Generation of reactive oxygen species in 1-methyl-4-phenylpyridinium (MPP+) treated dopaminergic neurons occurs as an NADPH oxidase-dependent two-wave cascade

Journal of Neuroinflammation

Volumn 8, Issue , 2011, Pages

  Zawada, W Michael ^a   Banninger, Gregg P ^a   Thornton, Jennifer ^a   Marriott, Beth ^a   Cantu, David ^a   Rachubinski, Angela L ^a   Das, Mita ^b   Griffin, W Sue T ^a   Jones, Susan M ^c  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c SWEDISH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; CELL PROTEIN; HYDROGEN PEROXIDE; LOSARTAN; MESSENGER RNA; PROTEIN P22 PHOX; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMALL INTERFERING RNA; SUPEROXIDE; UNCLASSIFIED DRUG; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; HERBICIDE; OXIDIZING AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL STRESS; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG MECHANISM; ENZYME ACTIVATION; FEMALE; FLOW CYTOMETRY; GENE SILENCING; IMMUNOBLOTTING; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; SUBSTANTIA NIGRA; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL LINE; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; METABOLISM; PROTEIN SUBUNIT;

1-METHYL-4-PHENYLPYRIDINIUM; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; CELL LINE; DOPAMINERGIC NEURONS; ELECTRON TRANSPORT COMPLEX I; FEMALE; HERBICIDES; HYDROGEN PEROXIDE; LOSARTAN; MICE; MICE, INBRED C57BL; NADPH OXIDASE; OXIDANTS; PROTEIN SUBUNITS; RATS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SUBSTANTIA NIGRA;

EID: 80053479099     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-8-129     Document Type: Article

References (75)

1. Rigoulet M, Yoboue ED, Devin A. Mitochondrial ROS generation and its regulation: mechanisms involved in H(2)O(2) signaling. Antioxid Redox Signal 2011, 14:459-468. 10.1089/ars.2010.3363, 20649461.
2. Niethammer P, Grabher C, Look AT, Mitchison TJ. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 2009, 459:996-999. 10.1038/nature08119, 2803098, 19494811.
3. Dexter DT, Carter CJ, Wells FR, Javoy-Agid F, Agid Y, Lees A, et al. Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J Neurochem 1989, 52:381-389. 10.1111/j.1471-4159.1989.tb09133.x, 2911023.
4. Alam ZI, Daniel SE, Lees AJ, Marsden DC, Jenner P, Halliwell B. A generalised increase in protein carbonyls in the brain in Parkinson's but not incidental Lewy body disease. J Neurochem 1997, 69:1326-1329.
5. Floor E, Wetzel MG. Increased protein oxidation in human substantia nigra pars compacta in comparison with basal ganglia and prefrontal cortex measured with an improved dinitrophenylhydrazine assay. J Neurochem 1998, 70:268-275.
6. Rock RB, Gekker G, Hu S, Sheng WS, Cheeran M, Lokensgard JR, et al. Role of microglia in central nervous system infections. Clin Microbiol Rev 2004, 17:942-64. table, 10.1128/CMR.17.4.942-964.2004, 523558, 15489356.
7. Gao HM, Liu B, Zhang W, Hong JS. Critical role of microglial NADPH oxidase-derived free radicals in the in vitro MPTP model of Parkinson's disease. FASEB J 2003, 17:1954-1956.
8. Wu DC, Teismann P, Tieu K, Vila M, Jackson-Lewis V, Ischiropoulos H, et al. NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Proc Natl Acad Sci USA 2003, 100:6145-6150. 10.1073/pnas.0937239100, 156340, 12721370.
9. Kanthasamy A, Jin H, Mehrotra S, Mishra R, Kanthasamy A, Rana A. Novel cell death signaling pathways in neurotoxicity models of dopaminergic degeneration: relevance to oxidative stress and neuroinflammation in Parkinson's disease. Neurotoxicology 2010, 31:555-561. 10.1016/j.neuro.2009.12.003, 2888638, 20005250.
10. DeChatelet LR, McPhail LC, Mullikin D, McCall CE. An isotopic assay for NADPH oxidase activity and some characteristics of the enzyme from human polymorphonuclear leukocytes. J Clin Invest 1975, 55:714-721. 10.1172/JCI107981, 301807, 235561.
