Preservation of mitochondrial integrity and energy metabolism during experimental status epilepticus leads to neuronal apoptotic cell death in the hippocampus of the rat

Seizure

Volumn 18, Issue 6, 2009, Pages 420-428

  Chuang, Yao Chung ^a   Lin, Jui Wei ^a   Chen, Shang Der ^a   Lin, Tsu Kung ^a   Liou, Chia Wei ^a   Lu, Cheng Hsien ^a   Chang, Wen Neng ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

Apoptosis; ATP; Energy metabolism; Hippocampus; Mitochondrial integrity; Status epilepticus

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE 3; KAINIC ACID; PENICILLIN G SODIUM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DNA FRAGMENTATION; ELECTRON MICROSCOPY; ENERGY METABOLISM; EPILEPTIC STATE; EXPERIMENTAL MODEL; GOLGI COMPLEX; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; MICROINJECTION; MITOCHONDRION; NERVE CELL MEMBRANE; NERVE CELL NECROSIS; NICK END LABELING; NONHUMAN; POSTOPERATIVE INFECTION; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RAT; ROUGH ENDOPLASMIC RETICULUM; SEIZURE; STAINING; TEMPORAL LOBE;

ADENOSINE TRIPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; CASPASE 3; DISEASE MODELS, ANIMAL; DNA FRAGMENTATION; ENERGY METABOLISM; EXCITATORY AMINO ACID AGONISTS; HIPPOCAMPUS; IN SITU NICK-END LABELING; KAINIC ACID; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NEURONS; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, SPRAGUE-DAWLEY; STATUS EPILEPTICUS; TIME FACTORS;

EID: 67349288138     PISSN: 10591311     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.seizure.2009.03.002     Document Type: Article

References (42)

