Kainic acid-induced seizures produce necrotic, not apoptotic, neurons with internucleosomal DNA cleavage: Implications for programmed cell death mechanisms

Neuroscience

Volumn 98, Issue 1, 2000, Pages 41-53

  Fujikawa, D G ^a,b   Shinmei, S S ^a   Cai, B ^a,b  

^a Vet Aff Gtr LA Hlthcare Syst   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; DNA laddering; Necrosis; Programmed cell death; Status epilepticus; TUNEL

Indexed keywords

DIAZEPAM; DIZOCILPINE; DNA; EOSIN; HEMATOXYLIN; KAINIC ACID; PHENOBARBITAL;

AGAR GEL ELECTROPHORESIS; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN REGION; CELL DEATH; CELL NUCLEUS MEMBRANE; CELL STRUCTURE; CELL VACUOLE; CHROMATIN; CHROMATIN CONDENSATION; CONTROLLED STUDY; CYTOPLASM; DNA CLEAVAGE; ELECTRON MICROSCOPY; EPILEPTIC STATE; MALE; MICROSCOPY; MITOCHONDRION; NERVE CELL LESION; NEWBORN; NICK END LABELING; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; RAT; SEIZURE; STAINING;

ANIMALS; APOPTOSIS; DIZOCILPINE MALEATE; DNA FRAGMENTATION; ENTORHINAL CORTEX; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HIPPOCAMPUS; IN SITU NICK-END LABELING; KAINIC ACID; MALE; MICROSCOPY, ELECTRON; NECROSIS; NEURONS; NUCLEOSOMES; RATS; RATS, WISTAR; SEIZURES; STATUS EPILEPTICUS;

EID: 0034085349     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00085-3     Document Type: Article

References (69)