11. Joglar B, Rodriguez-Pallares J, Rodriguez-Perez AI, Rey P, Guerra MJ, Labandeira-Garcia JL. The inflammatory response in the MPTP model of Parkinson's disease is mediated by brain angiotensin: relevance to progression of the disease. J Neurochem 2009, 109:656-669. 10.1111/j.1471-4159.2009.05999.x, 19245663.
12. Brandes RP, Kreuzer J. Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc Res 2005, 65:16-27. 10.1016/j.cardiores.2004.08.007, 15621030.
13. Sumimoto H, Miyano K, Takeya R. Molecular composition and regulation of the Nox family NAD(P)H oxidases. Biochem Biophys Res Commun 2005, 338:677-686. 10.1016/j.bbrc.2005.08.210, 16157295.
14. Katsuyama M. NOX/NADPH oxidase, the superoxide-generating enzyme: its transcriptional regulation and physiological roles. J Pharmacol Sci 2010, 114:134-146. 10.1254/jphs.10R01CR, 20838023.
15. Pachucki J, Wang D, Christophe D, Miot F. Structural and functional characterization of the two human ThOX/Duox genes and their 5'-flanking regions. Mol Cell Endocrinol 2004, 214:53-62. 10.1016/j.mce.2003.11.026, 15062544.
16. Kawahara T, Quinn MT, Lambeth JD. Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol Biol 2007, 7:109. 10.1186/1471-2148-7-109, 1940245, 17612411.
17. Anantharam V, Kaul S, Song C, Kanthasamy A, Kanthasamy AG. Pharmacological inhibition of neuronal NADPH oxidase protects against 1-methyl-4-phenylpyridinium (MPP+)-induced oxidative stress and apoptosis in mesencephalic dopaminergic neuronal cells. Neurotoxicology 2007, 28:988-997. 10.1016/j.neuro.2007.08.008, 2140261, 17904225.
18. Kim JA, Neupane GP, Lee ES, Jeong BS, Park BC, Thapa P. NADPH oxidase inhibitors: a patent review. Expert Opin Ther Pat 2011, 21:1147-1158. 10.1517/13543776.2011.584870, 21554154.
19. Petry A, Weitnauer M, Gorlach A. Receptor activation of NADPH oxidases. Antioxid Redox Signal 2010, 13:467-487. 10.1089/ars.2009.3026, 20001746.
20. Naik P, Murumkar P, Giridhar R, Yadav MR. Angiotensin II receptor type 1 (AT1) selective nonpeptidic antagonists--a perspective. Bioorg Med Chem 2010, 18:8418-8456. 10.1016/j.bmc.2010.10.043, 21071232.
21. Rueckschloss U, Quinn MT, Holtz J, Morawietz H. Dose-dependent regulation of NAD(P)H oxidase expression by angiotensin II in human endothelial cells: protective effect of angiotensin II type 1 receptor blockade in patients with coronary artery disease. Arterioscler Thromb Vasc Biol 2002, 22:1845-1851. 10.1161/01.ATV.0000035392.38687.65, 12426214.
22. McGeer PL, Itagaki S, Boyes BE, McGeer EG. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 1988, 38:1285-1291.
23. Banati RB, Daniel SE, Blunt SB. Glial pathology but absence of apoptotic nigral neurons in long-standing Parkinson's disease. Mov Disord 1998, 13:221-227. 10.1002/mds.870130205, 9539333.
24. Orr CF, Rowe DB, Mizuno Y, Mori H, Halliday GM. A possible role for humoral immunity in the pathogenesis of Parkinson's disease. Brain 2005, 128:2665-2674. 10.1093/brain/awh625, 16219675.
25. Imamura K, Hishikawa N, Sawada M, Nagatsu T, Yoshida M, Hashizume Y. Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol 2003, 106:518-526. 10.1007/s00401-003-0766-2, 14513261.
26. Croisier E, Moran LB, Dexter DT, Pearce RK, Graeber MB. Microglial inflammation in the parkinsonian substantia nigra: relationship to alpha-synuclein deposition. J Neuroinflammation 2005, 2:14. 10.1186/1742-2094-2-14, 1177985, 15935098.
