Xanthine oxidase-induced neuronal death via the oxidation of NADH: Prevention by micromolar EDTA

Brain Research

Volumn 1280, Issue , 2009, Pages 33-42

  Al Gonaiah, Majed ^a   Smith, Robert A ^a   Stone, Trevor W ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Cerebellar granule neurons; NADH; Nicotinamide adenine dinucleotide; Peroxide; Superoxide dismutase; Xanthine oxidase

Indexed keywords

CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; EDETIC ACID; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUPEROXIDE; XANTHINE OXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL CULTURE; CELL DEATH; CEREBELLUM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GRANULE CELL; IN VIVO STUDY; NONHUMAN; OXIDATION; PREVENTION; PRIORITY JOURNAL; PROTECTION; RAT; TOXICITY;

ANIMALS; CATALASE; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; EDETIC ACID; HYDROGEN PEROXIDE; METALS; NAD; NEURONS; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; OXIDATION-REDUCTION; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE; XANTHINE OXIDASE;

EID: 67649427848     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.05.024     Document Type: Article

References (61)

1. Allen R.E., Claxson A.W., Blake D.R., and Morris C.J. Inhibition of xanthine oxidase by allopurinol: its lack of effect on models of inflammation. Ann. Rheum. Dis. 49 (1990) 422-423
2. Aruoma O.I., Halliwell B., Gajewski E., and Dizdaroglu M. Copper-ion-dependent damage to the bases in DNA in the presence of hydrogen peroxide. Biochem. J. 273 (1991) 601-604
3. Bartesaghi S., Trujillo M., Denicola A., Folkes L., Wardman P., and Radi R. Reactions of desferrioxamine with peroxynitrite-derived carbonate and nitrogen dioxide radicals. Free Radic. Biol. Med. 36 (2004) 471-483
4. Benders M.J., Bos A.F., Rademaker C.M., Rijken M., Torrance H.L., Groenendaal F., and van Bel F. Early postnatal allopurinol does not improve short term outcome after severe birth asphyxia. Arch. Dis. Child., Fetal Neonatal Ed. 91 (2006) F163-F165
5. Berry C.E., and Hare J.M. Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J. Physiol. 555 (2004) 589-606
6. Britigan B.E., Pou S., Rosen G.M., Lilleg D.M., and Buettner G.R. Hydroxyl radical is not a product of the reaction of xanthine oxidase and xanthine. The confounding problem of adventitious iron bound to xanthine oxidase. J. Biol. Chem. 265 (1990) 17533-17538
7. Chan P.C., and Bielski B.H. Enzyme-catalyzed free radical reactions with nicotinamide adenine nucleotides. II. Lactate dehydrogenase-catalyzed oxidation of reduced nicotinamide adenine dinucleotide by superoxide radicals generated by xanthine oxidase. J. Biol. Chem. 249 (1974) 1317-1319
8. Coetzee A., Roussouw G., and Macgregor L. Failure of allopurinol to improve left ventricular stroke work after cardiopulmonary bypass surgery. J. Cardiothorac. Vasc. Anesth. 10 (1996) 627-633
9. Darr D., and Fridovich I. Vanadate and molybdate stimulate the oxidation of NADH by superoxide radical. Arch. Biochem. Biophys. 232 (1984) 562-565
10. Engelmann M.D., Bobier R.T., Hiatt T., and Cheng I.F. Variability of the Fenton reaction characteristics of the EDTA, DTPA, and citrate complexes of iron. Biometals 16 (2003) 519-527
11. Fatokun A.A., Stone T.W., and Smith R.A. Hydrogen peroxide-induced oxidative stress in the osteoblast-like MC3T3-E1 cells: the effects of glutamate and protection by purines. Bone 39 (2006) 542-551
12. Fatokun A.A., Stone T.W., and Smith R.A. Hydrogen peroxide mediates damage by xanthine and xanthine oxidase in cerebellar granule neuronal cultures. Neurosci. Lett. 416 (2007) 34-38
13. Fridovich I., and Handler P. Xanthine oxidase. V. Differential inhibition of the reduction of various electron acceptors. J. Biol. Chem. 237 (1962) 916-921
14. Gilbert D.A. Oxidations and transhydrogenations involving pyridine-dinucleotides catalysed by bovine milk xanthine oxidase. Nature 197 (1963) 1066-1068
