Pharmacologic suppression of oxidative damage and dendritic degeneration following kainic acid-induced excitotoxicity in mouse cerebrum

NeuroToxicology

Volumn 29, Issue 4, 2008, Pages 621-627

  Zaja Milatovic, Snjezana ^a   Gupta, Ramesh C ^b   Aschner, Michael ^a   Montine, Thomas J ^c   Milatovic, Dejan ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b MURRAY STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Excitotoxicity; Isoprostanes; Neurodegeneration; Oxidative damage; Spine density

Indexed keywords

CITRULLINE; IBUPROFEN; KAINIC ACID; N TERT BUTYL ALPHA PHENYLNITRONE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITE; DRUG INHIBITION; ENZYME ACTIVITY; EXCITOTOXICITY; FEMALE; MOUSE; NERVE CELL; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; SEIZURE;

ANIMALS; CEREBRUM; CITRULLINE; DENDRITES; DISEASE MODELS, ANIMAL; DRUG INTERACTIONS; FEMALE; FUNCTIONAL LATERALITY; ISOPROSTANES; KAINIC ACID; MICE; MICE, INBRED C57BL; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; NEUROTOXICITY SYNDROMES; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS;

MUS;

EID: 46149099325     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2008.04.009     Document Type: Article

References (75)