27. Hirsch EC. Glial cells and Parkinson's disease. J Neurol 2000, 247(Suppl 2):II58-II62.
28. Minghetti L, Levi G. Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide. Prog Neurobiol 1998, 54:99-125. 10.1016/S0301-0082(97)00052-X, 9460796.
29. Lawson LJ, Perry VH, Dri P, Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990, 39:151-170. 10.1016/0306-4522(90)90229-W, 2089275.
30. Jeohn GH, Cooper CL, Jang KJ, Liu B, Lee DS, Kim HC, et al. Go6976 inhibits LPS-induced microglial TNFalpha release by suppressing p38 MAP kinase activation. Neuroscience 2002, 114:689-697. 10.1016/S0306-4522(02)00356-1, 12220570.
31. Gao HM, Jiang J, Wilson B, Zhang W, Hong JS, Liu B. Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J Neurochem 2002, 81:1285-1297. 10.1046/j.1471-4159.2002.00928.x, 12068076.
32. Babior BM. NADPH oxidase. Curr Opin Immunol 2004, 16:42-47. 10.1016/j.coi.2003.12.001, 14734109.
33. Babior BM. NADPH oxidase: an update. Blood 1999, 93:1464-1476.
34. Noh KM, Koh JY. Induction and activation by zinc of NADPH oxidase in cultured cortical neurons and astrocytes. J Neurosci 2000, 20:RC111.
35. Tejada-Simon MV, Serrano F, Villasana LE, Kanterewicz BI, Wu GY, Quinn MT, et al. Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol Cell Neurosci 2005, 29:97-106. 10.1016/j.mcn.2005.01.007, 2013304, 15866050.
36. Serrano F, Kolluri NS, Wientjes FB, Card JP, Klann E. NADPH oxidase immunoreactivity in the mouse brain. Brain Res 2003, 988:193-198. 10.1016/S0006-8993(03)03364-X, 14519542.
37. Mizuki K, Kadomatsu K, Hata K, Ito T, Fan QW, Kage Y, et al. Functional modules and expression of mouse p40(phox) and p67(phox), SH3-domain-containing proteins involved in the phagocyte NADPH oxidase complex. Eur J Biochem 1998, 251:573-582. 10.1046/j.1432-1327.1998.2510573.x, 9490028.
38. Glass MJ, Huang J, Oselkin M, Tarsitano MJ, Wang G, Iadecola C, et al. Subcellular localization of nicotinamide adenine dinucleotide phosphate oxidase subunits in neurons and astroglia of the rat medial nucleus tractus solitarius: relationship with tyrosine hydroxylase immunoreactive neurons. Neuroscience 2006, 143:547-564. 10.1016/j.neuroscience.2006.08.051, 1808229, 17027166.
39. Hilburger EW, Conte EJ, McGee DW, Tammariello SP. Localization of NADPH oxidase subunits in neonatal sympathetic neurons. Neurosci Lett 2005, 377:16-19. 10.1016/j.neulet.2004.11.066, 15722179.
40. Tejada-Simon MV, Serrano F, Villasana LE, Kanterewicz BI, Wu GY, Quinn MT, et al. Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol Cell Neurosci 2005, 29:97-106. 10.1016/j.mcn.2005.01.007, 2013304, 15866050.
41. Munnamalai V, Suter DM. Reactive oxygen species regulate F-actin dynamics in neuronal growth cones and neurite outgrowth. J Neurochem 2009, 108:644-661. 10.1111/j.1471-4159.2008.05787.x, 2995541, 19054285.
42. Abramov AY, Canevari L, Duchen MR. Calcium signals induced by amyloid beta peptide and their consequences in neurons and astrocytes in culture. Biochim Biophys Acta 2004, 1742:81-87. 10.1016/j.bbamcr.2004.09.006, 15590058.
43. Gao HM, Liu B, Zhang W, Hong JS. Critical role of microglial NADPH oxidase-derived free radicals in the in vitro MPTP model of Parkinson's disease. FASEB J 2003, 17:1954-1956.
44. Clarkson ED, Rosa FG, Edwards-Prasad J, Weiland DA, Witta SE, Freed CR, et al. Improvement of neurological deficits in 6-hydroxydopamine-lesioned rats after transplantation with allogeneic simian virus 40 large tumor antigen gene-induced immortalized dopamine cells. Proc Natl Acad Sci USA 1998, 95:1265-1270. 10.1073/pnas.95.3.1265, 18740, 9448320.
