Mitochondrial involvement and oxidative stress in temporal lobe epilepsy

Free Radical Biology and Medicine - Tập 62 - Trang 121-131 - 2013
Shane Rowley1, Manisha Patel2,1
1Neuroscience Training Program and School of Pharmacy, University of Colorado at Denver, Aurora, CO 80045, USA
2Department of Pharmaceutical Sciences, School of Pharmacy, University of Colorado at Denver, Aurora, CO 80045, USA

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Hauser, 1991, Risk factors for epilepsy, Epilepsy Res. Suppl., 4, 45

Liang, 2000, Mitochondrial superoxide production in kainate-induced hippocampal damage, Neuroscience, 101, 563, 10.1016/S0306-4522(00)00397-3

Patel, 2001, Enhanced hippocampal F2-isoprostane formation following kainate-induced seizures, J. Neurochem., 79, 1065, 10.1046/j.1471-4159.2001.00659.x

Jarrett, 2008, The ketogenic diet increases mitochondrial glutathione levels, J. Neurochem., 106, 1044, 10.1111/j.1471-4159.2008.05460.x

Garriga-Canut, 2006, 2-Deoxy-D-glucose reduces epilepsy progression by NRSF-CtBP-dependent metabolic regulation of chromatin structure, Nat. Neurosci., 9, 1382, 10.1038/nn1791

Rahman, 2012, Mitochondrial disease and epilepsy, Dev. Med. Child Neurol., 54, 397, 10.1111/j.1469-8749.2011.04214.x

Kawai, 2006, Magnetic resonance imaging and positron emission tomography findings in status epilepticus following severe hypoglycemia, Ann. Nucl. Med., 20, 371, 10.1007/BF02987250

Vielhaber, 2008, Subfield-specific loss of hippocampal N-acetyl aspartate in temporal lobe epilepsy, Epilepsia, 49, 40, 10.1111/j.1528-1167.2007.01280.x

Savic, 2000, In vivo measurements of glutamine+glutamate (Glx) and N-acetyl aspartate (NAA) levels in human partial epilepsy, Acta Neurol. Scand., 102, 179, 10.1034/j.1600-0404.2000.102003179.x

Kann, 2005, Metabolic dysfunction during neuronal activation in the ex vivo hippocampus from chronic epileptic rats and humans, Brain, 128, 2396, 10.1093/brain/awh568

Meldrum, 1993, Excitotoxicity and selective neuronal loss in epilepsy, Brain Pathol. (Zurich), 3, 405, 10.1111/j.1750-3639.1993.tb00768.x

Kilany, 2012, Elevated serum Bcl-2 in children with temporal lobe epilepsy, Seizure, 21, 250, 10.1016/j.seizure.2012.01.004

Henshall, 2000, Alterations in bcl-2 and caspase gene family protein expression in human temporal lobe epilepsy, Neurology, 55, 250, 10.1212/WNL.55.2.250

Duchen, 2000, Mitochondria and calcium: from cell signalling to cell death, J. Physiol., 529, 57, 10.1111/j.1469-7793.2000.00057.x

Chuang, 2009, 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, 731, 10.1111/j.1528-1167.2008.01778.x

Kovács, 2005, Mitochondrial calcium ion and membrane potential transients follow the pattern of epileptiform discharges in hippocampal slice cultures, J. Neurosci, 25, 4260, 10.1523/JNEUROSCI.4000-04.2005

Jarrett, 2008, damage and impaired base excision repair during epileptogenesis, Neurobiol. Dis., 30, 130, 10.1016/j.nbd.2007.12.009

Kunz, 2000, Mitochondrial complex I deficiency in the epileptic focus of patients with temporal lobe epilepsy, Ann. Neurol., 48, 766, 10.1002/1531-8249(200011)48:5<766::AID-ANA10>3.0.CO;2-M

Mueller, 2001, Brain glutathione levels in patients with epilepsy measured by in vivo 1H-MRS, Neurology, 57, 1422, 10.1212/WNL.57.8.1422

Baron, 2007, Mitochondrial dysfunction in neurodegenerative disorders, Biochem. Soc. Transact, 35, 1228, 10.1042/BST0351228

