Dopaminergic neuron-specific oxidative stress caused by dopamine itself

Acta Medica Okayama

Volumn 62, Issue 3, 2008, Pages

  Miyazaki, Ikuko ^a   Asanuma, Masato ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

Dopamine quinone; L DOPA; Methamphetamine; Parkinson's disease; Quinoprotein

Indexed keywords

DOPAMINE; DOPAMINE QUINONE; DRUG DERIVATIVE; FREE RADICAL;

ANIMAL; DISEASE MODEL; HUMAN; METABOLISM; NERVE CELL; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; FREE RADICALS; HUMANS; NEURONS; OXIDATIVE STRESS; PARKINSON DISEASE;

EID: 50949117770     PISSN: 0386300X     EISSN: 0386300X     Source Type: Journal    
DOI: None     Document Type: Review

References (99)

1. Hotchkiss AJ and Gibb JW: Long-term effects of multiple doses of methamphetamine on tryptophan hydroxylase and tyrosine hydroxylase activity in rat brain. J Pharmacol Exp Ther (1980) 214: 257-262.
2. Ricaurte GA, Schuster CR and Seiden LS: Long-term effects of repeated methylamphetamine administration on dopamine and serotonin neurons in the rat brain: a regional study. Brain Res (1980) 193: 153-163.
3. Wagner GC, Ricaurte GA, Seiden LS, Schuster CR, Miller RJ and Westley J: Long-lasting depletions of striatal dopamine and loss of dopamine uptake sites following repeated administration of methamphetamine. Brain Res (1980) 181: 151-160.
4. Axt KJ, Commins DL, Vosmer G and Seiden LS: alpha-Methyl-p-tyrosine pretreatment partially prevents methamphetamine-induced endogenous neurotoxin formation. Brain Res (1990) 515: 269-276.
5. Cadet JL and Brannock C: Free radicals and the pathobiology of brain dopamine systems. Neurochem Int (1998) 32: 117-131.
6. Cadet JL, Jayanthi S and Deng X: Speed kills: cellular and molecular bases of methamphetamine-induced nerve terminal degeneration and neuronal apoptosis. FASEB J (2003) 17: 1775-1788.
7. Cubells JF, Rayport S, Rajendran G and Sulzer D: Methamphetamine neurotoxicity involves vacuolation of endocytic organelles and dopamine-dependent intracellular oxidative stress. J Neurosci (1994) 14: 2260-2271.
8. Fumagalli F, Gainetdinov RR, Wang YM, Valenzano KJ, Miller GW and Caron MG: Increased methamphetamine neurotoxicity in heterozygous vesicular monoamine transporter 2 knock-out mice. J Neurosci (1999) 19: 2424-2431.
9. LaVoie MJ and Hastings TG: Dopamine quinone formation and protein modification associated with the striatal neurotoxicity of methamphetamine: evidence against a role for extracellular dopamine. J Neurosci (1999) 19: 1484-1491.
10. Liu Y and Edwards RH: The role of vesicular transport proteins in synaptic transmission and neural degeneration. Annu Rev Neurosci (1997) 20: 125-156.
11. Marek GJ, Vosmer G and Seiden LS: Dopamine uptake inhibitors block long-term neurotoxic effects of methamphetamine upon dopaminergic neurons. Brain Res (1990) 513: 274-279.
12. Seiden LS and Vosmer G: Formation of 6-hydroxydopamine in caudate nucleus of the rat brain after a single large dose of methylamphetamine. Pharmacol Biochem Behav (1984) 21: 29-31.
13. Uhl GR: Hypothesis: the role of dopaminergic transporters in selective vulnerability of cells in Parkinson's disease. Ann Neurol (1998) 43: 555-560.
14. Wrona MZ, Yang Z, Zhang F and Dryhurst G: Potential new insights into the molecular mechanisms of methamphetamine-induced neurodegeneration. NIDA Res Monogr (1997) 173: 146-174.
15. Yuan J, Callahan BT, McCann UD and Ricaurte GA: Evidence against an essential role of endogenous brain dopamine in methamphetamine-induced dopaminergic neurotoxicity. J Neurochem (2001) 77: 1338-1347.