45. Singer TP, Ramsay RR. Mechanism of the neurotoxicity of MPTP. An update. FEBS Lett 1990, 274:1-8. 10.1016/0014-5793(90)81315-F, 2253761.
46. Noh KM, Koh JY. Induction and activation by zinc of NADPH oxidase in cultured cortical neurons and astrocytes. J Neurosci 2000, 20:RC111.
47. Hilburger EW, Conte EJ, McGee DW, Tammariello SP. Localization of NADPH oxidase subunits in neonatal sympathetic neurons. Neurosci Lett 2005, 377:16-19. 10.1016/j.neulet.2004.11.066, 15722179.
48. Abramov AY, Jacobson J, Wientjes F, Hothersall J, Canevari L, Duchen MR. Expression and modulation of an NADPH oxidase in mammalian astrocytes. J Neurosci 2005, 25:9176-9184. 10.1523/JNEUROSCI.1632-05.2005, 16207877.
49. Gao HM, Liu B, Hong JS. Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J Neurosci 2003, 23:6181-6187.
50. Ramsay RR, Krueger MJ, Youngster SK, Gluck MR, Casida JE, Singer TP. Interaction of 1-methyl-4-phenylpyridinium ion (MPP+) and its analogs with the rotenone/piericidin binding site of NADH dehydrogenase. J Neurochem 1991, 56:1184-1190. 10.1111/j.1471-4159.1991.tb11409.x, 2002336.
51. Hasegawa E, Asagami H, Kang D, Minakami S, Takeshige K. 1-Methyl-4-phenylpyridinium (MPP+) inhibits mitochondrial oxygen consumption mediated by succinate as well as malate in rat pheochromocytoma PC12 cells. Biochem Mol Biol Int 1995, 35:409-413.
52. Hasegawa E, Takeshige K, Oishi T, Murai Y, Minakami S. 1-Methyl-4-phenylpyridinium (MPP+) induces NADH-dependent superoxide formation and enhances NADH-dependent lipid peroxidation in bovine heart submitochondrial particles. Biochem Biophys Res Commun 1990, 170:1049-1055. 10.1016/0006-291X(90)90498-C, 2167668.
53. Griendling KK, Sorescu D, Lassegue B, Ushio-Fukai M. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol 2000, 20:2175-2183. 10.1161/01.ATV.20.10.2175, 11031201.
54. Grammatopoulos TN, Jones SM, Ahmadi FA, Hoover BR, Snell LD, Skoch J, et al. Angiotensin type 1 receptor antagonist losartan, reduces MPTP-induced degeneration of dopaminergic neurons in substantia nigra. Mol Neurodegener 2007, 2:1. 10.1186/1750-1326-2-1, 1783655, 17224059.
55. Rodriguez-Pallares J, Parga JA, Munoz A, Rey P, Guerra MJ, Labandeira-Garcia JL. Mechanism of 6-hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamine-induced degeneration of dopaminergic neurons. J Neurochem 2007, 103:145-156.
56. Misiak M, Beyer C, Arnold S. Gender-specific role of mitochondria in the vulnerability of 6-hydroxydopamine-treated mesencephalic neurons. Biochim Biophys Acta 2010, 1797:1178-1188. 10.1016/j.bbabio.2010.04.009, 20416276.
57. Wu DC, Teismann P, Tieu K, Vila M, Jackson-Lewis V, Ischiropoulos H, et al. NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Proc Natl Acad Sci USA 2003, 100:6145-6150. 10.1073/pnas.0937239100, 156340, 12721370.
58. Cristovao AC, Choi DH, Baltazar G, Beal MF, Kim YS. The role of NADPH oxidase 1-derived reactive oxygen species in paraquat-mediated dopaminergic cell death. Antioxid Redox Signal 2009, 11:2105-2118. 10.1089/ars.2009.2459, 2935343, 19450058.
59. Qian L, Flood PM, Hong JS. Neuroinflammation is a key player in Parkinson's disease and a prime target for therapy. J Neural Transm 2010, 117:971-979. 10.1007/s00702-010-0428-1, 20571837.
