Chelation of mitochondrial iron prevents seizure-induced mitochondrial dysfunction and neuronal injury

Journal of Neuroscience

Volumn 28, Issue 45, 2008, Pages 11550-11556

  Liang, Li Ping ^a   Jarrett, Stuart G ^a   Patel, Manisha ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b Research Building 2 ^*  (United States)

Author keywords

Epilepsy; Glutathione; Iron chelator; Kainic acid; MtDNA damage; Oxidative stress

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; GLUTATHIONE; MITOCHONDRIAL DNA; N,N' BIS(2 HYDROXYBENZYL)ETHYLENEDIAMINE N,N' DIACETIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG PENETRATION; EPILEPTIC STATE; HIPPOCAMPUS; IRON CHELATION; MALE; MITOCHONDRION; NERVE CELL LESION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SEIZURE;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BLEOMYCIN; CHELATING AGENTS; COLORIMETRY; DISEASE MODELS, ANIMAL; DNA, MITOCHONDRIAL; EDETIC ACID; GLUTATHIONE; GLUTATHIONE DISULFIDE; HIPPOCAMPUS; IRON; KAINIC ACID; MALE; MITOCHONDRIAL DISEASES; ORGANIC CHEMICALS; RATS; RATS, SPRAGUE-DAWLEY; STATUS EPILEPTICUS; SUBCELLULAR FRACTIONS; TIME FACTORS;

EID: 58149251841     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3016-08.2008     Document Type: Article

References (57)