1. Anthony D.C., Montine T.J., and Graham D.G. In: Klaasen C.D. (Ed). Casarett and Doull's toxicology: the basic science of poisons (2001), McGraw-Hill, New York 535
2. Asanuma M., Nishibayashi-Asanuma S., Miyazaki I., and Kohno M. Neuroprotective effects of non-steroidal anti-inflammatory drugs by direct scavenging of nitric oxide radicals. J Neurochem 76 (2001) 1895-1904
3. Bagetta G., Rodino P., Paoletti M., Arabia A., Massoud R., and Nistico G. Systemic administration of lithium chloride and tacrine but not kainic acid augments citrulline content of rat brain. Eur J Pharmacol 294 (1995) 341-344
4. 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
5. Ben-Ari Y., and Cossart R. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 23 (2000) 580-587
6. Ben-Ari Y. Cell death and synaptic reorganizations produced by seizures. Epilepsia 42 (2001) 5-7
7. Bolanos J.P., Peuchen S., Heales S.J., Land J.M., and Clark J.B. Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J Neurochem 63 (1994) 910-916
8. Burette A., Zabel U., Weinberg R.J., Schmidt H.H., and Valtschanoff J.G. Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J Neurosci 22 (2002) 8961-8970
9. Breder C.D., Dewitt D., and Kraig R.P. Characterization of inducible cyclooxygenase in rat brain. J Comp Neurol 355 (1995) 296-315
10. Breder C.D., Smith W.L., Raz A., Masferrer J., Seibert K., Needleman P., et al. Distribution and characterization of cyclooxygenase immunoreactivity in the ovine brain. J Comp Neurol 322 (1992) 409-438
11. 2+ entry via AMPA/KA receptors and excitotoxicity in cultured cerebellar Purkinje cells. J Neurosci 14 (1994) 187-197
12. Bruce A.J., and Baudry M. Oxygen free radicals in rat limbic structures after kainate-induced seizures. Free Radic Biol Med 18 (1995) 993-1002
13. Cadenas E., and Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29 (2000) 222-230
14. Carney J.M., and Floyd R.A. Protection against oxidative damage to CNS by alpha-phenyl-tert-butylnitrone (PBN) and other spin-trapping agents: a novel series of nonlipid free radical scavengers. J Mol Neurosci 3 (1991) 47-57
15. Cheng Y., and Sun A.Y. Oxidative mechanisms involved in kainate-induced cytotoxicity in cortical neurons. Neurochem Res 19 (1994) 1557-1564
16. Choi D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1 (1988) 623-634
17. Cock H.R., Tong X., and Hargreaves I.P. Mitochondrial dysfunction associated with neuronal death following status epilepticus in rat. Epilepsy Res 48 (2002) 157-168
18. Coyle J.T., and Puttfarcken P. The effects of oxidative stress on the brain. Science 262 (1993) 689-695
19. Dodrill C.B. Progressive cognitive decline in adolescents and adults with epilepsy. Prog Brain Res 135 (2002) 399-407
20. Dong H., Csernansky C.A., Goico B., and Csernansky J.G. Hippocampal neurogenesis following kainic acid-induced apoptosis in neonatal rats. J Neurosci 23 (2003) 1742-1749
21. Dudek F., Obenaus A., Schweitzer J., and Wuarin J. Functional significance of hippocampal plasticity in epileptic brain: electrophysiological changes of the dentate granule cells associated with mossy fiber sprouting. Hippocampus 4 (1994) 259-265
22. Dugan L.L., Sensi S.L., Canzoniero L.M.T., Handran S.D., Rothman S.M., Lin T.S., et al. Chronic epilepsy and cognition. Lancet Neurol 3 (1995) 663-672
23. + produces progressive neuronal degeneration which is mediated by oxidative stress. Exp Neurol 144 (1997) 193-198
24. Farooqui A.A., Yi Ong W., Lu X.R., Halliwell B., and Horrocks L.A. Neurochemical consequences of kainate-induced toxicity in brain: involvement of arachidonic acid release and prevention of toxicity by phospholipase A(2) inhibitors. Brain Res Rev 38 (2001) 61-78
25. Fetcher L.D., Liu Y., and Pearce T.A. Cochlear protection from carbon monoxide exposure by free radical blockers in the guinea pig. Toxicol Appl Pharmacol 142 (1997) 47-55
26. Frantseva M.V., Velazquez J.L.P., and Hwang P.A. Free radical production correlates with cell death in an in vitro model of epilepsy. Eur J Neurosci 12 (2000) 1431-1439
27. Frederiksson A., Eriksson P., and Archer T. MPTP-induced deficits in motor activity: neuroprotective effects of the spin trapping agents, alpha-phenyl-tert-butylnitrone (PBN). J Neural Trans 104 (1997) 579-592
28. Gido G., Kristian T., and Siesjo B.K. Extracellular potassium in a neocortical cone area after transient focal ischemia. Stroke 28 (1997) 206-210
