Excitotoxicity and neuronal death in epilepsy;Excitotoxicidad y muerte neuronal en la epilepsia

Biotecnologia Aplicada

Volumn 30, Issue 1, 2013, Pages 1-8

  Lorigados, Lourdes ^a   Orozco, Sandra ^b   Morales, Lilia ^c   Estupiñán, Bárbara ^c   García, Iván ^d   Rocha, Luisa ^e  

^a CENTRO INTERNACIONAL DE RESTAURACIÓN NEUROLÓGICA CIREN   (Cuba)

^b INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^c Departamento de Neurofisiología   (Mexico)

^d Servicio de Neurocirugía   (Mexico)

^e DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Apoptosis; Epilepsy; Excitotoxicity; Necrosis

Indexed keywords

CASPASE; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; ENZYME ACTIVATION; EPILEPSY; EXCITOTOXICITY; MULTIGENE FAMILY; NERVE CELL NECROSIS;

EID: 84876905062     PISSN: 08644551     EISSN: 10272852     Source Type: Journal    
DOI: None     Document Type: Article

References (95)

1. Yang JL, Sykora P, Wilson DM, 3rd, Mattson MP, Bohr VA. The excitatory neurotransmitter glutamate stimulates DNA repair to increase neuronal resiliency. Mech Ageing Dev. 2011;132(8-9): 405-11.
2. Wang Y, Qin ZH. Molecular and cellular mechanisms of excitotoxic neuronal death. Apoptosis. 2010; 15(11):1382-402.
3. Severino PC, Muller Gdo A, Vandresen- Filho S, Tasca CI. Cell signaling in NMDA preconditioning and neuroprotection in convulsions induced by quinolinic acid. Life Sci. 2011;89(15- 16):570-6.
4. Araujo IM, Carreira BP, Carvalho CM, Carvalho AP. Calpains and delayed calcium deregulation in excitotoxicity. Neurochem Res. 2010; 35(12):1966-9.
5. Wang Y, Denisova JV, Kang KS, Fontes JD, Zhu BT, Belousov AB. Neuronal gap junctions are required for NMDA receptor- mediated excitotoxicity: implications in ischemic stroke. J Neurophysiol. 2010;104(6):3551-6.
6. Farooqui AA, Ong WY, Horrocks LA. Glutamate receptors and their association with other neurochemical parameters in excitotoxicity. In: Farooqui AA, Ong WY, Horrocks LA, editors. Neurochemical aspects of excitotoxicity. New York: Springer; 2008. p. 105-36.
7. Fujikawa DG, Shinmei SS, Cai B. Kainic acid-induced seizures produce necrotic, not apoptotic, neurons with internucleosomal DNA cleavage: implications for programmed cell death mechanisms. Neuroscience. 2000;98(1):41-53.
8. Fujikawa DG, Shinmei SS, Cai B. Seizure-induced neuronal necrosis: implications for programmed cell death mechanisms. Epilepsia. 2000; 41 Suppl 6:S9-13.
9. Ebert U, Brandt C, Loscher W. Delayed sclerosis, neuroprotection, and limbic epileptogenesis after status epilepticus in the rat. Epilepsia. 2002;43 Suppl 5:86-95.
10. Kubova H, Druga R, Lukasiuk K, Suchomelova L, Haugvicova R, Jirmanova I, et al. Status epilepticus causes necrotic damage in the mediodorsal nucleus of the thalamus in immature rats. J Neurosci. 2001; 21(10):3593-9.
11. Bengzon J, Mohapel P, Ekdahl CT, Lindvall O. Neuronal apoptosis after brief and prolonged seizures. Prog Brain Res. 2002;135:111-9.
12. Henshall DC, Araki T, Schindler CK, Lan JQ, Tiekoter KL, Taki W, et al. Activation of Bcl-2-associated death protein and counter-response of Akt within cell populations during seizureinduced neuronal death. J Neurosci. 2002;22(19):8458-65.
13. Liou AK, Clark RS, Henshall DC, Yin XM, Chen J. To die or not to die for neurons in ischemia, traumatic brain injury and epilepsy: a review on the stress-activated signaling pathways and apoptotic pathways. Prog Neurobiol. 2003;69(2):103-42.
14. Dong XX, Wang Y, Qin ZH. Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sin. 2009;30(4): 379-87.
