H2O2 signaling in the nigrostriatal dopamine pathway via ATP-sensitive potassium channels: Issues and answers

Antioxidants and Redox Signaling

Volumn 9, Issue 2, 2007, Pages 219-231

  Avshalumov, Marat V ^a   Bao, Li ^a   Patel, Jyoti C ^a   Rice, Margaret E ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; DICHLOROFLUORESCEIN; DOPAMINE; FLUORESCENT DYE; GLUTAMATE RECEPTOR; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; 2',7'-DICHLOROFLUORESCEIN; ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; FLUORESCEIN DERIVATIVE; POTASSIUM; UNCLASSIFIED DRUG;

BRAIN SLICE; COGNITION; CYCLIC POTENTIOMETRY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOPAMINE RELEASE; DOPAMINERGIC SYSTEM; DOPAMINERGIC TRANSMISSION; FLUORESCENCE; HUMAN; IMAGE ANALYSIS; MOTOR ACTIVITY; NIGRONEOSTRIATAL SYSTEM; OXIDATION; PRIORITY JOURNAL; REVIEW; REWARD; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; ANIMAL; CHEMISTRY; CORPUS STRIATUM; FLUORESCENCE MICROSCOPY; GLIA; METABOLISM; MITOCHONDRION; NERVE CELL;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIOXIDANTS; CORPUS STRIATUM; DOPAMINE; FLUORESCEINS; HUMANS; HYDROGEN PEROXIDE; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; NEUROGLIA; NEURONS; POTASSIUM; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 33846262003     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2007.9.219     Document Type: Review

References (145)

1. Adam-Vizi V. Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antioxid Redox Signal 7: 1140-1149, 2005.
2. ATP channels. Physiol Rev 78: 227-245, 1998.
3. Albin RL, Young AB, and Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci 12: 366-375, 1989.
4. 2 gradients across biomembranes. FEBS Lett 475: 121-126, 2000.
5. 2 induce apoptosis through Fenton chemistry independent of the cellular thiol state. Free Radic Biol Med 30:1008-1018, 2001.
6. Arnaiz SL, Coronel MF, and Boveris A. Nitric oxide, superoxide, and hydrogen peroxide production in brain mitochondria after haloperidol treatment. Nitric Oxide 3: 235-243, 1999.
7. + channels. Trends Neurosci 21: 288-294, 1998.
8. Atkins CM and Sweatt JD, Reactive oxygen species mediate activity-dependent neuron-glia signaling in output fibers of the hippocampus. J Neurosci 19: 7241-7248, 1999.
9. Auerbach JM and Segal M. Peroxide modulation of slow onset potentiation in rat hippocampus. J Neurosci 17: 8695-8701, 1997.
10. Avshalumov MV and Rice ME. NMDA-receptor activation mediates hydrogen peroxide-induced pathophysiology in rat hippocampal slices. J Neurophysiol 87: 2896-2903, 2002.
11. 2 underlies glutamate-dependent inhibition of striatal dopamine release. Proc Natl Acad Sci USA 100: 11729-11734, 2003.
12. 2. J Neurosci 23: 2744-2750, 2003.
13. 2 signaling Neuron Glia Biol 1: 365-376, 2004.
14. Avshalumov MV, Chen BT, Koós T, Tepper JM, and Rice ME. Endogenous hydrogen peroxide regulates the excitability of midbrain dopamine neurons via ATP-sensitive potassium channels. J Neurosci 25: 4222-4231, 2005.
15. + channel openers. J Biol Chem 275: 717-720, 2000.
16. Babior BM. The respiratory burst of phagocytes. J Clin Invest 73: 599-601, 1984.
17. Babior BM. NADPH oxidase: an update. Blood 93: 1464-1476, 1999.
18. 2 mediates glutamate-dependent inhibition of striatal dopamine release, 2004 Abstract Viewer/Itinerary Planner, Washington, DC: Society for Neuroscience, 46.7, 2004.
19. 2, not decreased ATP. J Neurosci 25: 10029-10040, 2005.
20. Bass NH, Hess HH, Pope A, and Thalheimer C. Quantitative cytoarchitechtonic distribution of neurons, glia and DNA in rat cerebral cortex. J Comp Neurol 143: 481-490, 1971.