1. Alam ZI, Daniel SE, Lees AJ, Marsden DC, Jenner P, Halliwell B (1997) A generalised increase in protein carbonyls in the brain in Parkinson's but not incidental Lewy body disease. J Neurochem 69:1326-1329.
2. Ando K, Ogawa K, Misaki S, Kikugawa K (2002) Increased release of free Fe ions in human erythrocytes during aging in the circulation. Free Radic Res 36:1079-1084.
3. Andreassen OA, Ferrante RJ, Dedeoglu A, Albers DW, Klivenyi P, Carlson EJ, Epstein CJ, Beal MF (2001) Mice with a partial deficiency of manganese superoxide dismutase show increased vulnerability to the mitochondrial toxins malonate, 3-nitropropionic acid, and MPTP. Exp Neurol 167:189-195.
4. Arbiser JL, Kraeft SK, van Leeuwen R, Hurwitz SJ, Selig M, Dickersin GR, Flint A, Byers HR, Chen LB (1998) Clioquinol-zinc chelate: a candidate causative agent of subacute myelo-optic neuropathy. Mol Med 4:665-670.
5. Ayala-Torres S, Chen Y, Svoboda T, Rosenblatt J, Van Houten B (2000) Analysis of gene-specific DNA damage and repair using quantitative polymerase chain reaction. Methods 22:135-147.
6. Baran H, Lassmann H, Sperk G, Seitelberger F, Hornykiewicz O (1987) Effect of mannitol treatment on brain neurotransmitter markers in kainic acid-induced epilepsy. Neuroscience 21:679-684.
7. Beard JL, Connor JR, Jones BC (1993) Iron in the brain. Nutr Rev 51:157-170.
8. Beinert H, Holm RH, Münck E (1997) Iron-sulfur clusters: nature's modular, multipurpose structures. Science 277:653-659.
9. Ben-Ari Y, Tremblay E, Riche D, Ghilini G, Naquet R (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6:1361-1391.
10. Ben-Shachar D, Eshel G, Finberg JP, Youdim MB (1991) The iron chelator desferrioxamine (Desferal) retards 6-hydroxydopamine-induced degeneration of nigrostriatal dopamine neurons. J Neurochem 56:1441-1444.
11. Bergeron RJ, Wiegand J, Brittenham GM (1999) HBED: the continuing development of a potential alternative to deferoxamine for iron-chelating therapy. Blood 93:370-375.
12. Bergeron RJ, Wiegand J, Brittenham GM (2002) HBED ligand: preclinical studies of a potential alternative to deferoxamine for treatment of chronic iron overload and acute iron poisoning. Blood 99:3019-3026.
13. Brittenham GM (2003) Iron chelators and iron toxicity. Alcohol 30:151-158.
14. Burkitt MJ, Milne L, Raafat A (2001) A simple, highly sensitive and improved method for the measurement of bleomycin-detectable iron: the 'catalytic iron index' and its value in the assessment of iron status in haemochromatosis. Clin Sci (Lond) 100:239-247.
15. Cherny RA, Atwood CS, Xilinas ME, Gray DN, Jones WD, McLean CA, Barnham KJ, Volitakis I, Fraser FW, Kim Y, Huang X, Goldstein LE, Moir RD, Lim JT, Beyreuther K, Zheng H, Tanzi RE, Masters CL, Bush AI (2001) Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 30:665-676.
16. Cock HR (2002) The role of mitochondria and oxidative stress in neuronal damage after brief and prolonged seizures. Prog Brain Res 135:187-196.
17. Evans PJ, Halliwell B (1994) Measurement of iron and copper in biological systems: bleomycin and copper-phenanthroline assays. Methods Enzymol 233:82-92.
18. Foury F, Talibi D (2001) Mitochondrial control of iron homeostasis. A genome wide analysis of gene expression in a yeast frataxin-deficient strain. J Biol Chem 276:7762-7768.
19. Glickstein H, El RB, Shvartsman M, Cabantchik ZI (2005) Intracellular labile iron pools as direct targets of iron chelators: a fluorescence study of chelator action in living cells. Blood 106:3242-3250.
20. Halliwell B, Gutteridge JM (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186:1-85.
21. Hammond EJ, Ramsay RE, Villarreal HJ, Wilder BJ (1980) Effects of intracortical injection of blood and blood components on the electrocorticogram. Epilepsia 21:3-14.
22. Henshall DC, Simon RP (2005) Epilepsy and apoptosis pathways. J Cereb Blood Flow Metab 25:1557-1572.
23. Hill JM, Switzer RC 3rd (1984) The regional distribution and cellular localization of iron in the rat brain. Neuroscience 11:595-603.
24. Hopkins KJ, Wang G, Schmued LC (2000) Temporal progression of kainic acid induced neuronal and myelin degeneration in the rat forebrain. Brain Res 864:69-80.
25. Jarrett SG, Liang LP, Hellier JL, Staley KJ, Patel M (2008) Mitochondrial DNA damage and impaired base excision repair during epileptogenesis. Neurobiol Dis 30:130-138.
26. Kalivendi SV, Kotamraju S, Cunningham S, Shang T, Hillard CJ, Kalyanaraman B (2003) 1-Methyl-4-phenylpyridinium (MPP+)-induced apoptosis and mitochondrial oxidant generation: role of transferrin-receptor-dependent iron and hydrogen peroxide. Biochem J 371:151-164.
27. Kasai H, Crain PF, Kuchino Y, Nishimura S, Ootsuyama A, Tanooka H (1986) Formation of 8-hydroxyguanine moiety in cellular DNA by agents producing oxygen radicals and evidence for its repair. Carcinogenesis 7:1849-1851.