29. Gupta R.C., Milatovic D., and Dettbarn W.-D. Nitric oxide (NO) modulates high-energy phosphates in brain regions of rats intoxicated with DFP or carbofuran: prevention by PBN or vitamin E. Arch Toxicol 75 (2001) 346-356
30. Gupta R.C., Milatovic D., and Dettbarn W.-D. Depletion of energy metabolites following acetylcholinesterase inhibitor-induced status epilepticus: protection by antioxidants. Neurotoxicology 22 (2001) 271-282
31. Gupta R.C., Milatovic D., Zivin M., and Dettbarn W.-D. Seizure-induced changes in energy metabolites and effects of N-tert-butyl-α-phenylnitrone (PBN) and vitamin E. Pflugers Arch Eur J Physiol 440 (2001) R160-R162
32. Gupta R.C., and Dettbarn W.-D. Prevention of kainic acid seizures-induced changes in levels of nitric oxide and high-energy phosphates by 7-nitroindazole in rat brain regions. Brain Res 981 (2003) 184-192
33. Gupta R.C., Milatovic S., Dettbarn W.-D., Aschner M., and Milatovic D. Neuronal oxidative injury and dendritic damage induced by carbofuran: protection by memantine. Toxicol Appl Pharmacol 219 (2007) 97-105
34. Hamburger S.A., and McCay P.B. Spin trapping of ibuprofen radicals: evidence that ibuprofen is a hydroxyl radical scavenger. Free Radic Res 9 (1990) 337-342
35. Hashimoto K., Watanabe K., Nishimura T., Iyo M., Shirayama Y., and Minabe Y. Behavioral changes and expression of heat shock protein HSP-70 mRNA, brain-derived neurotrophic factor mRNA, and cyclooxygenase-2 mRNA in rat brain following seizures induced by systemic administration of kainic acid. Brain Res 804 (1998) 212-223
36. He Q.P., Smith M.L., Li P.A., and Siesjo B.K. Necrosis of the substantia nigra, pars reticulate, influorothyl-induced status epilepticus is ameliorated by the spin trap alpha-phenyl-N-tert-butylnitrone. Free Radic Biol Med 22 (1997) 917-922
37. Heinemann U., Buchheim K., and Gabriel S. Cell death and metabolic activity during epileptiform discharges and status epilepticus in the hippocampus. Prog Brain Res 135 (2002) 197-210
38. Isokawa M., and Levesque M.F. Increased NMDA responses and dendritic degeneration in human epileptic hippocampal neurons in slices. Neurosci Lett 132 (1991) 212-216
39. Jiang M., Lee C.L., Smith K.L., and Swann J.W. Spine loss and other persistent alterations of hippocampal pyramidal cell dendrites in a model of early-onset epilepsy. J Neurosci 18 (1998) 8356-8368
40. Kelley K.A., Ho L., Winger D., Freire-Moar J., Borelli C.B., Aisen P.S., et al. Potentiation of excitotoxicity in transgenic mice overexpressing neuronal cyclooxygenase-2. Am J Pathol 155 (1999) 995-1004
41. 2 or as SOD mimics?. J Biol Chem 271 (1996) 26026-26031
42. Kunz W.S., Goussakov I.V., and Beck H. Altered mitochondrial oxidative phosphorylation in hippocampal slices of kainate-treated rats. Brain Res 826 (1999) 236-242
43. Lafon-Cazal M., Pietri S., Culcasi M., and Bockaert J. NMDA-dependent superoxide production and neurotoxicity. Nature 364 (1993) 535-537
44. Lancelot E., Revaud M.L., and Boulee R.G. Alpha-N-tert-butylnitrone attenuates excitotoxicity in rat striatum by preventing hydroxyl radical accumulation. Free Radic Biol Med 23 (1997) 1031-1034
45. Leuner B., Falduto J., and Shors T. Associative memory formation increases the observation of dendritic spines in the hippocampus. J Neurosci 23 (2003) 659-665
46. Lizasoain I., Moro M.A., Knowles R.G., Darley-Usmar V., and Moncada S. Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose. Biochem J 314 (1996) 877-880
47. Macdonald R.L., and Stoodley M. Pathophysiology of cerebral ischaemia. Neurol Med Chir (Tokyo) 38 (1998) 1-11
48. Marini H., Altavilla D., Bellomo M., Adamo E.B., Marini R., Laureanti R.F., et al. Modulation of IL-1 beta gene expression by lipid peroxidation inhibition after kainic acid-induced rat brain injury. Exp Neurol 188 (2004) 178-186
49. Milatovic D., Gupta R.C., and Dettbarn W.-D. Involvement of nitric oxide in kainic acid-induced excitotoxicity in rat brain. Brain Res 957 (2002) 330-337
50. Milatovic D., Zaja-Milatovic S., Montine K.S., Horner P.J., and Montine T.J. Pharmacologic suppression of neuronal oxidative damage and dendritic degeneration following direct activation of glial innate immunity in mouse cerebrum. J Neurochem 87 (2003) 1518-1526