O’Brien, 1997, Hippocampal atrophy is not a major determinant of regional hypometabolism in temporal lobe epilepsy, Epilepsia, 38, 74, 10.1111/j.1528-1157.1997.tb01080.x

Sashindranath, 2010, Early hippocampal oxidative stress is a direct consequence of seizures in the rapid electrical amygdala kindling model, Epilepsy Res., 90, 285, 10.1016/j.eplepsyres.2010.06.005

Frantseva, 2000, Oxidative stress is involved in seizure-induced neurodegeneration in the kindling model of epilepsy, Neuroscience, 97, 431, 10.1016/S0306-4522(00)00041-5

Gluck, 2000, CNS oxidative stress associated with the kainic acid rodent model of experimental epilepsy, Epilepsy Res., 39, 63, 10.1016/S0920-1211(99)00111-4

Peterson, 2002, Hydroethidine detection of superoxide production during the lithium–pilocarpine model of status epilepticus, Epilepsy Res., 49, 226, 10.1016/S0920-1211(02)00047-5

Forster, 1996, Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain, Proc. Natl. Acad. Sci. USA, 93, 4765, 10.1073/pnas.93.10.4765

Floor, 1998, Increased protein oxidation in human substantia nigra pars compacta in comparison with basal ganglia and prefrontal cortex measured with an improved dinitrophenylhydrazine assay, J. Neurochem, 70, 268, 10.1046/j.1471-4159.1998.70010268.x

Bruce, 1995, Oxygen free radicals in rat limbic structures after kainate-induced seizures, Free Radic. Biol. Med., 18, 993, 10.1016/0891-5849(94)00218-9

Gardner, 1992, Inactivation–reactivation of aconitase in Escherichia coli: a sensitive measure of superoxide radical, J. Biol. Chem., 267, 8757, 10.1016/S0021-9258(19)50343-X

Gardner, 1997, Nitric oxide sensitivity of the aconitases, J. Biol. Chem., 272, 25071, 10.1074/jbc.272.40.25071

Liang, 2004, Mitochondrial oxidative stress and increased seizure susceptibility in Sod2(−/+) mice, Free Radic. Biol. Med., 36, 542, 10.1016/j.freeradbiomed.2003.11.029

Cock, 2002, Mitochondrial dysfunction associated with neuronal death following status epilepticus in rat, Epilepsy Res., 48, 157, 10.1016/S0920-1211(01)00334-5

Wallace, 2005, A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine, Annu. Rev. Genet., 39, 359, 10.1146/annurev.genet.39.110304.095751

Ryan, 2012, Post-translational oxidative modification and inactivation of mitochondrial complex I in epileptogenesis, J. Neurosci., 32, 11250, 10.1523/JNEUROSCI.0907-12.2012

Liang, 2008, Chelation of mitochondrial iron prevents seizure-induced mitochondrial dysfunction and neuronal injury, J. Neurosci., 28, 11550, 10.1523/JNEUROSCI.3016-08.2008

Gerlach, 1994, Altered brain metabolism of iron as a cause of neurodegenerative diseases?, J. Neurochem., 63, 793, 10.1046/j.1471-4159.1994.63030793.x

Lee, 2010, Iron elevations in the aging Parkinsonian brain: a consequence of impaired iron homeostasis?, J. Neurochem., 112, 332, 10.1111/j.1471-4159.2009.06470.x

Amici, 1989, Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions, J. Biol. Chem., 264, 3341, 10.1016/S0021-9258(18)94071-8

Kudin, 2004, Characterization of superoxide-producing sites in isolated brain mitochondria, J. Biol. Chem., 279, 4127, 10.1074/jbc.M310341200

Fato, 1787, Differential effects of mitochondrial Complex I inhibitors on production of reactive oxygen species, Biochim. Biophys. Acta, 384–3892, 2009

Hirst, 2010, Towards the molecular mechanism of respiratory complex I, Biochem. J., 425, 327, 10.1042/BJ20091382

Murphy, 2009, How mitochondria produce reactive oxygen species, Biochem. J., 417, 1, 10.1042/BJ20081386