21. Berger UV and Hediger MA. The vitamin C transporter SVCT2 is expressed by astrocytes in culture but not in situ. Neuroreport 11: 1395-1399, 2000.
22. Bernard V and Bolam JP. Subcellular and subsynaptic distribution of the NR1 subunit of the NMDA receptor in the neostriatum and globus pallidus of the rat: colocalization at synapses with the GluR2/3 subunit of the AMPA receptor. Eur J Neurosci 10: 3721-3738, 1998.
23. Bindokas VP, Jordan J, Lee CC, and Miller RJ. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J Neurosci 16: 1324-1336, 1996.
24. Björnberg O, Ostergaard H, and Winther JR. Measuring intracellular redox conditions using GFP-based sensors. Antioxid Redox Signal 8: 354-361, 2006.
25. Boveris A and Chance B. The mitochondrial generation of hydrogen peroxide: general properties and the effect of hyperbaric oxygen. Biochem J 134: 707-716, 1973.
26. Brahma B, Forman RE, Stewart EE, Nicholson C, and Rice ME. Ascorbate inhibits brain slice edema. J Neurochem 74: 1263-1270, 2000.
27. Cannon CM and Bseikri MR. Is dopamine required for natural reward? Physiol Behav 81: 741-748, 2004.
28. Cannon MB and Remington SJ. Re-engineered redox-sensitive green fluorescent protein for improved response rate. Protein Sci 15: 45-57, 2006
29. Cao W, Carney JM, Duchon A, Floyd RA, and Chevion M. Oxygen free radical involvement in ischemia and reperfusion injury to brain. Neurosci Lett 88; 233-238, 1988.
30. Carlsson A. Treatment of Parkinson's with L-DOPA. The early discovery phase, and a comment on current problems. J Neural Transm 109: 777-787, 2002.
31. 2+ overload and ROS generation in spinal motor neurons in vitro. J Neurosci 20, 240-250, 2000.
32. Castner SA, Goldman-Rakic PS, and Williams GV. Animal models of working memory: insights for targeting cognitive dysfunction in schizophrenia. Psychopharmacol (Berl) 174: 111-125, 2004.
33. Cathcart R, Schwiers E, and Ames BN. Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal Biochem 134: 111-116, 1983.
34. Chan PH. Mitochondria and neuronal death/survival signaling pathways in cerebral ischemia. Neurochem Res 29: 1943-1949, 2004.
35. Chance B, Sies H, and Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605, 1979.
36. Chang MCY, Pralle A, Isacoff EY, and Chang CJ. A selective, cell-permeable optical probe for hydrogen peroxide in living cells. Am Chem Soc 126: 15392-1593, 2004.
37. Chase TN and Oh JD, Striatal dopamine- and glutamate-mediated dysregulation in experimental parkinsonism. Trends Neurosci 23, S86-S91, 2000.
38. 2 is a novel, endogenous modulator of synaptic dopamine release. J Neurophysiol 85: 2468-2476, 2001.
39. 2: susceptibility in substantia nigra but resistance in the ventral tegmental area. J Neurophysiol 87: 1155-1158, 2002.
40. Chen Q, Veenman L, Knopp K, Yan Z, Medina L, Song WJ, Surmeier DJ, and Reiner A. Evidence for the preferential localization of glutamate receptor-1 subunits of AMPA receptors to the dendritic spines of medium spiny neurons in rat striatum. Neuroscience 83: 749-761, 1998.
41. ATP channels in guinea pig ventricular cells. Am J Physiol 269: H1625-H1633, 1995.
42. Cohen G. Enzymatic/nonenzymatic sources of oxyradicals and regulation of antioxidant defenses. Ann NY Acad Sci 738: 8-14, 1994.
43. Cohen G, Farooqui R, and Kesler N. Parkinson disease: a new link between monoamine oxidase and mitochondrial electron flow. Proc Natl Acad Sci USA 94: 4890-4894, 1997.
44. Davies KJA. Proteolytic systems as secondary antioxidant defenses. In: Chow, C.K. (Ed.), Cellular Antioxidant Defense Mechanisms. CRC Press, Boca Raton, pp. 25-67, 1988.
45. Desagher S, Glowinski J, and Premont J. Astrocytes protect neurons from hydrogen peroxide toxicity. J Neurosci 16: 2553-2562, 1996.