28. Kaur D, Yantiri F, Rajagopalan S, Kumar J, Mo JQ, Boonplueang R, Viswanath V, Jacobs R, Yang L, Beal MF, DiMonte D, Volitaskis I, Ellerby L, Cherny RA, Bush AI, Andersen JK (2003) Genetic or pharmacological iron chelation prevents MPTP-induced neurotoxicity in vivo: a novel therapy for Parkinson's disease. Neuron 37:899-909.
29. Kirk EA, Heinecke JW, LeBoeuf RC (2001) Iron overload diminishes atherosclerosis in apoE-deficient mice. J Clin Invest 107:1545-1553.
30. Kudin AP, Kudina TA, Seyfried J, Vielhaber S, Beck H, Elger CE, Kunz WS (2002) Seizure-dependent modulation of mitochondrial oxidative phosphorylation in rat hippocampus. Eur J Neurosci 15:1105-1114.
31. Lakritz J, Plopper CG, Buckpitt AR (1997) Validated high-performance liquid chromatography-electrochemical method for determination of glutathione and glutathione disulfide in small tissue samples. Anal Biochem 247:63-68.
32. Liang LP, Patel M (2004a) Iron-sulfur enzyme mediated mitochondrial superoxide toxicity in experimental Parkinson's disease. J Neurochem 90:1076-1084.
33. Liang LP, Patel M (2004b) Mitochondrial oxidative stress and increased seizure susceptibility in Sod2(-/+) mice. Free Radic Biol Med 36:542-554.
34. Liang LP, Patel M (2006) Seizure-induced changes in mitochondrial redox status. Free Radic Biol Med 40:316-322.
35. Liang LP, Ho YS, Patel M (2000) Mitochondrial superoxide production in kainate-induced hippocampal damage. Neuroscience 101:563-570.
36. May ME, Fish WW (1978) The UV and visible spectral properties of ferritin. Arch Biochem Biophys 190:720-725.
37. Patel M (2004) Mitochondrial dysfunction and oxidative stress: cause and consequence of epileptic seizures. Free Radic Biol Med 37:1951-1962.
38. Patel M, Liang LP, Hou H, Williams BB, Kmiec M, Swartz HM, Fessel JP, Roberts LJ 2nd (2008) Seizure-induced formation of isofurans: novel products of lipid peroxidation whose formation is positively modulated by oxygen tension. J Neurochem 104:264-270.
39. Petrat F, de Groot H, Rauen U (2001) Subcellular distribution of chelatable iron: a laser scanning microscopic study in isolated hepatocytes and liver endothelial cells. Biochem J 356:61-69.
40. Petrat F, de Groot H, Sustmann R, Rauen U (2002a) The chelatable iron pool in living cells: a methodically defined quantity. Biol Chem 383:489-502.
41. Petrat F, Weisheit D, Lensen M, de Groot H, Sustmann R, Rauen U (2002b) Selective determination of mitochondrial chelatable iron in viable cells with a new fluorescent sensor. Biochem J 362:137-147.
42. Rauen U, Springer A, Weisheit D, Petrat F, Korth HG, de Groot H, Sustmann R (2007) Assessment of chelatable mitochondrial iron by using mitochondrion-selective fluorescent iron indicators with different iron-binding affinities. Chembiochem 8:341-352.
43. Riemer J, Hoepken HH, Czerwinska H, Robinson SR, Dringen R (2004) Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal Biochem 331:370-375.
44. Ryter SW, Tyrrell RM (2000) The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic Biol Med 28:289-309.
45. Samuni AM, Afeworki M, Stein W, Yordanov AT, DeGraff W, Krishna MC, Mitchell JB, Brechbiel MW (2001) Multifunctional antioxidant activity of HBED iron chelator. Free Radic Biol Med 30:170-177.
46. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123-130.
47. Schmued LC, Albertson C, Slikker W Jr (1997) Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 751:37-46.
48. Shigenaga MK, Park JW, Cundy KC, Gimeno CJ, Ames BN (1990) In vivo DNA damage: measurement of 8-hydroxy-2′ deoxyguanosine in DNA and urine by high-performance liquid chromatography with electrochemical detection. Methods Enzymol 186:521-530.
49. Shoham S, Youdim MB (2004) Nutritional iron deprivation attenuates kainate-induced neurotoxicity in rats: implications for involvement of iron in neurodegeneration. Ann N Y Acad Sci 1012:94-114.
50. Sohal RS, Wennberg-Kirch E, Jaiswal K, Kwong LK, Forster MJ (1999) Effect of age and caloric restriction on bleomycin-chelatable and nonheme iron in different tissues of C57BL/6 mice. Free Radic Biol Med 27:287-293.
51. Wang XS, Ong WY, Connor JR (2002) Increase in ferric and ferrous iron in the rat hippocampus with time after kainate-induced excitotoxic injury. Exp Brain Res 143:137-148.
52. Willmore LJ, Sypert GW, Munson JB (1978) Recurrent seizures induced by cortical iron injection: a model of posttraumatic epilepsy. Ann Neurol 4:329-336.
53. Yakes FM, Van Houten B (1997) Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 94:514-519.
54. Yassin MS, Ekblom J, Xilinas M, Gottfries CG, Oreland L (2000) Changes in uptake of vitamin B(12) and trace metals in brains of mice treated with clioquinol. J Neurol Sci 173:40-44.
55. Youdim MB, Green AR (1978) Iron deficiency and neurotransmitter synthesis and function. Proc Nutr Soc 37:173-179.
56. Youdim MB, Ben-Shachar D, Yehuda S (1989) Putative biological mechanisms of the effect of iron deficiency on brain biochemistry and behavior. Am J Clin Nutr 50:607-615, discussion 615-617.
57. Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR (2004) Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci 5:863-873.