1. Becker A.J., Gillardon F., Blümke I., Langendörfer D., Beck H., Wiestler O.D. Differential regulation of apoptosis-related genes in resistant and vulnerable subfields of the rat epileptic hippocampus. Molec Brain Res. 67:1999;172-176.
2. Bengzon J., Kokaia Z., Elmér E., Nanobashvili A., Kokaia M., Lindvall O. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. natn. Acad. Sci. U.S.A. 94:1997;10,432-10,437.
3. Berg M., Bruhn T., Johansen F.F., Diemer N.H. Kainic acid-induced seizures and brain damage in the rat: different effects of NMDA- and AMPA receptor antagonists. Pharmac. Toxicol. 73:1993;262-268.
4. Brown A.W., Brierley J.B. Anoxic-ischaemic cell change in rat brain: light microscopic and fine-structural observations. J. neurol. Sci. 16:1972;59-84.
5. Charriaut-Marlangue C., Ben-Ari Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. NeuroReport. 7:1995;61-64.
6. Clifford D.B., Olney J.W., Benz A.M., Fuller T.A., Zorumski C.F. Ketamine, phencyclidine and MK-801 protect against kainic acid-induced seizure-related brain damage. Epilepsia. 31:1990;382-390.
7. Colbourne F., Sutherland G.R., Auer R.N. Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J. Neurosci. 19:1999;4200-4210.
8. Collins R.J., Harmon B.V., Gobé G.C., Kerr J.F. Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. Int. J. Radiat. Biol. 61:1992;451-453.
9. Dong Z., Saikumar P., Weinberg J.M., Venkatachalam M.A. Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Involvement of serine but not cysteine proteases. Am. J. Path. 151:1997;1205-1213.
10. Evans M.C., Griffiths T., Meldrum B.S. Kainic-acid seizures and the reversibility of calcium loading in vulnerable neurons in the hippocampus. Neuropath. appl. Neurobiol. 10:1983;285-302.
11. Faherty C.J., Xanthoudakis S., Smeyne R.J. Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment. Molec. Brain Res. 70:1999;159-163.
12. Fariello R.G., Golden G.T., Smith G.G., Reyes P.F. Potentiation of kainic acid epileptogenicity and sparing from neuronal damage by an NMDA receptor antagonist. Epilepsy Res. 3:1989;206-213.
13. Ferrer I., Martin F., Serrano T., Reiriz J., Pérez-Navarro E., Alberch J., Macaya A., Planas A.M. Both apoptosis and necrosis occur following intrastriatal administration of excitotoxins. Acta neuropath., Berlin. 90:1995;504-510.
14. Filipkowski R.K., Hetman M., Kaminska B., Kaczmarek L. DNA fragmentation in rat brain after administration of kainate. NeuroReport. 5:1994;1538-1540.
15. Fujikawa D.G. The neuroprotective effect of ketamine administered after status epilepticus onset. Epilepsia. 36:1995;186-195.
16. Fujikawa D.G. The temporal evolution of neuronal damage from pilocarpine-induced status epilepticus. Brain Res. 725:1996;11-22.
17. Fujikawa D.G., Daniels A.H., Kim J.S. The competitive NMDA-receptor antagonist CGP 40116 protects against status epilepticus-induced neuronal damage. Epilepsy Res. 17:1994;207-219.
18. Fujikawa D.G., Kim J.S., Daniels A.H., Alcaraz A.F., Sohn T.B. In vivo elevation of extracellular potassium in the rat amygdala increases extracellular glutamate and aspartate and damages neurons. Neuroscience. 74:1996;695-706.
19. Fujikawa D.G., Cai B., Shinmei S.S., Allen S.G. Neuronal death from kainic-acid-induced seizures is morphologically necrotic despite "apoptotic" biochemical features. Soc. Neurosci. Abstr. 23:1998;757.
20. Fujikawa D.G., Shinmei S.S., Cai B. Lithium-pilocarpine-induced status epilepticus produces necrotic neurons with internucleosomal DNA fragmentation in adult rats. Eur. J. Neurosci. 11:1999;1605-1614.
21. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:1992;493-501.
22. Gillardon F., Wickert H., Zimmerman M. Up-regulation of bax and down-regulation of bcl-2 is associated with kainate-induced apoptosis in mouse brain. Neurosci. Lett. 192:1995;85-88.
23. Gillardon F., Böttinger B., Schmitz B., Zimmerman M., Hossmann K.-A. Activation of CPP-32 protease in hippocampal neurons following ischemia and epilepsy. Molec. Brain Res. 50:1997;16-22.
24. Gold R., Schmied M., Giegerich G., Breitschopf H., Hartung H.P., Toyka K.V., Lassmann H. Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Lab. Invest. 71:1994;219-225.
