Oxidative inactivation of mitochondrial aconitase results in iron and H2O2-mediated neurotoxicity in rat primary mesencephalic cultures

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Cantu, David ^a   Schaack, Jerome ^a   Patel, Manisha ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; CATALASE; HYDROGEN PEROXIDE; IRON; MITOCHONDRIAL ACONITASE; N,N' BIS(2 HYDROXYBENZYL)ETHYLENEDIAMINE N,N' DIACETIC ACID; PARAQUAT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; FENTON'S REAGENT; OXYGEN;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME INACTIVATION; FENTON REACTION; IRON CHELATION; IRON STORAGE; MESENCEPHALON; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; RAT; ANIMAL; CELL CULTURE; CHEMISTRY; ENZYMOLOGY; METABOLISM; MITOCHONDRION; NERVE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

RATTUS;

ACONITATE HYDRATASE; ANIMALS; CELLS, CULTURED; HYDROGEN PEROXIDE; IRON; MESENCEPHALON; MITOCHONDRIA; NEURONS; OXIDATIVE STRESS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 70349464469     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007095     Document Type: Article

References (45)

1. Schapira AH (1999) Mitochondrial involvement in Parkinson's disease, Huntington's disease, hereditary spastic paraplegia and Friedreich's ataxia. Biochim Biophys Acta 1410: 159-170.
2. Schapira AH (2008) Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Lancet Neurol 7: 97-109.
3. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443: 787-795.
4. Baron M, Kudin AP, Kunz WS (2007) Mitochondrial dysfunction in neurodegenerative disorders. Biochem Soc Trans 35: 1228-1231.
5. Gardner PR, Fridovich I (1991) Superoxide sensitivity of the Escherichia coli 6-phosphogluconate dehydratase. J Biol Chem 266: 1478-1483.
6. Tretter L, Adam-Vizi V (2005) Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress. Philos Trans R Soc Lond B Biol Sci 360: 2335-2345.
7. Flint DH, Tuminello JF, Emptage MH (1993) The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem 268: 22369-22376.
8. Gardner PR, Fridovich I (1991) Superoxide sensitivity of the Escherichia coli aconitase. J Biol Chem 266: 19328-19333.
9. Keyer K, Imlay JA (1996) Superoxide accelerates DNA damage by elevating free-iron levels. Proc Natl Acad Sci U S A 93: 13635-13640.
10. Vasquez-Vivar J, Kalyanaraman B, Kennedy MC (2000) Mitochondrial aconitase is a source of hydroxyl radical. An electron spin resonance investigation. J Biol Chem 275: 14064-14069.
11. Boveris A, Chance B (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134: 707-716.
12. Imlay JA, Fridovich I (1991) Assay of metabolic superoxide production in Escherichia coli. J Biol Chem 266: 6957-6965.
13. Cadenas E, Boveris A, Ragan CI, Stoppani AO (1977) Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch Biochem Biophys 180: 248-257.
14. Marcus DL, Thomas C, Rodriguez C, Simberkoff K, Tsai JS, et al. (1998) Increased peroxidation and reduced antioxidant enzyme activity in Alzheimer's disease. Exp Neurol 150: 40-44.
15. Pearce RK, Owen A, Daniel S, Jenner P, Marsden CD (1997) Alterations in the distribution of glutathione in the substantia nigra in Parkinson's disease. J Neural Transm 104: 661-677.
16. Liang LP, Patel M (2004) Iron-sulfur enzyme mediated mitochondrial superoxide toxicity in experimental Parkinson's disease. J Neurochem 90: 1076-1084.
17. Patel M, Day BJ, Crapo JD, Fridovich I, McNamara JO (1996) Requirement for superoxide in excitotoxic cell death. Neuron 16: 345-355.
18. Melov S, Coskun P, Patel M, Tuinstra R, Cottrell B, et al. (1999) Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc Natl Acad Sci U S A 96: 846-851.
19. Park LC, Albers DS, Xu H, Lindsay JG, Beal MF, et al. (2001) Mitochondrial impairment in the cerebellum of the patients with progressive supranuclear palsy. J Neurosci Res 66: 1028-1034.
20. Tabrizi SJ, Cleeter MW, Xuereb J, Taanman JW, Cooper JM, et al. (1999) Biochemical abnormalities and excitotoxicity in Huntington's disease brain. Ann Neurol 45: 25-32.