Rothstein, 1994, Localization of neuronal and glial glutamate transporters, Neuron, 13, 713, 10.1016/0896-6273(94)90038-8

Frizzo, 2007, Extracellular adenosine triphosphate induces glutamate transporter-1 expression in hippocampus, Hippocampus, 17, 305, 10.1002/hipo.20269

Trotti, 1998, Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration?, Trends Pharmacol. Sci., 19, 328, 10.1016/S0165-6147(98)01230-9

Meldrum, 1999, Glutamate receptors and transporters in genetic and acquired models of epilepsy, Epilepsy Res., 36, 189, 10.1016/S0920-1211(99)00051-0

Tritschler, 1993, alterations as a source of human disorders, Neurology, 43, 280, 10.1212/WNL.43.2.280

Esposito, 1999, Mitochondrial disease in mouse results in increased oxidative stress, Proc. Natl. Acad. Sci. USA, 96, 4820, 10.1073/pnas.96.9.4820

Bohr, 2002, Mitochondrial DNA repair of oxidative damage in mammalian cells, Gene, 286, 127, 10.1016/S0378-1119(01)00813-7

Kudin, 2002, Seizure-dependent modulation of mitochondrial oxidative phosphorylation in rat hippocampus, Eur. J. Neurosci., 15, 1105, 10.1046/j.1460-9568.2002.01947.x

Dizdaroglu, 1991, Chemical determination of free radical-induced damage to DNA, Free Radic. Biol. Med., 10, 225, 10.1016/0891-5849(91)90080-M

Halliwell, 1986, Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts, Arch. Biochem. Biophys., 246, 501, 10.1016/0003-9861(86)90305-X

Coyle, 1993, Oxidative stress, glutamate, and neurodegenerative disorders, Science, 262, 689, 10.1126/science.7901908

Eraković, 1997, The influence of nicardipine and ifenprodil on the brain free arachidonic acid level and behavior in hypoxia-exposed rats, Prog. Neuro-psychopharmacol. Biol. Psychiatry, 21, 633, 10.1016/S0278-5846(97)00037-7

Mrsić, 1997, The influence of nimodipine and MK-801 on the brain free arachidonic acid level and the learning ability in hypoxia-exposed rats, Prog. Neuro-psychopharmacol. Biol. Psychiatry, 21, 345, 10.1016/S0278-5846(97)00005-5

Roberts, 2000, Measurement of F(2)-isoprostanes as an index of oxidative stress in vivo, Free Radic. Biol. Med., 28, 505, 10.1016/S0891-5849(99)00264-6

Patel, 2008, Seizure-induced formation of isofurans: novel products of lipid peroxidation whose formation is positively modulated by oxygen tension, J. Neurochem., 104, 264, 10.1111/j.1471-4159.2007.04974.x

Cini, 1995, Studies on lipid peroxidation and protein oxidation in the aging brain, Neurobiol. Aging, 16, 53, 10.1016/0197-4580(95)80007-E

Tejada, 2007, Antioxidant response and oxidative damage in brain cortex after high dose of pilocarpine, Brain Res. Bull., 71, 372, 10.1016/j.brainresbull.2006.10.005

Reed, 1995, Influence of metabolic inhibitors on mitochondrial permeability transition and glutathione status, Biochim. Biophys. Acta, 1271, 43, 10.1016/0925-4439(95)00008-R

Liang, 2006, Seizure-induced changes in mitochondrial redox status, Free Radic. Biol. Med., 40, 316, 10.1016/j.freeradbiomed.2005.08.026

O’Donovan, 2002, CoASH and CoASSG levels in lungs of hyperoxic rats as potential biomarkers of intramitochondrial oxidant stresses, Pediatr. Res., 51, 346, 10.1203/00006450-200203000-00014

Waldbaum, 2010, Persistent impairment of mitochondrial and tissue redox status during lithium–pilocarpine-induced epileptogenesis, J. Neurochem., 115, 1172, 10.1111/j.1471-4159.2010.07013.x

Sudha, 2001, Oxidative stress and antioxidants in epilepsy, Clin. Chim. Acta, 303, 19, 10.1016/S0009-8981(00)00337-5

