Activation of NADPH oxidase and extracellular superoxide production in seizure-induced hippocampal damage

Journal of Neurochemistry

Volumn 92, Issue 1, 2005, Pages 123-131

  Patel, Manisha ^a,b,c   Li, Qing You ^a   Chang, Ling Yi ^b   Crapo, James ^b   Liang, Li Ping ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^c Box C238 ^*  (United States)

Author keywords

Chemiluminescence; Excitotoxicity; Hippocampus; Kainate; Microglia; Superoxide

Indexed keywords

KAINIC ACID; PROTEIN P47; PROTEIN P67; RAC1 PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL ACTIVATION; CHEMOLUMINESCENCE; CONTROLLED STUDY; CYTOSOL; ENZYME SUBUNIT; EPILEPTIC STATE; HIPPOCAMPUS; IMMUNOBLOTTING; MALE; MICROGLIA; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEIZURE;

ANIMALS; EXTRACELLULAR SPACE; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NADPH OXIDASE; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; SUPEROXIDE DISMUTASE;

ANIMALIA;

EID: 13244288760     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02838.x     Document Type: Article

References (54)

1. Anderson M. F. and Sims N. R. (2000) Improved recovery of highly enriched mitochondrial fractions from small brain tissue samples. Brain Res. Brain Res. Protoc. 5, 95-101.
2. Andersson P. B., Perry V. H. and Gordon S. (1991) The kinetics and morphological characteristics of the macrophage-microglial response to kainic acid-induced neuronal degeneration. Neuroscience 42, 201-214.
3. Babior B. M. (1999) NADPH oxidase: an update. Blood 93, 1464-1476.
4. Bianca V. D., Dusi S., Bianchini E., Dal Pra I. and Rossi F. (1999) beta-amyloid activates the O-2 forming NADPH oxidase in microglia, monocytes, and neutrophils. A possible inflammatory mechanism of neuronal damage in Alzheimer's disease. J. Biol. Chem. 274, 15 493-15 499.
5. Bindokas V. P., Jordan J., Lee C. C. and Miller R. J. (1996) Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J. Neurosci. 16, 1324-1336.
6. Bolscher B. G., Denis S. W., Verhoeven A. J. and Roos D. (1990) The activity of one soluble component of the cell-free NADPH:O2 oxidoreductase of human neutrophils depends on guanosine 5′-O-(3-thio)triphosphate. J. Biol. Chem. 265, 15 782-15 787.
7. Bowler R. P., Arcaroli J., Abraham E., Patel M., Chang L. Y. and Crapo J. D. (2003) Evidence for extracellular superoxide dismutase as a mediator of hemorrhage-induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 284, L680-L687.
8. Bruce A. J. and Baudry M. (1995) Oxygen free radicals in rat limbic structures after kainate-induced seizures. Free Radic. Biol. Med. 18, 993-1002.
9. Bruce-Keller A. J., Umberger G., McFall R. and Mattson M. P. (1999) Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Ann. Neurol. 45, 8-15.
10. Clark R. A., Volpp B. D., Leidal K. G. and Nauseef W. M. (1989) Translocation of cytosolic components of neutrophil NADPH oxidase. Trans. Assoc. Am. Physicians 102, 224-230.
11. DeLeo F. R. and Quinn M. T. (1996) Assembly of the phagocyte NADPH oxidase: molecular interaction of oxidase proteins. J. Leukoc. Biol. 60, 677-691.
12. Duerrschmidt N., Wippich N., Goettsch W., Broemme H. J. and Morawietz H. (2000) Endothelin-1 induces NAD(P)H oxidase in human endothelial cells. Biochem. Biophys. Res. Commun. 269, 713-717.
13. Dugan L. L., Sensi S. L., Canzoniero L. M., Handran S. D., Rothman S. M., Lin T. S., Goldberg M. P. and Choi D. W. (1995) Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci. 15, 6377-6388.
14. Dykens J. A., Stern A. and Trenkner E. (1987) Mechanism of kainate toxicity to cerebellar neurons in vitro is analogous to reperfusion tissue injury. J. Neurochem. 49, 1222-1228.
