neurologica Taiwanica, vol. 19, no. 1, pp. 3-15, 2010.
4. J. E. Cavazos, S. M. Jones, and D. J. Cross, "Sprouting and synaptic reorganization in the subiculum and CA1 region of the hippocampus in acute and chronic models of partial-onset epilepsy," Neuroscience, vol. 126, no. 3, pp. 677-688, 2004.
5. I. Blumcke, H. Beck, A. A. Lie, and O. D. Wiestler, "Molecular neuropathology of human mesial temporal lobe epilepsy," Epilepsy Research, vol. 36, no. 2-3, pp. 205-223, 1999.
6. M. Majores, S. Schoch, A. Lie, and A. J. Becker, "Molecular neuropathology of temporal lobe epilepsy: complementary approaches in animal models and human disease tissue," Epilepsia, vol. 48, supplement 2, pp. 4-12, 2007.
7. S. Waldbaumand M. Patel, "Mitochondria, oxidative stress, and temporal lobe epilepsy," Epilepsy Research, vol. 88, no. 1, pp. 23-45, 2010.
8. I. Blumcke, M. Thom, and O. D. Wiestler, "Ammon's horn sclerosis: a maldevelopmental disorder associated with temporal lobe epilepsy," Brain Pathology, vol. 12, no. 2, pp. 199-211, 2002.
9. M. Valko, D. Leibfritz, J. Moncol, M. T. D. Cronin, M. Mazur, and J. Telser, "Free radicals and antioxidants in normal physiological functions and human disease," International Journal of Biochemistry and Cell Biology, vol. 39, no. 1, pp. 44-84, 2007.
10. S. Waldbaum and M. Patel, "Mitochondrial dysfunction and oxidative stress: a contributing link to acquired epilepsy" Journal of Bioenergetics and Biomembranes, vol. 42, no. 6, pp. 449-455, 2010.
11. B. Halliwell and J. Gutteridge, "Cellular response to oxidative stress: adaptation, damage, repair, senescence and death," in FreeRadical in Biology andMedicine, chapter 4, pp. 187-267, 4th edition, 2007.
12. N. Cardenas-Rodriguez, B. Huerta-Gertrudis, L. Rivera-Espinosa et al., "Role of oxidative stress in refractory epilepsy: Evidence in patients and experimental models," International Journal of Molecular Sciences, vol. 14, no. 1, pp. 1455-1476, 2013.
13. E.-J. Shin, J. H. Jeong, Y. H. Chung et al., "Role of oxidative stress in epileptic seizures," Neurochemistry International, vol. 59, no. 2, pp. 122-137, 2011.
14. H. Cock, "The role of mitochondria in status epilepticus," Epilepsia, vol. 48, supplement 8, pp. 24-27, 2007.
15. I. Akdogan and N. Goksin-Yonguc, "Experimental epilepsy models and morphologic alterations of experimental epilepsy models in brain and hippocampus," in Underlying Mechanisms of Epilepsy, pp. 269-282, InTech, 2011.
16. M. Andres-Mach, J. R. Fike, and J. J. uszczki, "Neurogenesis in the epileptic brain: a brief overview from temporal lobe epilepsy," Pharmacological Reports, vol. 63, no. 6, pp. 1316-1323, 2011.
17. M. Valko, C. J. Rhodes, J. Moncol, M. Izakovic, and M. Mazur, "Free radicals, metals and antioxidants in oxidative stressinduced cancer," Chemico-Biological Interactions, vol. 160, no. 1, pp. 1-40, 2006.
18. M. Ramalingam and S.-J. Kim, "Reactive oxygen/nitrogen species and their functional correlations in neurodegenerative diseases," Journal of Neural Transmission, vol. 119, no. 8, pp. 891-910, 2012.
19. S. Gandhi and A. Y. Abramov, "Mechanismof oxidative stress in neurodegeneration," OxidativeMedicine and Cellular Longevity, vol. 2012, Article ID428010, 11 pages, 2012.
20. S. Orrenius, V. Gogvadze, and B. Zhivotovsky, "Mitochondrial oxidative stress: implications for cell death," Annual Review of Pharmacology and Toxicology, vol. 47, pp. 143-183, 2007.