25. Grasl-Kraupp B., Ruttkay-Nedecky B., Koudelka H., Bukowska K., Bursch W., Schulte-Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis and autolytic cell death: a cautionary note. Hepatology. 21:1995;1465-1468.
26. Gwag B.J., Koh J.-Y., Demaro J.A., Ying H.S., Jacquin M., Choi D.W. Slowly triggered excitotoxicity occurs by necrosis in cortical cultures. Neuroscience. 77:1997;393-401.
27. Higuchi M., Honda T., Proske R., Yeh E. Regulation of reactive oxygen species-induced apoptosis and necrosis by caspase 3-like proteases. Oncogene. 17:1998;2753-2760.
28. Ikonomidou C., Bosch F., Miksa M., Bittigau P., Vöckler J., Dikranian K., Tenkova T.I., Stefovska V., Turski L., Olney J.W. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science. 283:1999;70-74.
29. Ingvar M., Morgan P.F., Auer R.N. The nature and timing of excitotoxic neuronal necrosis in the cerebral cortex, hippocampus and thalamus due to flurothyl-induced status epilepticus. Acta neuropath., Berlin. 75:1988;362-369.
30. Ishimaru M.J., Ikonomidou C., Tenkova T.I., Der T.C., Dikranian K., Sesma M.A., Olney J.W. Distinguishing excitotoxic from apoptotic neurodegeneration in the developing rat brain. J. comp. Neurol. 408:1999;461-476.
31. Kerr J.F.R., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 26:1972;239-257.
32. Koh J.-Y., Goldberg M.P., Hartley D.M., Choi D.W. Non-NMDA receptor-mediated neurotoxicity in cortical culture. J. Neurosci. 10:1990;693-705.
33. Liu H., Cao Y., Basbaum A.I., Mazarati A.M., Sankar R., Wasterlain C.G. Resistance to excitotoxin-induced seizures and neuronal death in mice lacking the preprotachykinin A gene. Proc. natn. Acad. Sci. U.S.A. 96:1999;12,096-12,101.
34. Liu W., Bi X., Tocco G., Baudry M., Schreiber S.S. Increased expression of cyclin D1 in the adult rat brain following kainic acid treatment. NeuroReport. 7:1996;2785-2789.
35. Lobner D., Choi D.W. Preincubation with protein synthesis inhibitors protects cortical neurons against oxygen-glucose deprivation-induced death. Neuroscience. 72:1996;335-341.
36. López 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. 91:1999;1461-1470.
37. Martin D.P., Schmidt R.E., DiStefano P.S., Lowry O.H., Carter J.G., Johnson E.M. Jr. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106:1988;829-844.
38. Mikati M.A., Werner S., Gatt A., Liu Z., Rahmeh A.A., Rachid R.A., Stafstrom C.E., Holmes G.L. Consequences of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor blockade during status epilepticus in the developing brain. Devl Brain Res. 113:1999;139-142.
39. Morrison R.S., Wenzel H.J., Kinoshita Y., Robbins C.A., Donehower L.A., Schwartzkroin P.A. Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J. Neurosci. 16:1996;1337-1345.
40. Olney J.W., Rhee V., Ho O.L. Kainic acid: a powerful neurotoxic analogue of glutamate. Brain Res. 77:1974;507-512.
41. Olney J.W., deGubareff T., Sloviter R.S. "Epileptic" brain damage in rats induced by sustained electrical stimulation of the perforant path. II. Ultrastructural analysis of acute hippocampal pathology. Brain Res. Bull. 10:1983;699-712.
42. Parent J.M., Yu T.M., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17:1997;3727-3738.
43. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 1986;Academic, Orlando.
44. Petito C.K., Torres-Munoz T., Roberts B., Olarte J.P., Nowak T.S. Jr, Pulsinelli W.A. DNA fragmentation follows delayed neuronal death in CA1 neurons exposed to transient global ischemia in the rat. J. Cereb. Blood Flow Metab. 17:1997;967-976.
45. Pohl D., Bittigau P., Ishimaru M.J., Stadthaus D., Hübner C., Olney J.W., Turski L., Ikonomidou C. N-Methyl-D-aspartate antagonists and apoptotic cell death triggered by head trauma in developing rat brain. Proc. natn. Acad. Sci. U.S.A. 96:1999;2508-2513.
46. Pollard H., Charriaut-Marlangue C., Cantagrel S., Represa A., Robain O., Moreau J., Ben-Ari Y. Kainate-induced apoptotic cell death in hippocampal neurons. Neuroscience. 63:1994;7-18.
47. Portera-Cailliau C., Hedreen J.C., Price D.L., Koliatsos V.E. Evidence for apoptotic cell death in Huntington Disease and excitotoxic animal models. J. Neurosci. 15:1995;3775-3787.
