Neuronal cell death in a rat model for mesial temporal lobe epilepsy is induced by the initial status epilepticus and not by later repeated spontaneous seizures

Epilepsia

Volumn 44, Issue 5, 2003, Pages 647-658

  Gorter, Jan A ^a,b,d   Gonçalves Pereira, Pedro M ^a   Van Vliet, Erwin A ^a   Aronica, Eleonora ^b,c   Lopes da Silva, Fernando H ^a,b   Lucassen, Paul J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b STICHTING EPILEPSIE INSTELLINGEN NEDERLAND SEIN   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d NONE   (Netherlands)

Author keywords

Apoptosis; Epileptogenesis; Fluoro Jade; Necrosis; Parahippocampal region; Progression; Sclerosis; TUNEL

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE COURSE; DISEASE SEVERITY; ELECTROSTIMULATION; EPILEPTIC STATE; HIPPOCAMPUS; MALE; NERVE CELL; NERVE CELL NECROSIS; NICK END LABELING; NISSL SUBSTANCE; NONHUMAN; PRIORITY JOURNAL; RAT; SCLEROSIS; TEMPORAL LOBE EPILEPSY;

ANIMALS; APOPTOSIS; CELL COUNT; CELL DEATH; CHRONIC DISEASE; DISEASE PROGRESSION; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; IN SITU NICK-END LABELING; KINDLING, NEUROLOGIC; MALE; NECROSIS; PARAHIPPOCAMPAL GYRUS; RATS; RATS, SPRAGUE-DAWLEY; RISK FACTORS; SCLEROSIS; STATUS EPILEPTICUS;

EID: 0038666150     PISSN: 00139580     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1528-1157.2003.53902.x     Document Type: Article

References (47)