1. Henshall D.C., and Simon R.P. Epilepsy and apoptosis pathways. J Cereb Blood Flow Metab 25 (2005) 1557-1572
2. Fujikawa D.G. Prolonged seizures and cellular injury: understanding the connection. Epilepsy Behav 7 Suppl 3 (2005) S3-11
3. Sutula T.P., Hagen J., and Pitkänen A. Do epileptic seizures damage the brain?. Curr Opin Neurol 16 (2003) 189-195
4. Haut S.R., Velisková J., and Moshé S.L. Susceptibility of immature and adult brains to seizure effects. Lancet Neurol 3 (2004) 608-617
5. Chen J.W.Y., and Wasterlain C.G. Status epilepticus: pathophysiology and management in adults. Lancet Neurol 5 (2006) 246-256
6. Shorvon S. Does convulsive status epilepticus (SE) result in cerebral damage or affect the course of epilepsy-the epidemiological and clinical evidence?. Prog Brain Res 135 (2002) 85-93
7. Bengzon J., Mohapel P., Ekdahl C.T., and Lindvall O. Neuronal apoptosis after brief and prolonged seizures. Prog Brain Res 135 (2002) 111-119
8. Narkilahti S., Pirttila T.J., Lukasiuk K., Tuunanen J., and Pitkanen A. Expression and activation of caspase 3 following status epilepticus in the rat. Eur J Neurosci 18 (2003) 1486-1496
9. Weise J., Engelhorn T., Dorfler A., Aker S., Bahr M., and Hufnagel A. Expression time course and spatial distribution of activated caspase-3 after experimental status epilepticus: contribution of delayed neuronal cell death to seizure-induced neuronal injury. Neurobiol Dis 18 (2005) 582-590
10. Daugas E., Nochy D., Ravagnan L., Loeffler M., Susin S.A., Zamzami N., et al. Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett 476 (2000) 118-123
11. Kroemer G. Mitochondrial control of apoptosis: an overview. Biochem Soc Symp 66 (1999) 1-15
12. Eguchi Y., Shimizu S., and Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 57 (1997) 1835-1840
13. Halestrap A.P., Clarke S.J., and Javadov S.A. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res 61 (2004) 372-385
14. Leist M., Single B., Castoldi A.F., Kuhnle S., and Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185 (1997) 1481-1486
15. Chuang Y.C., Chang A.Y.W., Lin J.W., Hsu S.P., and Chan S.H.H. Mitochondrial dysfunction and ultrastructural damage in the hippocampus during kainic acid-induced status epilepticus in the rat. Epilepsia 45 (2004) 1202-1209
16. Chuang Y.C., Chen S.D., Liou C.W., Lin T.K., Chang W.N., Chan S.H.H., et al. Contribution of nitric oxide, superoxide anion, and peroxynitrite to activation of mitochondrial apoptotic signaling in hippocampal CA3 subfield following experimental temporal lobe status epilepticus. Epilepsia 50 (2009) 731-746
17. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14 (1985) 375-403
18. Henshall D.C., Sinclair J., and Simon R.P. Relationship between seizure-induced transcription of the DNA damage-inducible gene GADD45, DNA fragmentation, and neuronal death in focally evoked limbic epilepsy. J Neurochem 73 (1999) 1573-1583
19. Chuang Y.C., Chen S.D., Lin T.K., Liou C.W., Chang W.N., Chan S.H.H., 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 52 (2007) 1263-1273
20. Chan S.H.H., Wu K.L.H., Wang L.L., and Chan J.Y.H. Nitric oxide- and superoxide-dependent mitochondrial signaling in endotoxin-induced apoptosis in the rostral ventrolateral medulla of rats. Free Radic Biol Med 39 (2005) 603-618
21. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., and Lipton S.A. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 92 (1995) 7162-7166
22. Endo H., Kamada H., Nito C., Nishi T., and Chan P.H. Mitochondrial translocation of p53 mediates release of cytochrome c and hippocampal CA1 neuronal death after transient global cerebral ischemia in rats. J Neurosci 26 (2006) 7974-7983
23. Lu K., Liang C.L., Chen H.J., Chen S.D., Hsu H.C., Liliang P.C., et al. Injury severity and cell death mechanisms: effects of concomitant hypovolemic hypotension on spinal cord ischemia-reperfusion in rats. Exp Neurol 185 (2004) 120-132
24. Chen S.D., Wu H.Y., Yang D.I., Lee S.Y., Shaw F.Z., Lin T.K., et al. Effects of rosiglitazone on global ischemia-induced hippocampal injury and expression of mitochondrial uncoupling protein 2. Biochem Biophys Res Commun 351 (2006) 198-203
25. Chan J.Y.H., Cheng H.L., Chou J.L.J., Li F.C.H., Dai K.Y., Chan S.H.H., et al. Heat shock protein 60 or 70 activates nitric-oxide synthase (NOS) I- and inhibits NOS II-associated signaling and depresses the mitochondrial apoptotic cascade during brain stem death. J Biol Chem 282 (2007) 4585-4600
26. Yen D.H.T., Chan J.Y.H., Huang C.I., Lee C.H., Chan S.H.H., and Chang A.Y.W. Coenzyme Q10 confers cardiovascular protection against acute mevinphos intoxication by ameliorating bioenergetic failure and hypoxia in the rostral ventrolateral medulla of the rat. Shock 23 (2005) 353-359
27. Schindler C.K., Pearson E.G., Bonner H.P., So N.K., Simon R.P., Prehn J.H., et al. Caspase-3 cleavage and nuclear localization of caspase-activated DNase in human temporal lobe epilepsy. J Cereb Blood Flow Metab 26 (2006) 583-589
28. Liou A.K.F., Clark R.S., Henshall D.C., Yin X.M., and 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 69 (2003) 103-142
29. Halestrap A. Biochemistry: a pore way to die. Nature 434 (2005) 578-579
30. Tejada S., Sureda A., Roca C., Gamundi A., and Esteban S. Antioxidant response and oxidative damage in brain cortex after high dose of pilocarpine. Brain Res Bull 71 (2007) 372-375
31. Patel M. Mitochondrial dysfunction and oxidative stress: cause and consequence of epileptic seizures. Free Radic Biol Med 37 (2004) 1951-1962
32. Lossi L., and Merighi A. In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS. Prog Neurobiol 69 (2003) 287-312
33. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J.A., et al. Mitochondrial Complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem 278 (2003) 8516-8525
34. Pelicano H., Feng L., Zhou Y., Carew J.S., Hileman E.O., Plunkett W., et al. Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J Biol Chem 278 (2003) 37832-37839
35. Chauvin C., De Oliveira F., Ronot X., Mousseau M., Leverve X., and Fontaine E. Rotenone inhibits the mitochondrial permeability transition-induced cell death in U937 and KB cells. J Biol Chem 276 (2001) 41394-41398
36. Majno G., and Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146 (1995) 3-15
37. Hatefi Y. The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 54 (1985) 1015-1069
38. Galella G., Turano C., and Girvin J. Metabolic changes in the hippocampus after prolonged epileptic discharge. J Neurosurg Sci 27 (1983) 69-71
39. Bengzon J., Kokaia Z., Elmer E., Nanobashvili A., Kokaia M., and Lindvall O. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci USA 94 (1997) 10432-10437
40. Henshall D.C., Chen J., and Simon R.P. Involvement of caspase-3-like protease in the mechanism of cell death following focally evoked limbic seizures. J Neurochem 74 (2000) 1215-1223
41. Fujikawa D.G., Shinmei S.S., and Cai B. Lithium-pilocarpine-induced status epilepticus produces necrotic neurons with internucleosomal DNA fragmentation in adult rats. Eur J Neurosci 11 (1999) 1605-1614
42. Fujikawa D.G., Shinmei S.S., and Cai B. Kainic acid-induced seizures produce necrotic, not apoptotic, neurons with internucleosomal DNA cleavage: implications for programmed cell death mechanisms. Neuroscience 98 (2000) 41-53