15. Qin ZH, Tao LY, Chen X. Dual roles of NF-kappaB in cell survival and implications of NF-kappaB inhibitors in neuroprotective therapy. Acta Pharmacol Sin 2007;28(12):1859-72.
16. Zhang XD, Wang Y, Zhang X, Han R, Wu JC, Liang ZQ, et al. p53 mediates mitochondria dysfunctiontriggered autophagy activation and cell death in rat striatum. Autophagy. 2009;5(3):339-50.
17. Shacka JJ, Lu J, Xie ZL, Uchiyama Y, Roth KA, Zhang J. Kainic acid induces early and transient autophagic stress in mouse hippocampus. Neurosci Lett. 2007;414(1):57-60.
18. Wang Y, Dong XX, Cao Y, Liang ZQ, Han R, Wu JC, et al. p53 induction contributes to excitotoxic neuronal death in rat striatum through apoptotic and autophagic mechanisms. Eur J Neurosci. 2009; 30(12):2258-70.
19. Olney JW. Excitatory transmitters and epilepsy-related brain damage. Int Rev Neurobiol. 1985;27:337-62.
20. Haglid KG, Wang S, Qiner Y, Hamberger A. Excitotoxicity. Experimental correlates to human epilepsy. Mol Neurobiol. 1994;9(1-3):259-63.
21. Nicholls DG, Ward MW. Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts. Trends Neurosci. 2000;23(4):166-74.
22. Murchison D, Griffith WH. Mitochondria buffer non-toxic calcium loads and release calcium through the mitochondrial permeability transition pore and sodium/calcium exchanger in rat basal forebrain neurons. Brain Res. 2000;854(1-2):139-51.
23. Almeida A, Heales SJ, Bolanos JP, Medina JM. Glutamate neurotoxicity is associated with nitric oxide-mediated mitochondrial dysfunction and glutathione depletion. Brain Res. 1998;790(1-2): 209-16.
24. Olney JW. New insights and new issues in developmental neurotoxicology. Neurotoxicology. 2002;23(6):659-68.
25. Struzynska L. A glutamatergic component of lead toxicity in adult brain: the role of astrocytic glutamate transporters. Neurochem Int. 2009;55(1-3): 151-6.
26. Pereno GL. Fisiopatología de la epilepsia del lóbulo temporal: revisión del proceso de muerte neuronal a la neuroplasticidad. Rev Argentina Cienc Comportamiento. 2010;2(1):46-57.
27. Eid T, Williamson A, Lee TS, Petroff OA, de Lanerolle NC. Glutamate and astrocytes-key players in human mesial temporal lobe epilepsy? Epilepsia. 2008;49 Suppl 2:42-52.
28. Ueda Y, Yokoyama H, Nakajima A, Tokumaru J, Doi T, Mitsuyama Y. Glutamate excess and free radical formation during and following kainic acid-induced status epilepticus. Exp Brain Res. 2002;147(2):219-26.
29. Morimoto K, Fahnestock M, Racine RJ. Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol. 2004;73(1):1-60.
30. Rogawski MA, Kurzman PS, Yamaguchi SI, Li H. Role of AMPA and GluR5 kainate receptors in the development and expression of amygdala kindling in the mouse. Neuropharmacology. 2001;40(1): 28-35.
31. Deshpande LS, Lou JK, Mian A, Blair RE, Sombati S, Attkisson E, et al. Time course and mechanism of hippocampal neuronal death in an in vitro model of status epilepticus: role of NMDA receptor activation and NMDA dependent calcium entry. Eur J Pharmacol. 2008;583(1):73-83.
32. Rice AC, DeLorenzo RJ. NMDA receptor activation during status epilepticus is required for the development of epilepsy. Brain Res. 1998; 782(1-2): 240-7.
33. Ullal G, Fahnestock M, Racine R. Time-dependent effect of kainateinduced seizures on glutamate receptor GluR5, GluR6, and GluR7 mRNA and Protein Expression in rat hippocampus. Epilepsia. 2005;46(5):616-23.
34. Vincent P, Mulle C. Kainate receptors in epilepsy and excitotoxicity. Neuroscience. 2009;158(1):309-23.
35. Lado FA, Laureta EC, Moshe SL. Seizure-induced hippocampal damage in the mature and immature brain. Epileptic Disord. 2002;4(2):83-97.