21. C. C. T. Aguiar, A. B. Almeida, P. V. P. Ara'ujo et al., "Oxidative stress and epilepsy: literature review," Oxidative Medicine and Cellular Longevity, vol. 2012,Article ID 795259, 12 pages, 2012.
22. S. I. Liochev and I. Fridovich, "TheHaber-Weiss cycle-70 years later: an alternative view," Redox Report, vol. 7, no. 1, pp. 55-57, 2002.
23. B. Martinc, I. Grabnar, and T. Vovk, "The role of reactive species in epileptogenesis and influence of antiepileptic drug therapy on oxidative stress," Current Neuropharmacology, vol. 10, no. 4, pp. 328-343, 2012.
24. H.-Y. Yun, V. L. Dawson, and T. M. Dawson, "Neurobiology of nitric oxide," Critical Reviews in Neurobiology, vol. 10, no. 3-4, pp. 291-316, 1996.
25. J. Emerit,M. Edeas, and F. Bricaire, "Neurodegenerative disease and oxidative stress," Biomedicine & Pharmacotherapy, vol. 58, no. 1, pp. 39-46, 2004.
26. W. K. Alderton, C. E. Cooper, and R. G. Knowles, "Nitric oxide synthases: structure, function and inhibition," Biochemical Journal, vol. 357, no. 3, pp. 593-615, 2001.
27. C. Nava-Ruiz, M. M'endez-Armenta, and C. R'os, "Lead neurotoxicity: effects on brain nitric oxide synthase," Journal of Molecular Histology, vol. 43, no. 5, pp. 553-563, 2012.
28. R. Kohen and A. Nyska, "Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification," Toxicologic Pathology, vol. 30, no. 6, pp. 620-650, 2002.
29. L. A. Ridnour,D. D. Thomas,D. Mancardi et al., "The chemistry of nitrosative stress induced by nitric oxide and reactive nitrogen oxide species. Putting perspective on stressful biological situations," Biological Chemistry, vol. 385, no. 1, pp. 1-10, 2004.
30. C. Szab'o, H. Ischiropoulos, and R. Radi, "Peroxynitrite: biochemistry, pathophysiology and development of therapeutics," Nature Reviews Drug Discovery, vol. 6, no. 8, pp. 662-680, 2007.
31. A. Federico, E. Cardaioli, P. Da Pozzo, P. Formichi, G. N. Gallus, and E. Radi, "Mitochondria, oxidative stress and neurodegeneration," Journal of the Neurological Sciences, vol. 322, no. 1-2, pp. 254-262, 2012.
32. G. Benard, B. Faustin, E. Passerieux et al., "Physiological diversity of mitochondrial oxidative phosphorylation," American Journal of Physiology-CellPhysiology, vol. 291, no. 6,pp. C1172-C1182, 2006.
33. S.-D. Chen, D.-I. Yang, T.-K. Lin, F.-Z. Shaw, C.-W. Liou, and Y.-C. Chuang, "Roles of oxidative stress, apoptosis, PGC-1 and mitochondrial biogenesis in cerebral ischemia," International Journal ofMolecular Sciences, vol. 12, no. 10, pp. 7199-7215, 2011.
34. H. Du and S. S. Yan, "Mitochondrial medicine for neurodegenerative diseases," International Journal of Biochemistry and Cell Biology, vol. 42, no. 5, pp. 560-572, 2010.
35. P. S. Brookes, Y. Yoon, J. L. Robotham,M. W. Anders, and S.-S. Sheu, "Calcium, ATP, and ROS: a mitochondrial love-hate triangle," American Journal of Physiology: Cell Physiology, vol. 287, no. 4, pp. C817-C833, 2004.
36. J. F. Harrison, S. B. Hollensworth, D. R. Spitz, W. C. Copeland, G. L. Wilson, and S. P. LeDoux, "Oxidative stress-induced apoptosis in neurons correlates with mitochondrial DNA base excision repair pathway imbalance," Nucleic Acids Research, vol. 33, no. 14, pp. 4660-4671, 2005.
37. R. Rizzuto, P. Pinton, D. Ferrari et al., "Calcium and apoptosis: facts and hypotheses," Oncogene, vol. 22, no. 53, pp. 8619-8627, 2003.
38. J. M. Mat'es, "Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology," Toxicology, vol. 153, no. 1-3, pp. 83-104, 2000.