15. Fattman C. L., Schaefer L. M. and Oury T. D. (2003) Extracellular superoxide dismutase in biology and medicine. Free Radic. Biol. Med. 35, 236-256.
16. Finkel T. (1999) Signal transduction by reactive oxygen species in non-phagocytic cells. J. Leukoc. Biol. 65, 337-340.
17. Hetherington H. P., Pan J. W. and Spencer D. D. (2002) 1H and 31P spectroscopy and bioenergetics in the lateralization of seizures in temporal lobe epilepsy. J. Magn. Reson. Imaging 16, 477-483.
18. Klegeris A. and McGeer P. L. (1994) Rat brain microglia and peritoneal macrophages show similar responses to respiratory burst stimulants. J. Neuroimmunol. 53, 83-90.
19. Kuzniecky R., Elgavish G. A., Hetherington H. P., Evanochko W. T. and Pohost G. M. (1992) In vivo 31P nuclear magnetic resonance spectroscopy of human temporal lobe epilepsy. Neurology 42, 1586-1590.
20. Lafon-Cazal M., Pietri S., Culcasi M. and Bockaert J. (1993) NMDA-dependent superoxide production and neurotoxicity. Nature 364, 535-537.
21. Lambeth J. D. (2004) NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189.
22. Lassegue B. and Clempus R. E. (2003) Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R277-R297.
23. Li J. M. and Shah A. M. (2002) Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J. Biol. Chem. 277, 19 952-19 960.
24. Liang L. P., Ho Y. S. and Patel M. (2000) Mitochondrial superoxide production in kainate-induced hippocampal damage. Neuroscience 101, 563-570.
25. Lucas M. and Solano F. (1992) Coelenterazine is a superoxide anion-sensitive chemiluminescent probe: its usefulness in the assay of respiratory burst in neutrophils. Anal. Biochem. 206, 273-277.
26. MacGregor D. G., Higgins M. J., Jones P. A., Maxwell W. L., Watson M. W., Graham D. I. and Stone T. W. (1996) Ascorbate attenuates the systemic kainate-induced neurotoxicity in the rat hippocampus. Brain Res. 727, 133-144.
27. Marklund S. L. and Karlsson K. (1990) Extracellular-superoxide dismutase, distribution in the body and therapeutic applications. Adv. Exp. Med. Biol. 264, 1-4.
28. Mehta J. L. and Li D. (2001) Epinephrine upregulates superoxide dismutase in human coronary artery endothelial cells. Free Radic. Biol. Med. 30, 148-153.
29. Minami M., Kuraishi Y. and Satoh M. (1991) Effects of kainic acid on messenger RNA levels of IL-1 beta, IL-6, TNF alpha and LIF in the rat brain. Biochem. Biophys. Res. Commun. 176, 593-598.
30. Noh K. M. and Koh J. Y. (2000) Induction and activation by zinc of NADPH oxidase in cultured cortical neurons and astrocytes. J. Neurosci. 20, RC111.
31. O'Donnell B. V., Tew D. G., Jones O. T. and England P. J. (1993) Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem. J. 290, 41-49.
32. Oury T. D., Ho Y. S., Piantadosi C. A. and Crapo J. D. (1992) Extracellular superoxide dismutase, nitric oxide, and central nervous system O2 toxicity. Proc. Natl Acad. Sci. USA 89, 9715-9719.
33. Oury T. D., Day B. J. and Crapo J. D. (1996) Extracellular superoxide dismutase: a regulator of nitric oxide bioavailability. Lab. Invest. 75, 617-636.
34. Patel M. and Day B. J. (1999) Metalloporphyrin class of therapeutic catalytic antioxidants. Trends Pharmacol. Sci. 20, 359-364.
35. Patel M., Day B. J., Crapo J. D., Fridovich I. and McNamara J. O. (1996) Requirement for superoxide in excitotoxic cell death. Neuron 16, 345-355.
36. Perez-Otano I., McMillian M. K., Chen J., Bing G., Hong J. S. and Pennypacker K. R. (1996) Induction of NF-kB-like transcription factors in brain areas susceptible to kainate toxicity. Glia 16, 306-315.