36. Cherubini E, Ben-Ari Y, Krnjevic K. Anoxia produces smaller changes in synaptic transmission, membrane potential, and input resistance in immature rat hippocampus. J Neurophysiol. 1989;62(4):882-95.
37. Stafstrom CE, Holmes GL. Effects of uncontrolled seizures. Neural changes in animal models. Adv Exp Med Biol. 2002;497:171-94.
38. Marks JD, Friedman JE, Haddad GG. Vulnerability of CA1 neurons to glutamate is developmentally regulated. Brain Res Dev Brain Res. 1996; 97(2):194-206.
39. Albala BJ, Moshe SL, Okada R. Kainic-acid-induced seizures: a developmental study. Brain Res. 1984;315(1): 139-48.
40. Bender R, Baram TZ. Do prolonged febrile seizures injury hippocampal neurons? Insights from animal models. In: Baram TZ, Shinnar S. editors. Febrile seizures. San Diego, Academic Press. 2002. p. 583-7.
41. Berger ML, Tremblay E, Nitecka L, Ben-Ari Y. Maturation of kainic acid seizure-brain damage syndrome in the rat. III. Postnatal development of kainic acid binding sites in the limbic system. Neuroscience. 1984;13(4):1095-104.
42. Ben-Ari Y, Tremblay E, Riche D, Ghilini G, Naquet R. Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience. 1981;6(7):1361-91.
43. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 1985;14(2):375-403.
44. Schwob JE, Fuller T, Price JL, Olney JW. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience. 1980;5(6):991-1014.
45. Sloviter RS. The neurobiology of temporal lobe epilepsy: too much information, not enough knowledge. C R Biol. 2005;328(2):143-53.
46. Sperk G, Lassmann H, Baran H, Seitelberger F, Hornykiewicz O. Kainic acid-induced seizures: dose-relationship of behavioural, neurochemical and histopathological changes. Brain Res. 1985;338(2):289-95.
47. Anguelova E, Smirnova T. Differential expression of small heat shock protein 27 in the rat hippocampus and septum after fimbria-fornix lesion. Neurosci Lett. 2000;280(2):99-102.
48. Valentim LM, Geyer AB, Tavares A, Cimarosti H, Worm PV, Rodnight R, et al. Effects of global cerebral ischemia and preconditioning on heat shock protein 27 immunocontent and phosphorylation in rat hippocampus. Neuroscience. 2001;107(1):43-9.
49. Planas AM, Soriano MA, Estrada A, Sanz O, Martin F, Ferrer I. The heat shock stress response after brain lesions: induction of 72 kDa heat shock protein (cell types involved, axonal transport, transcriptional regulation) and protein synthesis inhibition. Prog Neurobiol. 1997;51(6):607-36.
50. Planas AM, Soriano MA, Ferrer I, Rodriguez Farre E. Kainic acid-induced heat shock protein-70, mRNA and protein expression is inhibited by MK-801 in certain rat brain regions. Eur J Neurosci. 1995;7(2):293-304.
51. Yenari MA, Fink SL, Sun GH, Chang LK, Patel MK, Kunis DM, et al. Gene therapy with HSP72 is neuroprotective in rat models of stroke and epilepsy. Ann Neurol. 1998;44(4):584-91.
52. Pozas E, Ballabriga J, Planas AM, Ferrer I. Kainic acid-induced excitotoxicity is associated with a complex c-Fos and c-Jun response which does not preclude either cell death or survival. J Neurobiol. 1997;33(3):232-46.
53. Gass P, Herdegen T. Neuronal expression of AP1 proteins in excitotoxic neurodegenerative disorders and following nerve fiber lesions. Progr Neurobiol. 1995;47(4-5):257-90.
54. Kasof GM, Mandelzys A, Maika SD, Hammer RE, Curran T, Morgan JI. Kainic acid-induced neuronal death is associated with DNA damage and a unique immediate early gene response in c-fos-lacZ transgenic rats. J Neurosci. 1995;15(6):4238-49.
55. Chen ZL, Strickland S. Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell. 1997;91(7):917-25.
56. Tan Z, Levid J, Schreiber SS. Increased expression of Fas (CD95/APO-1) in adult rat brain after kainate-induced seizures. Neuroreport. 2001;12(9):1979-82.