15. Gonzalez R.J., and Tarloff J.B. Evaluation of hepatic subcellular fractions for Alamar Blue and MTT reductase activity. Toxicol. In Vitro 15 (2001) 257-259
16. Graf E., Mahoney J.R., Bryant R.G., and Eaton J.W. Iron-catalyzed hydroxyl radical formation. Stringent requirement for free iron coordination site. J. Biol. Chem. 259 (1984) 3620-3624
17. Greenstock C.L., and Miller R.W. The oxidation of tiron by superoxide anion. Kinetics of the reaction in aqueous solution in chloroplasts. Biochim. Biophys. Acta 396 (1975) 11-16
18. Gunasekar P.G., Kanthasamy A.G., Borowitz J.L., and Isom G.E. NMDA receptor activation produces concurrent generation of nitric oxide and reactive oxygen species: implication for cell death. J. Neurochem. 65 (1995) 2016-2021
19. Halliwell B. Superoxide dismutase: a contaminant of bovine catalase. Biochem. J. 135 (1973) 379-381
20. Halliwell B. Oxidative stress and neurodegeneration: where are we now?. J. Neurochem. 97 (2006) 1634-1658
21. Hamid R., Rotshteyn Y., Rabadi L., Parikh R., and Bullock P. Comparison of Alamar Blue and MTT assays for high through-put screening. Toxicol. In Vitro 18 (2004) 703-710
22. Harrison R. Structure and function of xanthine oxidoreductase: where are we now?. Free Radic. Biol. Med. 33 (2002) 774-797
23. Hartley A., Davies M., and Rice-Evans C. Desferrioxamine as a lipid chain-breaking antioxidant in sickle erythrocyte membranes. FEBS Lett. 264 (1990) 145-148
24. Hassan H.M., Dougherty H., and Fridovich I. Inhibitors of superoxide dismutases: a cautionary tale. Arch. Biochem. Biophys. 199 (1980) 349-354
25. Heikkila R.E., and Cohen G. 6-Hydroxydopamine: evidence for superoxide radical as an oxidative intermediate. Science 181 (1973) 456-457
26. Hoe S., Rowley D.A., and Halliwell B. Reactions of ferrioxamine and desferrioxamine with the hydroxyl radical. Chem. Biol. Interact. 41 (1982) 75-81
27. Imlay J.A., and Linn S. DNA damage and oxygen radical toxicity. Science 240 (1988) 1302-1309
28. Keberle H. The biochemistry of desferrioxamine and its relation to iron metabolism. Ann. N.Y. Acad. Sci. 119 (1964) 758-768
29. Lafon-Cazal M., Culcasi M., Gaven F., Pietri S., and Bockaert J. Nitric oxide, superoxide and peroxynitrite: putative mediators of NMDA-induced cell death in cerebellar granule cells. Neuropharmacology 32 (1993) 1259-1266
30. 2. Arch. Biochem. Biophys. 275 (1989) 40-43
31. -. Arch. Biochem. Biophys. 279 (1990) 1-7
32. -, HO.), and secondarily derived radicals in oxidation reactions catalyzed by vanadium salts. Arch. Biochem. Biophys. 291 (1991) 379-382
33. 2. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 743-744
34. 2 formation. Free Radic. Biol. Med. 42 (2007) 1465-1469
35. Liochev S., Ivancheva E., and Fridovich I. Effects of vanadate on the oxidation of NADH by xanthine oxidase. Arch. Biochem. Biophys. 269 (1989) 188-193
36. Lloyd D.R., and Phillips D.H. Oxidative DNA damage mediated by copper(II), iron(II) and nickel(II) Fenton reactions: evidence for site-specific mechanisms in the formation of double-strand breaks, 8-hydroxydeoxyguanosine and putative intrastrand cross-links. Mutat. Res. 424 (1999) 23-36
37. Lloyd J.B., Cable H., and Rice-Evans C. Evidence that desferrioxamine cannot enter cells by passive diffusion. Biochem. Pharmacol. 9 (1991) 1361-1363
38. Luo G.M., Qi D.H., Zheng Y.G., Mu Y., Yan G.L., Yang T.S., and Shen J.C. ESR studies on reaction of saccharide with the free radicals generated from the xanthine oxidase/hypoxanthine system containing iron. FEBS Lett. 492 (2001) 29-32
39. Maia L., Duarte R.O., Ponces-Freire A., Moura J.J., and Mira L. NADH oxidase activity of rat and human liver xanthine oxidoreductase: potential role in superoxide production. J. Biol. Inorg. Chem. 12 (2007) 777-787
40. Misra H.P., and Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 247 (1972) 3170-3175