37. Reynolds I. J. and Hastings T. G. (1995) Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 15, 3318-3327.
38. Rogers S. W., Andrews P. I., Gahring L. C., Whisenand T., Cauley K., Crain B., Hughes T. E., Heinemann S. F. and McNamara J. O. (1994) Autoantibodies to glutamate receptor GluR3 in Rasmussen's encephalitis. Science 265, 648-651.
39. Rong Y., Doctrow S. R., Tocco G. and Baudry M. (1999) EUK-134, a synthetic superoxide dismutase and catalase mimetic, prevents oxidative stress and attenuates kainate-induced neuropathology. Proc. Natl Acad. Sci. USA 96, 9897-9902.
40. Sankarapandi S., Zweier J. L., Mukherjee G., Quinn M. T. and Huso D. L. (1998) Measurement and characterization of superoxide generation in microglial cells: evidence for an NADPH oxidase-dependent pathway. Arch. Biochem. Biophys. 353, 312-321.
41. Sheng H., Brady T. C., Pearlstein R. D., Crapo J. D. and Warner D. S. (1999a) Extracellular superoxide dismutase deficiency worsens outcome from focal cerebral ischemia in the mouse. Neurosci. Lett. 267, 13-16.
42. Sheng H., Bart R. D., Oury T. D., Pearlstein R. D., Crapo J. D. and Warner D. S. (1999b) Mice overexpressing extracellular superoxide dismutase have increased resistance to focal cerebral ischemia. Neuroscience 88, 185-191.
43. Simons J. M., Hart B. A., Ip Vai Ching T. R., Van Dijk H. and Labadie R. P. (1990) Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils. Free Radic. Biol. Med. 8, 251-258.
44. Steward O., Torre E. R., Phillips L. L. and Trimmer P. A. (1990) The process of reinnervation in the dentate gyrus of adult rats: time course of increases in mRNA for glial flbrillary acidic protein. J. Neurosci. 10, 2373-2384.
45. Steward O., Torre E. R., Tomasulo R. and Lothman E. (1991) Neuronal activity up-regulates astroglial gene expression. Proc. Natl Acad. Sci. USA 88, 6819-6823.
46. Sun A. Y., Cheng Y., Bu Q. and Oldfield F. (1992) The biochemical mechanisms of the excitotoxicity of kainic acid. Free radical formation. Mol. Chem. Neuropathol. 17, 51-63.
47. Tammariello S. P., Quinn M. T. and Estus S. (2000) NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor-deprived sympathetic neurons. J. Neurosci. 20, RC53.
48. Tan D. X., Manchester L. C., Reiter R. J., Qi W., Kim S. J. and El-Sokkary G. H. (1998) Melatonin protects hippocampal neurons in vivo against kainic acid-induced damage in mice. J. Neurosci. Res. 54, 382-389.
49. Tarpey M. M., White C. R., Suarez E., Richardson G., Radi R. and Freeman B. A. (1999) Chemiluminescent detection of oxidants in vascular tissue. Lucigenin but not coelenterazine enhances superoxide formation. Circ. Res. 84, 1203-1211.
50. Torre E. R., Lothman E. and Steward O. (1993) Glial response to neuronal activity: GFAP-mRNA and protein levels are transiently increased in the hippocampus after seizures. Brain Res. 631, 256-264.
51. Vezzani A., Conti M., De Luigi A., Ravizza T., Moneta D., Marchesi F. and De Simoni M. G. (1999) Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J. Neurosci. 19, 5054-5065.
52. Vezzani A., Moneta D., Richichi C., Aliprandi M., Burrows S. J., Ravizza T., Perego C. and De Simoni M. G. (2002) Functional role of inflammatory cytokines and antiinflammatory molecules in seizures and epileptogenesis. Epilepsia 43, 30-35.
53. Walder C. E., Green S. P., Darbonne W. C., Mathias J., Rae J., Dinauer M. C., Curnutte J. T. and Thomas G. R. (1997) Ischemic stroke injury is reduced in mice lacking a functional NADPH oxidase. Stroke 28, 2252-2258.
54. Wu D. C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D. K., Ischiropoulos H. and Przedborski S. (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22, 1763-1771.