1. Mathern GW, Babb TL, Leite JP, et al. The pathogenic and progressive features of chronic human hippocampal epilepsy. Epilepsy Res 1996;26:151-61.
2. Sutula TP, Pitkanen A. More evidence for seizure-induced neuron loss: is hippocampal sclerosis both cause and effect of epilepsy? Neurology 2001;57:169-70.
3. Bengzon J, Kokaia Z, Elmer E, et al. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci U S A 1997;94:10432-7.
4. Cavazos JE, Das I, Sutula TP. Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci 1994;14:3106-21.
5. Bertram EH, Lothman EW. Morphometric effects of intermittent kindled seizures and limbic status epilepticus in the dentate gyrus of the rat. Brain Res 1993;603:25-31.
6. Adams B, Sazgar M, Osehobo P, et al. Nerve growth factor accelerates seizure development, enhances mossy fiber sprouting, and attenuates seizure-induced decreases in neuronal density in the kindling model of epilepsy. J Neurosci 1997;17:5288-96.
7. Schwob JE, Fuller T, Price JL, et al, Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience 1980;5:991-1014.
8. Nevander G, Ingvar M, Auer R, et al. Status epilepticus in welloxygenated rats causes neuronal necrosis. Ann Neurol 1985;18:281-90.
9. Du F, Eid T, Lothman EW, et al. Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J Neurosci 1995;15:6301-13.
10. Bertram EH, Lothman EW, Lenn NJ. The hippocampus in experimental chronic epilepsy: a morphometric analysis. Ann Neurol 1990;27:43-8.
11. Liu Z, Nagao T, Desjardins GC, et al. Quantitative evaluation of neuronal loss in the dorsal hippocampus in rats with long-term pilocarpine seizures. Epilepsy Res 1994;17:237-47.
12. Gorter JA, Van Vliet EA, Aronica E, et al. Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin-immunoreactive neurons. Eur J Neurosci 2001;13:657-69.
13. Schmued LC, Albertson C, Slikker W Jr. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 1997;751:37-46.
14. Lothman EW, Bertram EH, Bekenstein JW, et al. Self-sustaining limbic status epilepticus induced by "continuous" hippocampal stimulation: electrographic and behavioral characteristics. Epilepsy Res 1989;3:107-19.
15. Racine RJ. Modification of seizure activity by electrical stimulation, II: motor seizure. Electroencephalogr Clin Neurophysiol 1972;32:281-94.
16. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501.
17. Lucassen PJ, Chung WC, Vermeulen JP, et al. Microwaveenhanced in situ end-labeling of fragmented DNA: parametric studies in relation to postmortem delay and fixation of rat and human brain. J Histochem Cytochem 1995;43:1163-71.
18. English HF, Kyprianou N, Isaacs JT. Relationship between DNA fragmentation and apoptosis in the programmed cell death in the rat prostate following castration. Prostate 1989;15:233-50.
19. Lucassen PJ, Negoescu A, Labat-Moleur F, et al. Microwave enhanced in situ end labelling of apoptotic cells in tissue sections; pitfalls and possibilities. In: Shi SR, Gu J, Taylor CR, eds. Antigen retrieval techniques. Natick, Mass.: Eaton Publishing, 2000:71-91.
20. Amaral DG, Witter MP. Hippocampal formation. In: Paxinos G, ed. The rat nervous system. 2nd ed. London: Academic Press, 1995:443-93.
21. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. San Diego: Academic Press, 1998.
22. Aronica E, Yankaya B, Troost D, et al. Induction of neonatal sodium channel II and III alpha isoform mRNAs in neurons and microglia after status epilepticus in the rat hippocampus. Eur J Neurosci 2001;13:1261-6.
23. Eriksson C, Van Dam AM, Lucassen PJ, et al. Immunohistochemical localization of interleukin-1beta, interleukin-1 receptor antagonist and interleukin-1beta converting enzyme/caspase-1 in the rat brain after peripheral administration of kainic acid. Neuroscience 1999;93:915-30.
24. Kubova H, Druga R, Lukasiuk K, et al. Status epilepticus causes necrotic damage in the mediodorsal nucleus of the thalamus in immature rats. J Neurosci 2001;21:3593-9.
25. Sato M, Chang E, Igarashi T, et al. Neuronal injury and loss after traumatic brain injury: time course and regional variability. Brain Res 2001;917:45-54.
26. Ingvar M, Morgan PF, Auer RN. The nature and timing of excitotoxic neuronal necrosis in the cerebral cortex, hippocampus and thalamus due to flurothyl-induced status epilepticus. Acta Neuropathol 1988;75:362-9.
27. Covolan L, Mello LE. Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus. Epilepsy Res 2000;39:133-52.
28. Poirier JL, Capek R, De Koninck Y. Differential progression of dark neuron and Fluoro-Jade labelling in the rat hippocampus following pilocarpine-induced status epilepticus. Neuroscience 2000;97:59-68.
29. Tuunanen J, Lukasiuk K, Halonen T, et al. Status epilepticusinduced neuronal damage in the rat amygdaloid complex: distribution, time-course and mechanisms. Neuroscience 1999;94:473-95.
30. Sloviter RS, Dean E, Sollas AL, et al. Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J Comp Neurol 1996;366:516-33.
31. Fujikawa DG, Shinmei SS, Cai B. Lithium-pilocarpine-induced status epilepticus produces necrotic neurons with internucleosomal DNA fragmentation in adult rats. Eur J Neurosci 1999;11:1605-14.
32. Roy M, Sapolsky R. Neuronal apoptosis in acute necrotic insults: why is this subject such a mess? Trends Neurosci 1999;22:419-22.
33. Kondratyev A, Gale K. Intracerebral injection of caspase-3 inhibitor prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Brain Res Mol Brain Res 2000;75:216-24.
34. Mello LE, Covolan L. Spontaneous seizures preferentially injure interneurons in the pilocarpine model of chronic spontaneous seizures. Epilepsy Res 1996;26:123-9.
35. Pitkanen A, Nissinen J, Nairismagi J, et al. Progression of neuronal damage after status epilepticus and during spontaneous seizures in a rat model of temporal lobe epilepsy. Prog Brain Res 2002;135:67-83.
36. Hopkins KJ, Wang G, Schmued LC. Temporal progression of kainic acid induced neuronal and myelin degeneration in the rat forebrain. Brain Res 2000;864:69-80.
37. Cavazos JE, Sutula TP. Progressive neuronal loss induced by kindling: a possible mechanism for mossy fiber synaptic reorganization and hippocampal sclerosis [published erratum appears in Brain Res 1991 Feb 8;541:179]. Brain Res 1990;527:1-6.
38. Zhang LX, Smith MA, Li XL, et al. Apoptosis of hippocampal neurons after amygdala kindled seizures. Brain Res Mol Brain Res 1998;55:198-208.
39. Mouritzen-Dam AM. Epilepsy and neuron loss in the hippocampus. Epilepsia 1980;21:617-29.
40. Fisher PD, Sperber EF, Moshe SL. Hippocampal sclerosis revisited. Brain Dev 1998;20:563-73.
41. Fernandez G, Effenberger O, Vinz B, et al. Hippocampal malformation as a cause of familial febrile convulsions and subsequent hippocampal sclerosis. Neurology 1998;50:909-17.
42. Jackson GD, Chambers BR, Berkovic SF. Hippocampal sclerosis: development in adult life. Dev Neurosci 1999;21:207-14.
43. Kalviainen R, Salmenpera T, Partanen K, et al. Recurrent seizures may cause hippocampal damage in temporal lobe epilepsy. Neurology 1998;50:1377-82.
44. O'Brien TJ, So EL, Meyer FB, et al. Progressive hippocampal atrophy in chronic intractable temporal lobe epilepsy. Ann Neurol 1999;45:526-9.
45. Tasch E, Cendes F, Li LM, et al. Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy. Ann Neurol 1999;45:568-76.
46. Roch C, Leroy C, Nehlig A, et al. Magnetic resonance imaging in the study of the lithium-pilocarpine model of temporal lobe epilepsy in adult rats. Epilepsia 2002;43:325-35.
47. Liu RS, Lemieux L, Bell GS, et al. A longitudinal quantitative MRI study of community-based patients with chronic epilepsy and newly diagnosed seizures: methodology and preliminary findings. Neuroimage 2001;14::231-43.