48. Portera-Cailliau C., Price D.L., Martin L.J. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis continuum. J. comp. Neurol. 378:1997;70-87.
49. Portera-Cailliau C., Price D.L., Martin L.J. Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in adult brain are morphologically distinct: further evidence for an apoptosis-necrosis continuum. J. comp. Neurol. 378:1997;88-104.
50. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. clin. Neurophysiol. 32:1972;281-294.
51. Sakhi S., Bruce A., Sun N., Tocco G., Baudry M., Schreiber S.S. p53 induction is associated with neuronal damage in the central nervous system. Proc. natn. Acad. Sci. U.S.A. 91:1994;7525-7529.
52. Sakhi S., Sun N., Wing L.L., Mehta P., Schreiber S.S. Nuclear accumulation of p53 protein following kainic acid-induced seizures. NeuroReport. 7:1996;493-496.
53. Schauwecker P.E., Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. natn. Acad. Sci. U.S.A. 94:1997;4103-4108.
54. Schreiber S.S., Tocco G., Najm I., Thompson R.F., Baudry M. Cycloheximide prevents kainate-induced neuronal death and c-fos expression in adult rat brain. J. Molec. Neurosci. 4:1993;149-159.
55. Schwob J.E., Fuller T., Price J.L., Olney J.W. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience. 5:1980;991-1014.
56. Shimizu S., Eguchi Y., Kamiike W., Waguri S., Uchiyama Y., Matsuda H., Tsujimoto Y. Retardation of chemical hypoxia-induced necrotic cell death by Bcl-2 and ICE inhibitors: possible involvement of common mediators in apoptotic and necrotic signal transductions. Oncogene. 12:1996;2045-2050.
57. Simonian N.A., Getz R.L., Leveque J.C., Konradi C., Coyle J.T. Kainate induces apoptosis in neurons. Neuroscience. 74:1996;675-683.
58. Sloviter R.S., Dean E., Neubort S. Electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat: apoptosis in the adult central nervous system. J. comp. Neurol. 330:1993;337-351.
59. Sloviter R.S., Dean E., Sollas A.L., Goodman J.H. Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J. comp. Neurol. 366:1996;516-533.
60. Sohn S., Kim E.Y., Gwag B.J. Glutamate neurotoxicity in mouse cortical neurons: atypical necrosis with DNA ladders and chromatin condensation. Neurosci. Lett. 240:1998;47-150.
61. Sperk G., Lassmann H., Baran H., Kish S.J., Seitelberger F., Hornykiewicz O. Kainic acid induced seizures: neurochemical and histopathological changes. Neuroscience. 10:1983;1301-1315.
62. Suzuki A. Amyloid-beta protein induces necrotic cell death mediated by ICE cascade in PC12 cells. Expl Cell Res. 234:1997;507-511.
63. Timsit S., Rivera S., Ouaghi P., Guischard F., Tremblay E., Ben-Ari Y., Khrestchatisky M. Increased cyclin D1 in vulnerable brain regions in the hippocampus after ischaemia and epilepsy: a modulator of in vivo programmed cell death? Eur. J. Neurosci. 11:1999;263-278.
64. Tuunanen J., Lukasiuk K., Halonen T., Pitkänen A. Status epilepticus-induced neuronal damage in the rat amygdaloid complex: distribution, time-course and mechanisms. Neuroscience. 94:1999;473-495.
65. van Lookeren Campagne M., Lucassen P.J., Vermeulen J.P., Balázs R. NMDA and kainate induce internucleosomal DNA cleavage associated with both apoptotic and necrotic cell death in the neonatal rat brain. Eur. J. Neurosci. 7:1995;1627-1640.
66. van Lookeren Campagne M., Gill R. Ultrastructural morphological changes are not characteristic of apoptotic cell death following focal cerebral ischemia in the rat. Neurosci. Lett. 213:1996;111-114.
67. Wüllner U., Weller M., Groscurth P., Löschmann P.A., Schulz J.B., Müller I., Klockgether T. Evidence for an active type of cell death with ultrastructural features distinct from apoptosis: the effects of 3-acetylpyridine neurotoxicity. Neuroscience. 81:1997;721-734.
68. Wyllie A. H. (1981) Cell death: a new classification separating apoptosis from necrosis. In Cell Death in Biology and Pathology (eds Bowen I. D. and Lockshin R. A.). Chapman and Hall, London.
69. Wyllie A.H., Kerr J.F.R., Currie A.R. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:1980;251-306.