57. Gillardon F, Wickert H, Zimmermann M. Up-regulation of bax and downregulation of bcl-2 is associated with kainate-induced apoptosis in mouse brain. Neurosci Lett. 1995;192(2): 85-8.
58. Lopez E, Pozas E, Rivera R, Ferrer I. Bcl-2, Bax and Bcl-x expression following kainic acid administration at convulsant doses in the rat. Neuroscience. 1999;91(4):1461-70.
59. Gillardon F, Klimaschewski L, Wickert H, Krajewski S, Reed JC, Zimmermann M. Expression pattern of candidate cell death effector proteins Bax, Bcl-2, Bcl-X, and c-Jun in sensory and motor neurons following sciatic nerve transection in the rat. Brain Res. 1996;739(1-2):244-50.
60. Faherty CJ, Xanthoudakis S, Smeyne RJ. Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment. Brain Res Mol Brain Res. 1999;70(1):159-63.
61. Ferrer I, Lopez E, Blanco R, Rivera R, Krupinski J, Marti E. Differential c- Fos and caspase expression following kainic acid excitotoxicity. Acta Neuropathol. 2000;99(3):245-56.
62. Henshall DC, Chen J, Simon RP. Involvement of caspase-3-like protease in the mechanism of cell death following focally evoked limbic seizures. J Neurochem. 2000;74(3):1215-23.
63. Kienzler F, Norwood BA, Sloviter RS. Hippocampal injury, atrophy, synaptic reorganization, and epileptogenesis after perforant pathway stimulation-induced status epilepticus in the mouse. J Comp Neurol. 2009;515(2):181-96.
64. Sloviter RS, Zappone CA, Harvey BD, Frotscher M. Kainic acid-induced recurrent mossy fiber innervation of dentate gyrus inhibitory interneurons: possible anatomical substrate of granule cell hyper-inhibition in chronically epileptic rats. J Comp Neurol. 2006;494(6):944-60.
65. Tauck DL, Nadler JV. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci. 1985;5(4): 1016-22.
66. Bender R, Dubé C, Baram TZ. Mossy fiber sprouting into the inner molecular layer of the dentate gyrus follows prolonged febrile seizures in immature rat model. Epilepsia. 2000;41(suppl 7): 76-9.
67. Bendotti C, Pende M, Samanin R. Expression of GAP-43 in the granule cells of rat hippocampus after seizure-induced sprouting of mossy fibres: in situ hybridization and immunocytochemical studies. Eur J Neurosci. 1994;6(4):509-15.
68. Boschert U, O'Shaughnessy C, Dickinson R, Tessari M, Bendotti C, Catsicas S, et al. Developmental and plasticity-related differential expression of two SNAP-25 isoforms in the rat brain. J Comp Neurol. 1996;367(2):177-93.
69. Geddes JW, Hess EJ, Hart RA, Kesslak JP, Cotman CW, Wilson MC. Lesions of hippocampal circuitry define synaptosomal-associated protein-25 (SNAP-25) as a novel presynaptic marker. Neuroscience. 1990;38(2):515-25.
70. Numakawa T, Matsumoto T, Numakawa Y, Richards M, Yamawaki S, Kunugi H. Protective Action of Neurotrophic Factors and Estrogen against Oxidative Stress-Mediated Neurodegeneration. J Toxicol. 2011;2011:405194.
71. Numakawa T, Suzuki S, Kumamaru E, Adachi N, Richards M, Kunugi H. BDNF function and intracellular signaling in neurons. Histol Histopathol. 2010;25(2):237-58.
72. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35(4):495-516.
73. Fujikawa DG, Shinmei SS, Zhao S, Aviles ER, Jr. Caspase-dependent programmed cell death pathways are not activated in generalized seizure-induced neuronal death. Brain Res. 2007;1135(1):206-18.
74. Uysal H, Cevik IU, Soylemezoglu F, Elibol B, Ozdemir YG, Evrenkaya T, et al. Is the cell death in mesial temporal sclerosis apoptotic? Epilepsia. 2003;44(6): 778-84.
75. Uysal H, Cevik IU, Soylemezoglu F, Elibol B, Ozdemir YG, Evrenkaya T, et al. Is the cell death in mesial temporal sclerosis apoptotic? Epilepsia. 2003;44(6):778-84.