46. Deutsch SI., Rosse RB, Schwartz BL, and Mastropaolo J. A revised excitotoxic hypothesis of schizophrenia: therapeutic implications, Clin Neuropharmacol 24: 43-49, 2001.
47. Do KQ, Trabesinger AH, Kirsten-Kruger M, Lauer CJ, Dydak U, Hell D, Holsboer F, Boesiger P, and Cuenod M. Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo. Eur J Neurosci 12: 3721-3728, 2000.
48. Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, and Tsein RY. Imaging dynamic redox changes in mammalian cells with green fluorescent indicators. J Biol Chem 279: 22284-22293, 2004.
49. Dringen R and Hamprecht B. Involvement of glutathione peroxidase and catalase in the disposal of exogenous hydrogen peroxide by cultured astroglial cells. Brain Res 759: 67-75, 1997.
50. Dringen R and Hirrlinger J. Glutathione pathways in the brain. Biol Chem 384: 505-516, 2003.
51. Dringen R, Kussmaul L, Gutterer JM, Hirrlinger J, and Hamprecht B. The glutathione system of peroxide detoxification is less efficient in neurons than in astroglial cells. J Neurochem 72: 2523-2530, 1999.
52. Dringen R, Pawlowski PG, and Hirrlinger J. Peroxide detoxification by brain cells. J Neurosci Res 79: 157-165, 2005.
53. Drukarch B, Schepens E, Jongenelen CA, Stoof JC, and Langeveld CH. Astrocyte-mediated enhancement of neuronal survival is abolished by glutathione deficiency. Brain Res 770: 123-130, 1997.
54. Drukarch B, Schepens E, Stoof JC, Langeveld CH, and Van Muiswinkel FL. Astrocyte-enhanced neuronal survival is mediated by scavenging of extracellular reactive oxygen species. Free Rad Biol Med 25: 217-220, 1998.
55. Dugan LL, Sensi SL, Canzoniero LM, Handran SD, Rothman SM, Lin TS, Goldberg MP, and Choi DW. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J Neurosci 15: 6377-6388, 1995.
56. Dunn-Meynell AA, Routh VH, McArdle JJ, and Levin BE. Low-affinity sulfonylurea binding sites reside on neuronal cell bodies in the brain. Brain Res 745: 1-9, 1997.
57. Ebadi M, Srinivasan SK, and Baxi MD. Oxidative stress and antioxidant therapy in Parkinson's disease. Prog Neurobiol 48: 1-19, 1996.
58. Esposito F, Ammendola R, Faraonio R, Russo T, and Cimino F. Redox control of signal transduction, gene expression and cellular senescence. Neurochem Res 29: 617-628, 2004.
59. Evans AH and Lees AJ. Dopamine dysregulation syndrome in Parkinson's disease. Curr Opin Neurol 17: 393-398, 2004.
60. Fearnley J and Lees AJ. Aging and Parkinson's disease: substantia nigra regional selectivity. Brain 114: 2283-2301, 1991.
61. Fiskum G, Starkov A, Polster BM, and Chinopoulos C. Mitochondrial mechanisms of neural cell death and neuroprotective interventions in Parkinson's disease. Ann NY Acad Sci 991: 111-119, 2003.
62. Friede R. Der quantitative Anteil der Glia an der Cortexentwicklung. Acta Anatomica 20: 290-296, 1954.
63. A receptor subunits in the striatum of the rat. J Comp Neurol 416: 158-172, 2000.
64. Garguilo MG and Michael AC. Amperometric microsensors for monitoring choline in the extracellular fluid of brain. J Neurosci Meth 70: 73-82, 1996.
65. Greenamyre JT. Glutamatergic influences on the basal ganglia, Clin Neuropharmacol 24: 65-70, 2001.
66. Greenamyre JT, Sherer TB, Betarbet R, and Panov AV. Complex I and Parkinson's disease. IUBMB Life 52: 135-141, 2001
67. Haddad JJ. Antioxidant and prooxidant mechanisms in the regulation of redox(y)-sensitive transcription factors. Cell Signal 14, 879-897, 2002.
68. Hagerdal M, Harp J, Nilsson L, and Siesjö BK. The effect of induced hypothermia upon oxygen consumption in the rat brain. J Neurochem 24: 311-316, 1975
69. Haug H. Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). Am J Anat (now Developmental Dynamics) 180: 126-142, 1987.