39. R. Dringen, J. M. Gutterer, and J. Hirrlinger, "Glutathione metabolism in brain: Metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species," European Journal of Biochemistry, vol. 267, no. 16, pp. 4912-4916, 2000.
40. C. W. Olanow, "An introduction to the free radical hypothesis in Parkinson's disease," Annals of Neurology, vol. 32, pp. S2-S9, 1992.
41. C. W. Olanow, "A radical hypothesis for neurodegeneration," Trends in Neurosciences, vol. 16, no. 11, pp. 439-444, 1993.
42. P. G. Winyard, C. J. Moody, and C. Jacob, "Oxidative activation of antioxidant defence," Trends in Biochemical Sciences, vol. 30, no. 8, pp. 453-461, 2005.
43. W. Briner, "The role of metal regulatory proteins in brain oxidative stress: a tutorial," Oxidative Medicine and Cellular Longevity, vol. 2012,Article ID 981561, 9 pages, 2012.
44. M. Jozefczak, T. Remans, J. Vangronsveld, and A. Cuypers, "Glutathione is a key player in metal-induced oxidative stress defenses," International Journal ofMolecular Sciences, vol. 13,no. 3, pp. 3145-3175, 2012.
45. J. Lindenau, H. Noack, H. Possel, K. Asayama, and G. Wolf, "Cellular distribution of superoxide dismutases in the rat CNS," Glia, vol. 29, no. 1, pp. 25-34, 2000.
46. L. Miao and D. K. St. Clair, "Regulation of superoxide dismutase genes: implications in disease," Free Radical Biology and Medicine, vol. 47, no. 4, pp. 344-356, 2009.
47. S. A. Lipton and P. A. Rosenberg, "Mechanisms of disease: Excitatory amino acids as a final common pathway for neurologic disorders,"The New England Journal ofMedicine, vol. 330, no. 9, pp. 613-622, 1994.
48. J. Garthwaite, "Glutamate, nitric oxide and cell-cell signalling in the nervous system," Trends in Neurosciences, vol. 14, no. 2, pp. 60-67, 1991.
49. P. Singh, K. A. Mann, H. K. Mangat, and G. Kaur, "Prolonged glutamate excitotoxicity: effects on mitochondrial antioxidants and antioxidant enzymes,"Molecular and Cellular Biochemistry, vol. 243, no. 1-2, pp. 139-145, 2003.
50. E. W. Englander, "Brain capacity for repair of oxidatively damaged DNA and preservation of neuronal function," Mechanisms of Ageing and Development, vol. 129, no. 7-8, pp. 475-482, 2008.
51. R. de Bont and N. van Larebeke, "Endogenous DNA damage in humans: a review of quantitative data," Mutagenesis, vol. 19, no. 3, pp. 169-185, 2004.
52. C. Canugovi,M. Misiak,L. K. Ferrarelli, D. L. Croteau, andV. A. Bohr, "The role of DNA repair in brain related disease pathology," DNA Repair, vol. 12, no. 8, pp. 578-587, 2013.
53. W. P. Roos and B. Kaina, "DNA damage-induced cell death by apoptosis," Trends inMolecularMedicine, vol. 12, no. 9, pp. 440-450, 2006.
54. Q. Kong and C. L. Lin, "Oxidative damage to RNA: mechanisms, consequences, and diseases," Cellular and Molecular Life Sciences, vol. 67, no. 11, pp. 1817-1829, 2010.
55. E. Mariani, M. C. Polidori, A. Cherubini, and P. Mecocci, "Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview," Journal of ChromatographyB, vol. 827, no. 1, pp. 65-75, 2005.
56. R. Franco, R. S'anchez-Olea, E. M. Reyes-Reyes, and M. I. Panayiotidis, "Environmental toxicity, oxidative stress and apoptosis: m'enage à Trois," Mutation Research-Genetic Toxicology and Environmental Mutagenesis, vol. 674, no. 1-2, pp. 3-22, 2009.
57. L.-P. Liang, S. G. Jarrett, andM. Patel, "Chelation ofmitochondrial iron prevents seizure-induced mitochondrial dysfunction and neuronal injury," Journal of Neuroscience, vol. 28, no. 45, pp. 11550-11556, 2008.