51. Milatovic D., Zaja-Milatovic S., Montine K., Shie F.S., and Montine T.J. Neuronal oxidative damage and dendritic degeneration following activation of CD14-dependent innate immunity response in vivo. J Neuroinflamm 1 (2004) 1-20
52. Milatovic D., VanRollins M., Li K., Montine K.S., and Montine T.J. Suppression of cerebral oxidative damage from excitotoxicity and innate immune response in vivo by α- or γ-tocopherol. J Chromatogr B 827 (2005) 88-93
53. Miyajima T., and Kotake Y. Spin trap phenyl-N-tert-butylnitrone (PBN) inhibits induction of nitric oxide synthase in endotoxin-induction in mice. Free Radic Biol Med 22 (1995) 463-470
54. 2 receptor-dependent. J Neurochem 83 (2002) 463-470
55. Montine K.S., Quinn J.F., Zhang J., Fessel J.P., Roberts II L.J., Morrow J.D., et al. Chem Phys Lipids 128 (2004) 117
56. Muller M., Gahwiler B.H., Rietschin L., and Thompson S.M. Reversible loss of dendritic spines and altered excitability after chronic epilepsy in hippocampal slice cultures. Proc Natl Acad Sci USA 90 (1993) 257-261
57. Multani P., Myers R.H., Blume H.W., Schomer D.L., and Sotrel A. Neocortical dendritic pathology in human partial epilepsy: a quantitative Golgi study. Epilepsia 35 (1994) 728-736
58. Murphy M.P., Butler T., Kang D.E., Sterling N., Golde T.E., and Koo E.H. A subset of NSAIDs lower amyloidogenic A[beta]42 independently of cyclo-oxygenase activity. Nature 414 (2001) 212-216
59. Nicholls D.G., and Ward M.W. Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts. Trends Neurosci 23 (2000) 166-174
60. Parathath S., Parathath S., and Tsirka S. Nitric oxide mediates neurodegeneration and breakdown of the blood brain barrier in tPA-dependent excitotoxic injury in mice. J Cell Sci 119 (2006) 339-349
61. Patel M.N. Oxidative stress, mitochondrial dysfunction, and epilepsy. Free Radic Res 36 (2002) 1139-1146
62. Patel M., Liang L.P., and Roberts L.J. Enhanced hippocampal F2-isoprostane formation following kainate-induced seizures. J Neurochem 79 (2001) 1065-1069
63. Phillis J.W., and Clough-Helfman C. Protection from cerebral ischemic injury in gerbils with the spin trap agent N-tert-butyl-alpha-phenylnitrone (PBN). Neurosci Lett 116 (1990) 315-319
64. Sack C.A., Socci D.J., Crandall B.M., and Arendash G.W. Antioxidant treatment with phenyl-alpha-tert-butylnitrone (PBN) improves the cognitive performance and survival of aging rats. Neurosci Lett 205 (1996) 181-184
65. Sandhya T.L., Ong W.Y., Horrocks L.A., and Farooqui A.A. A light and electron microscopic study of cytoplasmic phospholipase A2 and cyclooxygenase-2 in the hippocampus after kainate lesions. Brain Res 788 (1998) 223-231
66. Sanz O., Estrada A., Ferrer I., and Planas A.M. Differential cellular distribution and dynamics of HSP70, cyclooxygenase-2, and c-Fos in the rat brain after transient focal ischemia or kainic acid. Neuroscience 80 (1997) 221-232
67. Schwob J.E., Fuller T., and Price J.L. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience 5 (1980) 991-1014
68. Takemiya T., Maehara M., Matsumura K., Yasuda S., Sugiura H., and Yamagata K. Prostaglandin E2 produced by late induced COX-2 stimulates hippocampal neuron loss after seizure in the CA3 region. Neurosci Res 56 (2006) 103-110
69. Thomas C.E., Ohlweiler D.F., Taylor V.L., and Schmidt C.J. Radical trapping and inhibition of iron-dependent CNS damage by cyclic nitrone spin traps. J Neurochem 68 (1997) 1173-1182
70. Tocco G., Freire-Moar J., Schreiber S.S., Sakhi S.H., Aisen P.S., and Pasinetti G.M. Maturational regulation and regional induction of cyclooxygenase-2 in rat brain: implications for Alzheimer's disease. Exp Neurol 144 (1997) 339-349
71. Uylings H.B., and de Brabander J.M. Neuronal changes in normal human aging and Alzheimer's disease. Brain Cogn 49 (2002) 268-276
72. Weggen S., Eriksen J.L., Das P., Sagi S.A., Wang R., Pietzik C.U., et al. A subset of NSAIDs lower amyloidogenic A[beta]42 independently of cyclo-oxygenase activity. Nature 414 (2001) 212-216
73. Wendland B., Schweize F.E., Ryan T.A., Nakane M., Murad F., Scheller R.H., et al. Existence of nitric oxide synthase in rat hippocampal pyramidal cells. Proc Natl Acad Sci USA 91 (1994) 2151-2155
74. Zhang J., Dawson V.L., Dawson T.M., and Snyder S.H. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 263 (1994) 687-689
75. Zeng L.H., Xu L., Rensing N.R., Sinatra P.M., Rothman S.M., and Wong M. Kainate seizures cause acute dendritic injury and actin depolymerization in vivo. J Neurosci 27 (2007) 11604-11613