70. + channels in substantia nigra. Biochem Biophys Res Comm 174: 909-914, 1991.
71. Homan-Muller JW, Weening RS, and Roos D. Production of hydrogen peroxide by phagocytizing human granulocytes. J Lab Clin Med 85: 198-207, 1975.
72. Hung HC and Lee EH. MPTP produces differential oxidative stress and antioxidative responses in the nigrostriatal and mesolimbic dopaminergic pathways. Free Radic Biol Med 24: 76-84, 1998.
73. Hyman SE and Malenka RC. Addiction and the brain: the neurobiology of compulsion and its persistence. Nat Rev Neurosci 2: 695-703, 2001.
74. 2 in vitro. Brain Res 671: 181-186, 1995.
75. Ichinari K, Kakei M, Matsuoka T, Nakashima H, and Tanaka H. Direct activation of the ATP-sensitive potassium channel by oxygen free radicals in guinea pig ventricular cells: its potentiation by MgADP. J Mol Cell Cardiol 28: 1867-1877, 1996.
76. + channels. Neuron 16: 1011-1017.
77. Kamsler A and Segal M. Hydrogen peroxide modulation of synaptic plasticity. J Neurosci 23: 269-276, 2003.
78. Kamsler A and Segal M. Hydrogen peroxide as a diffusible signal molecule in synaptic plasticity. Mol Neurobiol 29: 167-178, 2004.
79. ATP channel-forming Kir6.2 subunit and the sulfonylurea receptor SUR1 in rodent brain, FEBS Lett 401: 59-64, 1997.
80. Kemp JM and Powell TP. The structure of the caudate nucleus of the cat: light and electron microscopy. Philos Trans R Soc Lond B Biol Sci 262: 383-401, 1971.
81. Kishida KT, Pao M, Holland SM, and Klann E. NADPH oxidase is required for NMDA receptor-dependent activation of ERK in hippocampal area CA1. J Neurochem 94: 299-306, 2005.
82. Knapp LT and Klann E. Role of reactive oxygen species in hippocampal long-term potentiation: contributory or inhibitory? J Neurosci Res 70: 1-7, 2002.
83. Koob GF. Neurobiology of addiction. Toward the development of new therapies, Ann NY Acad Sci 909: 170-185, 2000.
84. 2 with stimulus-secretion coupling in mouse pancreatic beta-cells. J Physiol (Lond) 514: 471-481, 1999.
85. Kudin AP, Debska-Vielhaber G, and Kunz WS. Characterization of superoxide production sites in isolated rat brain and skeletal muscle mitochondria. Biomed Pharmacother 59: 163-168, 2005.
86. Kulagina NV and Michael AC. Monitoring hydrogen peroxide in the extracellular space of the brain with amperometric microsensors. Anal Chem 75: 4875-4881, 2003.
87. LeBel CP, Ischiropoulos H, and Bondy SC. Evaluation of the probe 2′,7′-dichloro-fluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5: 227-231, 1992.
88. Liss B, Bruns R, and Roeper J. Alternative sulfonylurea receptor expression defines sensitivity to K-ATP channels in dopaminergic midbrain neurons. EMBO J 18: 833-846, 1999.
89. Liu Y, Fiskum G, and Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80: 780-787, 2002.
90. Makar TK, Nedergaard M, Preuss A, Gebard AS, Perumal AS, and Cooper AJL. Vitamin E, ascorbate, glutathione, glutathione disulfide, and enzymes of oxidative metabolism in cultures of chick astrocytes and neurons: evidence that astrocytes play an important role in oxidative processes in the brain. J Neurochem 62: 45-53, 1994.
91. McIlwain H and Bachelard HS. Biochemistry and the Central Nervous System. New York: Churchill Livingstone, pp. 59-60, 1985
92. McMahon CP, Rocchitta G, Serra PA, Kirwan SM, Lowry JP, and O'Neill RD. Control of the oxygen dependence of an implantable polymer/enzyme composite biosensor for glutamate. Anal Chem 78: 2352-2359, 2006.
93. Meister A. Glutathione-ascorbic acid antioxidant system in animals. J Biol Chem 269: 9397-9400, 1994.
94. Miller EW, Albers AE, Pralle A, Isacoff EY, and Chang CJ. Boronate-based fluorescent probes for imaging cellular hydrogen peroxide. J Am Chem Soc 127: 16652-16659, 2005.