58. S. G. Jarrett, L. P. Liang, J. L. Hellier, K. J. Staley, and M. Patel, "MitochondrialDNAdamage and impaired base excision repair during epileptogenesis," Neurobiology of Disease, vol. 30, no. 1, pp. 130-138, 2008.
59. J. D. Robertson and S. Orrenius, "Molecular mechanisms of apoptosis induced by cytotoxic chemicals," Critical Reviews in Toxicology, vol. 30, no. 5, pp. 609-627, 2000.
60. M. O. Hengartner, "The biochemistry of apoptosis," Nature, vol. 407, no. 6805, pp. 770-776, 2000.
61. M. Kajta, "Apoptosis in the central nervous system: mechanisms and protective strategies," Polish Journal of Pharmacology, vol. 56, no. 6, pp. 689-700, 2004.
62. S. Krantic, N. Mechawar, S. Reix, and R. Quirion, "Apoptosisinducing factor: a matter of neuron life and death," Progress in Neurobiology, vol. 81, no. 3, pp. 179-196, 2007.
63. I. N. Lavrik, A. Golks, and P. H. Krammer, "Caspase: pharmacological manipulation of cell death," Journal of Clinical Investigation, vol. 115, no. 10, pp. 2665-2672, 2005.
64. D. C. Henshall and T. Engel, "Contribution of apoptosisassociated signaling pathways to epileptogenesis: lessons from Bcl-2 family knockouts," Frontiers in Cellular Neuroscience, vol. 7, no. 111, pp. 1-11, 2013.
65. T. Engel and D. C. Henshall, "Apoptosis, Bcl-2 family proteins and caspases: The ABCs of seizure-damage and epileptogenesis" International Journal of Physiology, Pathophysiology and Pharmacology, vol. 1, no. 2, pp. 97-115, 2009.
66. K. S. Panickar and R. A. Anderson, "Effect of polyphenols on oxidative stress and mitochondrial dysfunction in neuronal death and brain edema in cerebral ischemia," International Journal of Molecular Sciences, vol. 12, no. 11, pp. 8181-8207, 2011.
67. S.-D. Chen, A. Y. W. Chang, and Y.-C. Chuang, "The potential role of mitochondrial dysfunction in seizure-associated cell death in the hippocampus and epileptogenesis," Journal of Bioenergetics and Biomembranes, vol. 42, no. 6, pp. 461-465, 2010.
68. M. R. Gluck, E. Jayatilleke, S. Shaw, A. J. Rowan, and V. Haroutunian, "CNS oxidative stress associated with the kainic acid rodent model of experimental epilepsy," Epilepsy Research, vol. 39, no. 1, pp. 63-71, 2000.
69. E. A. Gilberti and L. D. Trombetta, "The relationship between stress protein induction and the oxidative defense system in the rat hippocampus following kainic acid administration," Toxicology Letters, vol. 116, no. 1-2, pp. 17-26, 2000.
70. W. Y. Ong, C. Y. Hu,O. P. Hjelle,O. P. Ottersen, and B. Halliwell, "Changes in glutathione in the hippocampus of rats injected with kainate: depletion in neurons and upregulation in glia," Experimental Brain Research, vol. 132, no. 4, pp. 510-516, 2000.
71. L.-P. Liang and M. Patel, "Seizure-induced changes in mitochondrial redox status," Free Radical Biology and Medicine, vol. 40, no. 2, pp. 316-322, 2006.
72. L. P. Liang, Y. S. Ho, and M. Patel, "Mitochondrial superoxide production in kainate-induced hippocampal damage," Neuroscience, vol. 101, no. 3, pp. 563-570, 2000.
73. M. Patel, L.-P. Liang, and L. J. Roberts II, "Enhanced hippocampal F2-isoprostane formation following kainate-induced seizures," Journal of Neurochemistry, vol. 79, no. 5, pp. 1065-1069, 2001.
74. E.-J. Shin, J. H. Jeong, G. Bing et al., "Kainate-induced mitochondrial oxidative stress contributes to hippocampal degeneration in senescence-accelerated mice," Cellular Signalling, vol. 20, no. 4, pp. 645-658, 2008.
75. E. Ben-Menachem, M. Kyllerman, and S. Marklund, "Superoxide dismutase and glutathione peroxidase function in progressive myoclonus epilepsies," Epilepsy Research, vol. 40, no. 1, pp. 33-39, 2000.