21. Longo VD, Liou LL, Valentine JS, Gralla EB (1999) Mitochondrial superoxide decreases yeast survival in stationary phase. Arch Biochem Biophys 365: 131-142.
22. Liochev SI, Fridovich I (1994) The role of O2.- in the production of HO.: in vitro and in vivo. Free Radic Biol Med 16: 29-33.
23. Schapira AH, Hartley A, Cleeter MW, Cooper JM (1993) Free radicals and mitochondrial dysfunction in Parkinson's disease. Biochem Soc Trans 21: 367-370.
24. Beal MF (1998) Mitochondrial dysfunction in neurodegenerative diseases. Biochim Biophys Acta 1366: 211-223.
25. Kaur D, Andersen J (2004) Does cellular iron dysregulation play a causative role in Parkinson's disease? Ageing Res Rev 3: 327-343.
26. Castello PR, Drechsel DA, Patel M (2007) Mitochondria are a major source of paraquat-induced reactive oxygen species production in the brain. J Biol Chem 282: 14186-14193.
27. Grammatopoulos TN, Ahmadi F, Jones SM, Fariss MW, Weyhenmeyer JA, et al. (2005) Angiotensin II protects cultured midbrain dopaminergic neurons against rotenone-induced cell death. Brain Res 1045: 64-71.
28. Petrat F, Weisheit D, Lensen M, de Groot H, Sustmann R, et al. (2002) Selective determination of mitochondrial chelatable iron in viable cells with a new fluorescent sensor. Biochem J 362: 137-147.
29. Liang LP, Jarrett SG, Patel M (2008) Chelation of mitochondrial iron prevents seizure-induced mitochondrial dysfunction and neuronal injury. J Neurosci (In Press).
30. Li QY, Pedersen C, Day BJ, Patel M (2001) Dependence of excitotoxic neurodegeneration on mitochondrial aconitase inactivation. J Neurochem 78: 746-755.
31. Vielhaber S, Niessen HG, Debska-Vielhaber G, Kudin AP, Wellmer J, et al. (2008) Subfield-specific loss of hippocampal N-acetyl aspartate in temporal lobe epilepsy. Epilepsia 49: 40-50.
32. Lian XY, Stringer JL (2004) Inhibition of aconitase in astrocytes increases the sensitivity to chemical convulsants. Epilepsy Res 60: 41-52.
33. Murakami K, Yoshino M (1997) Inactivation of aconitase in yeast exposed to oxidative stress. Biochem Mol Biol Int 41: 481-486.
34. Mackensen GB, Patel M, Sheng H, Calvi CL, Batinic-Haberle I, et al. (2001) Neuroprotection from delayed postischemic administration of a metalloporphyrin catalytic antioxidant. J Neurosci 21: 4582-4592.
35. Longo VD, Viola KL, Klein WL, Finch CE (2000) Reversible inactivation of superoxide-sensitive aconitase in Abeta1-42-treated neuronal cell lines. J Neurochem 75: 1977-1985.
36. Andres-Mateos E, Perier C, Zhang L, Blanchard-Fillion B, Greco TM, et al. (2007) DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc Natl Acad Sci U S A 104: 14807-14812.
37. Liang LP, Patel M (2004) Mitochondrial oxidative stress and increased seizure susceptibility in Sod2(-/+) mice. Free Radic Biol Med 36: 542-554.
38. Patel M, Li QY (2003) Age dependence of seizure-induced oxidative stress. Neuroscience 118: 431-437.
39. Yan LJ, Levine RL, Sohal RS (1997) Oxidative damage during aging targets mitochondrial aconitase. Proc Natl Acad Sci U S A 94: 11168-11172.
40. Sian J, Dexter DT, Lees AJ, Daniel S, Agid Y, et al. (1994) Alterations in glutathione levels in Parkinson's disease and other neurodegenerative disorders affecting basal ganglia. Ann Neurol 36: 348-355.
41. Sofic E, Lange KW, Jellinger K, Riederer P (1992) Reduced and oxidized glutathione in the substantia nigra of patients with Parkinson's disease. Neurosci Lett 142: 128-130.
42. Dexter DT, Wells FR, Agid F, Agid Y, Lees AJ, et al. (1987) Increased nigral iron content in postmortem parkinsonian brain. Lancet 2: 1219-1220.
43. Jha N, Jurma O, Lalli G, Liu Y, Pettus EH, et al. (2000) Glutathione depletion in PC12 results in selective inhibition of mitochondrial complex I activity. Implications for Parkinson's disease. J Biol Chem 275: 26096-26101.
44. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39: 889-909.
45. Hirsch EC, Hunot S, Hartmann A (2005) Neuroinflammatory processes in Parkinson's disease. Parkinsonism Relat Disord 11 Suppl 1: S9-S15.