95. + channels. Brain Res 526: 147-152, 1990.
96. Nirenberg MJ, Chan J, Liu Y, Edwards RH, and Pickel VM. Vesicular monoamine transporter-2: immunogold localization in striatal axons and terminals. Synapse 26: 194-198, 1997.
97. Olanow CW and Tatton WG. Etiology and pathogenesis of Parkinson's disease. Ann Rev Neurosci 22: 123-144, 1999.
98. Orth M and Schapira AH. Mitochondrial involvement in Parkinson's disease. Neurochem Int 40: 533-541, 2002.
99. Østergaard H, Henriksen A, Hansen FG, and Winther JR. Shedding light on disulfide bond formation: engineering a redox switch in green fluorescent protein. EMBO J 20: 5853-5862, 2001.
100. Oyama Y, Hayashi A, Ueha T, and Maekawa K. Characterization of 2′,7′-dichlorofluorescin fluorescence in dissociated mammalian brain neurons: estimation on intracellular content of hydrogen peroxide. Brain Res 635: 113-117, 1994.
101. Patel J and Rice ME. Monitoring dopamine release in brain slices. In: Encyclopedia of Sensors, Vol. 6, Grimes, C. A., Dickey, E. C., and Pishko, M. V. eds. Stevenson Ranch, California: American Scientific Publishers, pp. 313-334, 2006.
102. 2 generated in medium spiny neurons but not in dopamine terminals, 2004 Abstract Viewer/Itinerary Planner, Washington, DC: Society for Neuroscience, 46.6, 2004
103. Pellmar T. Electrophysiological correlates of peroxide damage in guinea pig hippocampus in vitro. Brain Res 364: 377-381, 1986.
104. Pellmar TC. Peroxide alters neuronal excitability in the CA1 region of guinea-pig hippocampus in vitro. Neuroscience 23: 447-456, 1987.
105. Pellmar TC. Use of brain slices in the study of free-radical actions. J Neurosci Meth 59: 93-98, 1995.
106. Peuchen S, Bolanos JP, Heales SJ, Almeida A, Duchen MR, and Clark JB. Interrelationships between astrocyte function, oxidative stress and antioxidant status within the central nervous system. Prog Neurobiol 52: 261-281, 1997.
107. 2 in biomembranes. Biochim Biophys Acta 694: 69-93, 1982.
108. Raps SP, Lai JCK, Hertz L, and Cooper AJL. Glutathione is present in high concentrations in cultured astrocytes but not in cultured neurons. Brain Res 493: 398-401, 1989.
109. Reynolds IJ and Hastings TG. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci 15: 3318-3327, 1995.
110. Rhee SG, Kang SW, Jeong W, Chang TS, Yang KS, and Woo HA. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 17: 183-189, 2005.
111. Rice ME. Ascorbate regulation and its neuroprotective role in the brain. Trends Neurosci 23: 209-216, 2000.
112. Rice ME and Nicholson C. Diffusion characteristics and extracellular volume fraction during normoxia and hypoxia in slices of rat neostriatum. J Neurophysiol 65: 264-272, 1991.
113. Rice ME and Russo-Menna I. Differential compartmentalization of brain ascorbate and glutathione between neurons and glia. Neuroscience 82: 1213-1223, 1998.
114. Saez JC, Kessler JA, Bennett MV, and Spray DC. Superoxide dismutase protects cultured neurons against death by starvation. Proc Natl Acad Sci USA 84: 3056-3059, 1987.
115. Sah R and Schwartz-Bloom RD. Optical imaging reveals elevated intracellular chloride in hippocampal pyramidal cells after oxidative stress. J Neurosci 19: 9209-9217, 1999.
116. 2+ efflux. Biochim Biophys Acta 1035: 300-305, 1990.
117. Sauer H, Wartenberg M, and Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 11: 173-186, 2001.
118. Sawa A and Snyder SH. Schizophrenia: diverse approaches to a complex disease. Science 296: 692-695, 2002.
119. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, and Marsden CD. Mitochondrial complex 1 deficiency in Parkinson's disease. J Neurochem 54: 823-827, 1990.