76. V. A. Yurekli and M. Naziroglu, "Selenium and topiramate attenuates blood oxidative toxicity in patients with epilepsy: a clinical pilot study," Biological Trace Element Research, vol. 152, no. 2, pp. 180-186, 2013.
77. S. A. Hamed, M. M. Abdellah, and N. El-Melegy, "Blood levels of trace elements, electrolytes, and oxidative stress/antioxidant systems in epileptic patients," Journal of Pharmacological Sciences, vol. 96, no. 4, pp. 465-473, 2004.
78. D. Deepa, B. Jayakumari, and S. V. Thomas, "Lipid peroxidation in women with epilepsy," Annals of Indian Academy of Neurology, vol. 11, no. 1, pp. 44-46, 2008.
79. K. Sudha, A. V. Rao, and A. Rao, "Oxidative stress and antioxidants in epilepsy," Clinica Chimica Acta, vol. 303, no. 1-2, pp. 19-24, 2001.
80. C. K. Schindler, E. G. Pearson, H. P. Bonner et al., "Caspase-3 cleavage and nuclear localization of caspase-activated DNase in human temporal lobe epilepsy," Journal of Cerebral Blood Flow and Metabolism, vol. 26, no. 4, pp. 583-589, 2006.
81. D. C. Henshall and B. S. Meldrum, "Cell death and survival mechanisms after and repetead brief seizures," in Jasper's Basic Mechanisms of the Epilepsies, J. L. Noebels, M. Avoli, M. A. Rogawski, R. W. Olsen, and V. D. Delgado-Escueta, Eds., pp. 1-19, 4th edition, 2010.
82. D. C. Henshall, R. S. B. Clark, P. D. Adelson, M. Chen, S. C. Watkins, andR. P. Simon, "Alterations in bcl-2 and caspase gene family protein expression in human temporal lobe epilepsy," Neurology, vol. 55, no. 2, pp. 250-257, 2000.
83. S. Xu, Q. Pang,Y. Liu,W. Shang,G. Zhai, andM. Ge, "Neuronal apoptosis in the resected sclerotic hippocampus in patients with mesial temporal lobe epilepsy," Journal of Clinical Neuroscience, vol. 14, no. 9, pp. 835-840, 2007.
84. Y. Ben-Ari and R. Cossart, "Kainate, a double agent that generates seizures: two decades of progress," Trends in Neurosciences, vol. 23, no. 11, pp. 580-587, 2000.
85. D. S. Reddy and R. Kuruba, "Experimental models of status epilepticus and neuronal injury for evaluation of therapeutic interventions," International Journal of Molecular Sciences, vol. 14, no. 9, pp. 18284-18318, 2013.
86. M. V. Frantseva, J. L. P. Velazquez, P. A. Hwang, and P. L. Carlen, "Free radical production correlates with cell death in an in vitro model of epilepsy," European Journal of Neuroscience, vol. 12,no. 4, pp. 1431-1439, 2000.
87. M. Patel, "Mitochondrial dysfunction and oxidative stress: cause and consequence of epileptic seizures," Free Radical Biology and Medicine, vol. 37, no. 12, pp. 1951-1962, 2004.
88. X. Wang and E. K. Michaelis, "Selective neuronal vulnerability to oxidative stress in the brain," Frontiers in Aging Neuroscience, vol. 2, no. 12, pp. 1-13, 2010.
89. Y. B. Ouyang, L. A. Voloboueva, L. J. Xu, and R. G. Giffard, "Selective dysfunction of hippocampal CA1 astrocytes contributes to delayed neuronal damage after transient forebrain ischemia," Journal ofNeuroscience, vol. 27,no. 16,pp. 4253-4260, 2007.
90. N. A. Simonian, R. L. Getz, J. C. Leveque, C. Konradi, and J. T. Coyle, "Kainic acid induces apoptosis in neurons," Neuroscience, vol. 75, no. 4, pp. 1047-1055, 1996.
91. D. C. Henshall, J. Chen, and R. P. Simon, "Involvement of caspase-3-like protease in themechanism of cell death following focally evoked limbic seizures," Journal of Neurochemistry, vol. 74, no. 3, pp. 1215-1223, 2000.
92. J. Bengzon, Z. Kokaia, E. Elmer, A. Nanobashvili, M. Kokaia, and O. Lindvall, "Apoptosis and proliferation of denture gyrus neurons after single and intermittent limbic seizures," Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 19, pp. 10432-10437, 1997.