76. Narkilahti S, Nissinen J, Pitkanen A. Administration of caspase 3 inhibitor during and after status epilepticus in rat: effect on neuronal damage and epileptogenesis. Neuropharmacology. 2003;44(8): 1068-88.
77. Pollard H, Charriaut-Marlangue C, Cantagrel S, Represa A, Robain O, Moreau J, et al. Kainate-induced apoptotic cell death in hippocampal neurons. Neuroscience. 1994;63(1):7-18.
78. Sloviter RS, Dean E, Sollas AL, Goodman JH. Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J Comp Neurol. 1996;366(3): 516-33.
79. Charriaut-Marlangue C, Ben-Ari Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport. 1995;7(1):61-4.
80. Roy M, Hom JJ, Sapolsky RM. HSVmediated delivery of virally derived antiapoptotic genes protects the rat hippocampus from damage following excitotoxicity, but not metabolic disruption. Gene Ther. 2002;9(3):214-9.
81. Yamamoto A, Murphy N, Schindler CK, So NK, Stohr S, Taki W, et al. Endoplasmic reticulum stress and apoptosis signaling in human temporal lobe epilepsy. J Neuropathol Exp Neurol. 2006; 65(3):217-25.
82. Schindler CK, Pearson EG, Bonner HP, So NK, Simon RP, Prehn JH, et al. Caspase-3 cleavage and nuclear localization of caspase- activated DNase in human temporal lobe epilepsy. J Cereb Blood Flow Metab. 2006;26(4):583-9.
83. Yamamoto A, Schindler CK, Murphy BM, Bellver-Estelles C, So NK, Taki W, et al. Evidence of tumor necrosis factor receptor 1 signaling in human temporal lobe epilepsy. Exp Neurol. 2006;202(2):410-20.
84. Kilany A, Raouf ER, Gaber AA, Aloush TK, Aref HA, Anwar M, et al. Elevated serum Bcl-2 in children with temporal lobe epilepsy. Seizure. 2012;21(4):250-3.
85. Sakhi S, Bruce A, Sun N, Tocco G, Baudry M, Schreiber SS. p53 induction is associated with neuronal damage in the central nervous system. Proc Natl Acad Sci USA. 1994;91(16):7525-9.
86. Liu H, Cao Y, Basbaum AI, Mazarati AM, Sankar R, Wasterlain CG. Resistance to excitotoxin-induced seizures and neuronal death in mice lacking the preprotachykinin A gene. Proc Natl Acad Sci USA. 1999;96(21):12096-101.
87. Lopez-Meraz ML, Wasterlain CG, Rocha LL, Allen S, Niquet J. Vulnerability of postnatal hippocampal neurons to seizures varies regionally with their maturational stage. Neurobiol Dis. 2010;37(2):394-402.
88. Culmsee C, Zhu X, Yu QS, Chan SL, Camandola S, Guo Z, et al. A synthetic inhibitor of p53 protects neurons against death induced by ischemic and excitotoxic insults, and amyloid beta-peptide. J Neurochem. 2001;77(1):220-8.
89. Morrison RS, Wenzel HJ, Kinoshita Y, Robbins CA, Donehower LA, Schwartzkroin PA. Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci. 1996;16(4):1337-45.
90. Zeiss CJ. The apoptosis-necrosis continuum: insights from genetically altered mice. Vet Pathol. 2003;40(5): 481-95.
91. Schmechel DE. Apoptosis in neurodegenerative disorders. In: Hannum YA, Boustany RM, editors. Apoptosis in neurobiology. Washington DC: CRC Press; p. 23-48.
92. Martin LJ. Neuronal cell death in nervous system development, disease, and injury (Review). Int J Mol Med. 2001;7(5): 455-78.
93. Lorigados L, Orozco S, Morales L, García I, Estupiñán B, Bender JE, et al. Muerte neuronal en la neocorteza de pacientes con epilepsia del lóbulo temporal resistente a fármacos. Neurología. 2008;23(9):555-65.
94. Lopez J, Gonzalez ME, Lorigados L, Morales L, Riveron G, Bauza JY. Oxidative stress markers in surgically treated patients with refractory epilepsy. Clin Biochem. 2007;40(5-6):292-8.
95. Pitkanen A. Drug-mediated neuroprotection and antiepileptogenesis: animal data. Neurology. 2002;59(9 Suppl 5): S27-33.