Carlsson, 1995, Mice lacking extracellular superoxide dismutase are more sensitive to hyperoxia, Proc. Natl. Acad. Sci. USA, 92, 6264, 10.1073/pnas.92.14.6264

Reaume, 1996, Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury, Nat. Genet., 13, 43, 10.1038/ng0596-43

Li, 1995, Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase, Nat. Genet., 11, 376, 10.1038/ng1295-376

Huang, 2001, Genetic modification of prenatal lethality and dilated cardiomyopathy in Mn superoxide dismutase mutant mice, Free Radic. Biol. Med., 31, 1101, 10.1016/S0891-5849(01)00694-3

Patel, 2003, Metalloporphyrins improve the survival of Sod2-deficient neurons, Aging Cell, 2, 219, 10.1046/j.1474-9728.2003.00055.x

Patel, 2005, Activation of NADPH oxidase and extracellular superoxide production in seizure-induced hippocampal damage, J. Neurochem., 92, 123, 10.1111/j.1471-4159.2004.02838.x

Hwang, 2003, Oscillatory shear stress stimulates endothelial production of O2− from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion, J. Biol. Chem., 278, 47291, 10.1074/jbc.M305150200

Liang, 2012, Mitochondrial oxidative stress and epilepsy in SOD2 deficient mice: attenuation by a lipophilic metalloporphyrin, Neurobiol. Dis., 45, 1068, 10.1016/j.nbd.2011.12.025

James, 2002, How mitochondrial damage affects cell function, J. Biomed. Sci., 9, 475, 10.1007/BF02254975

Galella, 1983, Metabolic changes in the hippocampus after prolonged epileptic discharge, J. Neurosurg. Sci., 27, 69

Handforth, 1995, Functional mapping of the late stages of status epilepticus in the lithium–pilocarpine model in rat: a 14C-2-deoxyglucose study, Neuroscience, 64, 1075, 10.1016/0306-4522(94)00377-H

Folbergrová, 1985, Cerebral metabolic changes during and following fluorothyl-induced seizures in ventilated rats, J. Neurochem., 44, 1419, 10.1111/j.1471-4159.1985.tb08778.x

Nakamoto, 1990, Cerebral uptake of [14C]deoxyglucose during the entire seizure and the recovery period in an El mouse, Epilepsy Res, 5, 43, 10.1016/0920-1211(90)90064-3

Nishikawa, 2000, Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage, Nature, 404, 787, 10.1038/35008121

Erecińska, 1994, Ions and energy in mammalian brain, Prog. Neurobiol., 43, 37, 10.1016/0301-0082(94)90015-9

Grisar, 1984, Glial and neuronal Na+–K+ pump in epilepsy, Ann. Neurol., 16, S128, 10.1002/ana.410160719

Gulyás, 2006, Populations of hippocampal inhibitory neurons express different levels of cytochrome c, Eur. J. Neurosci., 23, 2581, 10.1111/j.1460-9568.2006.04814.x

Verstreken, 2005, Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions, Neuron, 47, 365, 10.1016/j.neuron.2005.06.018

Vesce, 2005, Acute glutathione depletion restricts mitochondrial ATP export in cerebellar granule neurons, J. Biol. Chem., 280, 38720, 10.1074/jbc.M506575200

Yadava, 2007, Spare respiratory capacity rather than oxidative stress regulates glutamate excitotoxicity after partial respiratory inhibition of mitochondrial complex I with rotenone, J. Neurosci, 27, 7310, 10.1523/JNEUROSCI.0212-07.2007

S. Kovac, A. Y. Abramov, M. C. Walker, Energy depletion in seizures: anaplerosis as a strategy for future therapies. Neuropharmacology 10.1016/j.neuropharm.2012.05.012, in press.