93. Y. C. Chuang, S. D. Chen, T. K. Lin et al., "Upregulation of nitric oxide synthase II contributes to apoptotic cell death in the hippocampal CA3 subfield via a cytochrome c/caspase-3 signaling cascade following induction of experimental temporal lobe status epilepticus in the rat," Neuropharmacology, vol. 52, no. 5, pp. 1263-1273, 2007.
94. P. P. deDeyn, R. D'Hooge, B. Marescau, and Y.-Q. Pei, "Chemicalmodels of epilepsy with some reference to their applicability in the development of anticonvulsants," Epilepsy Research, vol. 12, no. 2, pp. 87-110, 1992.
95. W. Loscher, "Critical review of current animal models of seizures and epilepsy used in the discovery and development of new antiepileptic drugs," Seizure, vol. 20, no. 5, pp. 359-368, 2011.
96. M. G. Corda, M. Orlandi, D. Lecca, and O. Giorgi, "Decrease in gabaergic function induced by pentylenetetrazol kindling in rats: antagonism by MK-801," Journal of Pharmacology and Experimental Therapeutics, vol. 262, no. 2, pp. 792-800, 1992.
97. C. Rubio, M. Rubio-Osornio, S. Retana-M'arquez, M. L. Ver'onica Custodio, and C. Paz, "In vivo experimentalmodels of epilepsy," Central Nervous System Agents in Medicinal Chemistry, vol. 10, no. 4, pp. 298-309, 2010.
98. R.-Q. Huang, C. L. Bell-Horner, M. I. Dibas, D. F. Covey, J. A. Drewe, and G. H. Dillon, "Pentylenetetrazole-induced inhibition of recombinant -aminobutyric acid type A (GABA(A)) receptors:mechanism and site of action," Journal of Pharmacology and Experimental Therapeutics, vol. 298, no. 3, pp. 986-995, 2001.
99. M. I. Naseer, L. Shupeng, and M. O. Kim, "Maternal epileptic seizure induced by Pentylenetetrazol: apoptotic neurodegeneration and decreased GABAB1 receptor expression in prenatal rat brain," Molecular Brain, vol. 2, article 20, 2009.
100. K. Jandov'a, V. Riljak, J. Pokorn'y, and M. Langmeier, "Pentylentetrazol associated changes of hippocampal neurons in immature rats.," Prague medical report, vol. 108, no. 1, pp. 67-74, 2007.
101. N. Patsoukis, G. Zervoudakis, C. D. Georgiou, F. Angelatou, N. A. Matsokis, and N. T. Panagopoulos, "Effect of pentylenetetrazol-induced epileptic seizure on thiol redox state in the mouse cerebral cortex," Epilepsy Research, vol. 62, no. 1, pp. 65-74, 2004.
102. C. Rauca, I. Wiswedel, R. Zerbe, G. Keilhoff, and M. Krug, "The role of superoxide dismutase and -tocopherol in the development of seizures and kindling induced by pentylenetetrazol- influence of the radical scavenger -phenyl-Ntert-butyl nitrone," Brain Research, vol. 1009, no. 1-2, pp. 203-212, 2004.
103. H. S. El-Abhar and H. M. Abd El Gawad, "Modulation of cortical nitric oxide synthase, glutamate, and redox state by nifedipine and taurine in PTZ-kindled mice," Epilepsia, vol. 44, no. 3, pp. 276-281, 2003.
104. V. Erakovi'c, G. Zupan, J. Varljen, and A. Simoni'c, "Pentylenetetrazol-induced seizures and kindling: changes in free fatty acids, superoxide dismutase, and glutathione peroxidase activity," Neurochemistry International, vol. 42, no. 2, pp. 173-178, 2003.
105. C. Rauca, R. Zerbe, andH. Jantze, "Formation of free hydroxyl radicals after pentylenetetrazol-induced seizure and kindling," Brain Research, vol. 847, no. 2, pp. 347-351, 1999.
106. M. I. Naseer, I. Ullah, N. Ullah et al., "Neuroprotective effect of vitamin C against PTZ induced apoptotic neurodegeneration in adult rat brain,"PakistanJournal of Pharmaceutical Sciences, vol. 24, no. 3, pp. 263-268, 2011.