60. Tansey MG, Goldberg MS. Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol Dis 2010, 37:510-518. 10.1016/j.nbd.2009.11.004, 2823829, 19913097.
61. Lee SB, Bae IH, Bae YS, Um HD. Link between mitochondria and NADPH oxidase 1 isozyme for the sustained production of reactive oxygen species and cell death. J Biol Chem 2006, 281:36228-36235. 10.1074/jbc.M606702200, 17015444.
62. Ago T, Kuroda J, Pain J, Fu C, Li H, Sadoshima J. Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res 2010, 106:1253-1264. 10.1161/CIRCRESAHA.109.213116, 2855780, 20185797.
63. Block K, Gorin Y, Abboud HE. Subcellular localization of Nox4 and regulation in diabetes. Proc Natl Acad Sci USA 2009, 106:14385-14390. 10.1073/pnas.0906805106, 2732863, 19706525.
64. Abramov AY, Scorziello A, Duchen MR. Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J Neurosci 2007, 27:1129-1138. 10.1523/JNEUROSCI.4468-06.2007, 17267568.
65. Desouki MM, Kulawiec M, Bansal S, Das GM, Singh KK. Cross talk between mitochondria and superoxide generating NADPH oxidase in breast and ovarian tumors. Cancer Biol Ther 2005, 4:1367-1373. 10.4161/cbt.4.12.2233, 16294028.
66. Silva J, Pastorello M, Arzola J, Zavala LE, De JS, Varela M, et al. AT receptor and NAD(P)H oxidase mediate angiotensin II-stimulated antioxidant enzymes and mitogen-activated protein kinase activity in the rat hypothalamus. J Renin Angiotensin Aldosterone Syst 2010, 11:234-242. 10.1177/1470320310376987, 20807796.
67. Correia SC, Carvalho C, Cardoso S, Santos RX, Santos MS, Oliveira CR, et al. Mitochondrial preconditioning: a potential neuroprotective strategy. Front Aging Neurosci 2010, 2.
68. Cantu D, Schaack J, Patel M. Oxidative inactivation of mitochondrial aconitase results in iron and H2O2-mediated neurotoxicity in rat primary mesencephalic cultures. PLoS One 2009, 4:e7095. 10.1371/journal.pone.0007095, 2738973, 19763183.
69. Cantu D, Fulton RE, Drechsel DA, Patel M. Mitochondrial aconitase knockdown attenuates paraquat-induced dopaminergic cell death via decreased cellular metabolism and release of iron and H(2) O(2). J Neurochem 2011, 118:79-92. 10.1111/j.1471-4159.2011.07290.x, 21517855.
70. Abramov AY, Canevari L, Duchen MR. Beta-amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J Neurosci 2004, 24:565-575. 10.1523/JNEUROSCI.4042-03.2004, 14724257.
71. Wang XJ, Ye M, Zhang YH, Chen SD. CD200-CD200R regulation of microglia activation in the pathogenesis of Parkinson's disease. J Neuroimmune Pharmacol 2007, 2:259-264. 10.1007/s11481-007-9075-1, 18040859.
72. Wang XJ, Zhang S, Yan ZQ, Zhao YX, Zhou HY, Wang Y, et al. Impaired CD200-CD200R-mediated microglia silencing enhances midbrain dopaminergic neurodegeneration: Roles of aging, superoxide, NADPH oxidase, and p38 MAPK. Free Radic Biol Med 2011, 50:1094-1106. 10.1016/j.freeradbiomed.2011.01.032, 21295135.
73. Walker DG, Dalsing-Hernandez JE, Campbell NA, Lue LF. Decreased expression of CD200 and CD200 receptor in Alzheimer's disease: a potential mechanism leading to chronic inflammation. Exp Neurol 2009, 215:5-19. 10.1016/j.expneurol.2008.09.003, 2765462, 18938162.
74. Li J, Baud O, Vartanian T, Volpe JJ, Rosenberg PA. Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc Natl Acad Sci USA 2005, 102:9936-9941. 10.1073/pnas.0502552102, 1174990, 15998743.
75. Park SU, Ferrer JV, Javitch JA, Kuhn DM. Peroxynitrite inactivates the human dopamine transporter by modification of cysteine 342: potential mechanism of neurotoxicity in dopamine neurons. J Neurosci 2002, 22:4399-4405.