41. Nakamura M. Allopurinol-insensitive oxygen radical formation by milk xanthine oxidase systems. J. Biochem. 110 (1991) 450-456
42. Nakayama G.R., Caton M.C., Nova M.P., and Parandoosh Z. Assessment of the Alamar Blue assay for cellular growth and viability in vitro. J. Immunol. Methods 204 (1997) 205-208
43. O'Brien J., Wilson I., Orton T., and Pognan F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem. 267 (2000) 5421-5426
44. Okuda S., Nishiyama N., Saito H., and Katsuki H. Hydrogen peroxide-mediated neuronal cell death induced by an endogenous neurotoxin, 3-hydroxykynurenine. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 12553-12558
45. Osarogiagbon U.R., Choong S., Belcher J.D., Vercellotti G.M., Paller M.S., and Hebbel R.P. Reperfusion injury pathophysiology in sickle transgenic mice. Blood 96 (2000) 314-320
46. Patel M., Day B.J., Crapo J.D., Fridovich I., and McNamara J.O. Requirement for superoxide in excitotoxic cell death. Neuron 16 (1996) 345-355
47. Que B.G., Downey K.M., and So A.G. Degradation of deoxyribonucleic acid by a 1,10-phenanthroline-copper complex: the role of hydroxyl radicals. Biochemistry 19 (1980) 5987-5991
48. Rieger J.M., Shah A.R., and Gidday J.M. Ischemia-reperfusion injury of retinal endothelium by cyclooxygenase- and xanthine oxidase-derived superoxide. Exp. Eye Res. 74 (2002) 493-501
49. Rowley D.A., and Halliwell B. Superoxide-dependent formation of hydroxyl radicals from NADH and NADPH in the presence of iron salts. FEBS Lett. 142 (1982) 39-41
50. Sanders S.A., Eisenthal R., and Harrison R. NADH oxidase activity of human xanthine oxidoreductase-generation of superoxide anion. Eur. J. Biochem. 245 (1997) 541-548
51. Satoh T., Numakawa T., Abiru Y., Yamagata T., Ishikawa Y., Enokido Y., and Hatanaka H. Production of reactive oxygen species and release of l-glutamate during superoxide anion-induced cell death of cerebellar granule neurons. J. Neurochem. 70 (1998) 316-324
52. Sayre L.M., Perry G., and Smith M.A. Redox metals and neurodegenerative disease. Curr. Opin. Chem. Biol. 3 (1999) 220-225
53. Schramm M., Eimerl S., and Costa E. Serum and depolarizing agents cause acute neurotoxicity in cultured cerebellar granule cells: role of the glutamate receptor responsive to N-methyl-d-aspartate. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 1193-1197
54. Shinar E., Navok T., and Chevion M. The analogous mechanisms of enzymatic inactivation induced by ascorbate and superoxide in the presence of copper. J. Biol. Chem. 258 (1983) 14778-14783
55. Starke P.E., and Farber J.L. Ferric iron and superoxide ions are required for the killing of cultured hepatocytes by hydrogen peroxide. Evidence for the participation of hydroxyl radicals formed by an iron-catalyzed Haber-Weiss reaction. J. Biol. Chem. 260 (1985) 10099-10104
56. Thom S.R. Dehydrogenase conversion to oxidase and lipid peroxidation in brain after carbon monoxide poisoning. J. Appl. Physiol. 73 (1992) 1584-1589
57. Vile G.F., and Winterbourn C.C. High-affinity iron binding by xanthine oxidase. J. Free Radic. Biol. Med. 2 (1986) 393-396
58. White M.J., DiCaprio M.J., and Greenberg D.A. Assessment of neuronal viability with Alamar blue in cortical and granule cell cultures. J. Neurosci. Methods 70 (1996) 195-200
59. Wiezorek J.S., Brown D.H., Kupperman D.E., and Brass C.A. Rapid conversion to high xanthine oxidase activity in viable Kupffer cells during hypoxia. 1994. J. Clin. Invest. 94 (1994) 2224-2230
60. Zhang Z., Blake D.R., Stevens C.R., Kanczler J.M., Winyard P.G., Symons M.C., Benboubetra M., and Harrison R. A reappraisal of xanthine dehydrogenase and oxidase in hypoxic reperfusion injury: the role of NADH as an electron donor. Free Radic. Res. 28 (1998) 151-164
61. Zhao H., Joseph J., Fales H.M., Sokoloski E.A., Levine R.L., Vasquez-Vivar J., and Kalyanaraman B. Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 5727-5732