107. J. H. Goodman, "Experimental models of status epilepticus," in NeuropharmacologyMethods in Epilepsy Research, S. L. Peterson and T. E. Albertson, Eds., pp. 95-125, CRC Press, Boca Raton, Fla, USA, 1998.
108. M. Glien, C. Brandt, H. Potschka, H. Voigt, U. Ebert, andW. Loscher, "Repeated low-dose treatment of rats with pilocarpine: low mortality but high proportion of rats developing epilepsy," Epilepsy Research, vol. 46, no. 2, pp. 111-119, 2001.
109. G. Curiaa,D. Longob, G. Biaginib et al., "Thepilocarpinemodel of temporal lobe epilepsy," Journal of NeuroscienceMethods, vol. 172, pp. 143-157, 2008.
110. M. R. Priel and E. X. Albuquerque, "Short-term effects of pilocarpine on rat hippocampal neurons in culture," Epilepsia, vol. 43, no. 5, pp. 40-46, 2002.
111. T. Nagao, A. Alonso, and M. Avoli, "Epileptiform activity induced by pilocarpine in the rat hippocampal-entorhinal slice preparation," Neuroscience, vol. 72, no. 2, pp. 399-408, 1996.
112. I. Smolders, G. M. Khan, J. Manil, G. Ebinger, and Y. Michotte, "NMDAreceptor-mediated pilocarpine-induced seizures: characterization in freely moving rats by microdialysis," The British Journal of Pharmacology, vol. 121, no. 6, pp. 1171-1179, 1997.
113. R. M. Freitas, "Investigation of oxidative stress involvement in hippocampus in epilepsy model induced by pilocarpine," Neuroscience Letters, vol. 462, no. 3, pp. 225-229, 2009.
114. H. V. Nobre Jr., M. M. D. F. Fonteles, and R. M. D. de Freitas, "Acute seizure activity promotes lipid peroxidation, increased nitrite levels and adaptive pathways against oxidative stress in the frontal cortex and striatum," Oxidative Medicine and Cellular Longevity, vol. 2, no. 3, pp. 130-137, 2009.
115. P. S. D. Santos, J. P. Costa, A. D. R. Tom'e et al., "Oxidative stress in rat striatumafter pilocarpine-induced seizures is diminished by alpha-tocopherol," European Journal of Pharmacology, vol. 668, no. 1-2, pp. 65-71, 2011.
116. P. S. dos Santos, L. M. L. Campelo, R. L. M. de Freitas, C. M. Feitosa, G. B. Saldanha, and R. M. de Freitas, "Lipoic acid effects on glutamate and taurine concentrations in rat hippocampus after pilocarpine-induced seizures," Arquivos de Neuro-Psiquiatria, vol. 69, no. 2 B, pp. 360-364, 2011.
117. R. R. F. Pestana, E. R. Kinjo, M. S. Hernandes, and L. R. G. Britto, "Reactive oxygen species generated by NADPH oxidase are involved in neurodegeneration in the pilocarpine model of temporal lobe epilepsy," Neuroscience Letters, vol. 484, no. 3, pp. 187-191, 2010.
118. D. G. Fujikawa, S. S. Shinmei, and B. Cai, "Lithium-pilocarpineinduced status epilepticus produces necrotic neurons with internucleosomal DNA fragmentation in adult rats," European Journal of Neuroscience, vol. 11, no. 5, pp. 1605-1614, 1999.
119. X. Wen, Y. Huang, and J. Wang, "Erythropoietin preconditioning on hippocampus neuronal apoptosis following status epilepticus induced by Li-pilocarpine in rats through anticaspase-3 expression," Neurology India, vol. 54, no. 1, pp. 58-63, 2006.
120. L. Wang, Y. H. Liu, Y. G. Huang, and L. W. Chen, "Time-course of neuronal death in the mouse pilocarpine model of chronic epilepsy using Fluoro-Jade C staining," Brain Research, vol. 1241, pp. 157-167, 2008.
121. J. Liu, A. Wang, L. Li, Y. Huang, P. Xue, andA. Hao, "Oxidative stress mediates hippocampal neuron death in rats after lithiumpilocarpine-induced status epilepticus," Seizure, vol. 19, no. 3, pp. 165-172, 2010.