Cantu, 2009, Oxidative inactivation of mitochondrial aconitase results in iron and H2O2-mediated neurotoxicity in rat primary mesencephalic cultures, PLoS One, 4, e7095, 10.1371/journal.pone.0007095

Cantu, 2011, Mitochondrial aconitase knockdown attenuates paraquat-induced dopaminergic cell death via decreased cellular metabolism and release of iron and H2O2, J. Neurochem., 118, 79, 10.1111/j.1471-4159.2011.07290.x

Thiele, 2003, Assessing the efficacy of antiepileptic treatments: the ketogenic diet, Epilepsia, 44, 26, 10.1046/j.1528-1157.44.s7.4.x

Schwechter, 2003, Correlation between extracellular glucose and seizure susceptibility in adult rats, Ann. Neurol., 53, 91, 10.1002/ana.10415

Bough, 2006, Mitochondrial biogenesis in the anticonvulsant mechanism of the ketogenic diet, Ann. Neurol., 60, 223, 10.1002/ana.20899

Maalouf, 2007, Ketones inhibit mitochondrial production of reactive oxygen species production following glutamate excitotoxicity by increasing NADH oxidation, Neuroscience, 145, 256, 10.1016/j.neuroscience.2006.11.065

Stafstrom, 2009, Anticonvulsant and antiepileptic actions of 2-deoxy-D-glucose in epilepsy models, Ann. Neurol., 65, 435, 10.1002/ana.21603

Weindruch, 1988, Influences of aging and dietary restriction on serum thymosin alpha 1 levels in mice, J. Gerontol., 43, B40, 10.1093/geronj/43.2.B40

Gasior, 2010, Anticonvulsant and proconvulsant actions of 2-deoxy-D-glucose, Epilepsia, 51, 1385, 10.1111/j.1528-1167.2010.02593.x

Vexler, 2003, Fructose-1,6-bisphosphate preserves intracellular glutathione and protects cortical neurons against oxidative stress, Brain Res., 960, 90, 10.1016/S0006-8993(02)03777-0

Lian, 2007, Fructose-1,6-bisphosphate has anticonvulsant activity in models of acute seizures in adult rats, J. Neurosci., 27, 12007, 10.1523/JNEUROSCI.3163-07.2007

Giménez-Cassina, 2012, BAD-dependent regulation of fuel metabolism and K(ATP) channel activity confers resistance to epileptic seizures, Neuron, 74, 719, 10.1016/j.neuron.2012.03.032

Gibbs, 2006, Levetiracetam: antiepileptic properties and protective effects on mitochondrial dysfunction in experimental status epilepticus, Epilepsia, 47, 469, 10.1111/j.1528-1167.2006.00454.x

Barros, 2007, Effects of the vitamin E in catalase activities in hippocampus after status epilepticus induced by pilocarpine in Wistar rats, Neurosci. Lett., 416, 227, 10.1016/j.neulet.2007.01.057

Ogunmekan, 1989, A randomized, double-blind, placebo-controlled, clinical trial of D-alpha-tocopheryl acetate (vitamin E), as add-on therapy, for epilepsy in children, Epilepsia, 30, 84, 10.1111/j.1528-1157.1989.tb05287.x

Levy, 1992, The anticonvulsant effects of vitamin E: a further evaluation, Can. J. Neurol. Sci., 19, 201, 10.1017/S0317167100042268

Xu, 2008, Antioxidants and free radical scavengers do not consistently delay seizure onset in animal models of acute seizures, Epilepsy Behav, 13, 77, 10.1016/j.yebeh.2008.03.002

Patel, 1999, Metalloporphyrin class of therapeutic catalytic antioxidants, Trends Pharmacol. Sci., 20, 359, 10.1016/S0165-6147(99)01336-X

Melov, 2001, Lifespan extension and rescue of spongiform encephalopathy in superoxide dismutase 2 nullizygous mice treated with superoxide dismutase–catalase mimetics, J. Neurosci., 21, 8348, 10.1523/JNEUROSCI.21-21-08348.2001

Rong, 1999, EUK-134, a synthetic superoxide dismutase and catalase mimetic, prevents oxidative stress and attenuates kainate-induced neuropathology, Proc. Natl. Acad. Sci. USA, 96, 9897, 10.1073/pnas.96.17.9897

Brand, 2011, Assessing mitochondrial dysfunction in cells, Biochem. J., 435, 297, 10.1042/BJ20110162