120. Serrano F, Kolluri NS, Wientjes FB, Cacd JP and Klann E. NADPH oxidase immunoreactivity in the mouse brain. Brain Res 988: 193-188, 2003.
121. Siesjö BK. Brain Energy Metabolism. New York: Wiley, 1980, p. 131-150, 1980.
122. Seutin V, Scuvee-Moreau J, Masotte L, and Dresse A. Hydrogen peroxide hyperpolarizes rat CA1 pyramidal neurons by inducing an increase in potassium conductance. Brain Res 683: 275-278, 1995.
123. Shih JC, Chen K, and Ridd MJ. Monoamine oxidase: from genes to behavior. Ann Rev Neurosci 22: 197-217, 1999.
124. Slivka A, Mytilineou C, and Cohen G. Histochemical evaluation of glutathione in brain. Brain Res 409: 275-284, 1987.
125. Smith AD and Bolam JP. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurons. Trends Neurosci 13: 259-265, 1990.
126. Sonsalla PK, Manzino L, Sinton CM, Liang CL, German DC, and Zeevalk GD. Inhibition of striatal energy metabolism produces cell loss in the ipsilateral substantia nigra. Brain Research 773: 223-226, 1997.
127. Starkov AA, Chinopoulos C, and Fiskum G. Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36: 257-264, 2004.
128. Stone JR and Yang S. Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal 8: 243-270, 2006
129. Stults FH, Forstrom JW, Chiu, DTY, and Tappel AL. Rat liver glutathione peroxidase: purification and study of multiple forms. Arch Biochem Biophys 183: 490-497, 1977.
130. Tanaka J, Toku K, Zhang B, Ishihara K, Sakanaka M, and Maeda N. Astrocytes prevent neuronal death induced by reactive oxygen and nitrogen species. Glia 28: 85-96, 1999.
131. Tejada-Simon MV, Serrano F, Villasana LE, Kanterewicz BI, Wu GY, Quinn MT, and Klann E. Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol Cell Neurosci 29: 97-106, 2005.
132. ATP channels in guinea-pig ventricular myocytes. Pflugers Arch 437: 155-157, 1998.
133. Tower DB and Elliott KAC. Activity of the acetylcholine system in cerebral cortex of various unanesthetized animals. Am J Physiol 168: 747-759, 1952.
134. Tower DB and Young OM. The activities of butyrylcholinesterase and carbonic anhydrase, the rate of anaerobic glycolysis, and the question of a constant density of glial cells in the cerebral cortices of various mammalian species from mouse to whale. J Neurochem 20: 269-278, 1973.
135. Trépanier G, Furling D, Puymirat J, and Mirault ME. Immunocytochemical localization of seleno-glutathione peroxidase in the adult mouse brain. Neuroscience 75: 231-243, 1996.
136. +-dependent L-ascorbic acid transporters. Nature 399: 70-75, 1999.
137. m-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J Neurochem 79: 266-277, 2001.
138. Xia Y and Haddad GG. Major differences in CNS sulfonylurea receptor distribution between the rat (newborn, adult) and turtle. J Comp Neurol 314: 278-289, 1991.
139. Xu J, Kao SY, Lee FJ, Song W, Jin LW and Yankner BA. Dopamine-dependent neurotoxicity of α-synuclein: A mechanism for selective neurodegeneration in Parkinson disease. Nature Medicine 8: 600-606, 2002
140. Yamada T, McGeer PL, Baimbridge KG, and McGeer EG. Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28K. Brain Res 526: 303-307, 1990.
141. Yao JK, Reddy RD and van Kammen DP. Oxidative damage and schizophrenia: an overview of the evidence and its therapeutic implications. CNS Drugs 15: 287-310, 2001
142. Yu BP. Cellular defenses against damage from reactive oxygen species. Physiol Rev 74: 139-162, 1994.
143. Zekry D, Epperson TK, and Krause KH. A role for NOX NADPH oxidases in Alzheimer's disease and other types of dementia? IUBMB Life 55: 307-313, 2003.
144. Zhang Y, Dawson VL, and Dawson TM. Oxidative stress and genetics in the pathogenesis of Parkinson's disease. Neurobiol Dis 7: 240-250, 2000.
145. Zhou M, Diwu Z, Panchuk-Voloshina N, and Haugland RP. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal Biochem 253: 162-168, 1997.