16. Ogawa N: Factors affecting levodopa effects in Parkinson's disease. Acta Med Okayama (2000) 54: 95-101.
17. Ahlskog JE and Muenter MD: Frequency of levodopa-related dyskinesias and motor fluctuations as estimated from the cumulative literature. Mov Disord (2001) 16: 448-458.
18. Fornai F, Lenzi P, Gesi M, Ferrucci M, Lazzeri G, Capobianco L, de Blasi A, Battaglia G, Nicoletti F, Ruggieri S and Paparelli A: Similarities between methamphetamine toxicity and proteasome inhibition. Ann NY Acad Sci (2004) 1025: 162-170.
19. Asanuma M, Miyazaki I, Higashi Y, Tsuji T and Ogawa N: Specific gene expression and possible involvement of inflammation in methamphetamine-induced neurotoxicity. Ann NY Acad Sci (2004) 1025: 69-75.
20. Dabbeni-Sala F, Di Santo S, Franceschini D, Skaper SD and Giusti P: Melatonin protects against 6-OHDA-induced neurotoxicity in rats: a role for mitochondrial complex I activity. FASEB J (2001) 15: 164-170.
21. Glinka YY and Youdim MB: Inhibition of mitochondrial complexes I and IV by 6-hydroxydopamine. Eur J Pharmacol (1995) 292: 329-332.
22. Glinka Y, Gassen M and Youdim MB: Mechanism of 6-hydroxydopamine neurotoxicity. J Neural Transm Suppl (1997) 50: 55-66.
23. Hoglinger GU, Carrard G, Michel PP, Medja F, Lombes A, Ruberg M, Friguet B and Hirsch EC: Dysfunction of mitochondrial complex I and the proteasome: interactions between two biochemical deficits in a cellular model of Parkinson's disease. J Neurochem (2003) 86: 1297-1307.
24. Asanuma M, Miyazaki I, Diaz-Corrales FJ and Ogawa N: Quinone formation as dopaminergic neuron-specific oxidative stress in pathogenesis of sporadic Parkinson's disease and neurotoxin-induced parkinsonism. Acta Med Okayama (2004) 58: 221-233.
25. Castano A, Herrera AJ, Cano J and Machado A: Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J Neurochem (1998) 70: 1584-1592.
26. Gao HM, Jiang J, Wilson B, Zhang W, Hong JS and 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.
27. Elkon H, Melamed E and Offen D: 6-Hydroxydopamine increases ubiquitin conjugates and protein degradation: implications for the pathogenesis of Parkinson's disease. Cell Mol Neurobiol (2001) 21: 771-781.
28. Sulzer D, Bogulavsky J, Larsen KE, Behr G, Karatekin E, Kleinman MH, Turro N, Krantz D, Edwards RH, Greene LA and Zecca L: Neuromelanin biosynthesis is driven by excess cytosolic catecholamines not accumulated by synaptic vesicles. Proc Natl Acad Sci USA (2000) 97: 11869-11874.
29. Graham DG: Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol Pharmacol (1978) 14: 633-643.
30. Spencer JP, Jenner A, Butler J, Aruoma OI, Dexter DT, Jenner P and Halliwell B: Evaluation of the pro-oxidant and antioxidant actions of L-DOPA and dopamine in vitro: implications for Parkinson's disease. Free Radic Res (1996) 24: 95-105.
31. Kostrzewa RM, Kostrzewa JP and Brus R: Dopaminergic denervation enhances susceptibility to hydroxyl radicals in rat neostriatum. Amino Acids (2000) 19: 183-199.
32. Colado MI, O'Shea E, Granados R, Esteban B, Martin AB and Green AR: Studies on the role of dopamine in the degeneration of 5-HT nerve endings in the brain of Dark Agouti rats following 3,4-methylenedioxymethamphetamine (MDMA or ecstasy) administration. Br J Pharmacol (1999) 126: 911-924.
33. Olanow CW and Cohen G: The pathogenesis of Parkinson's disease; in The Scientific Basis for the Treatment of Parkinson's Disease, Olanow CW and Lieberman AN eds, The Parthenon Publishing Group, Lanes, U.K. (1992) pp. 59-76.
34. Ogawa N, Edamatsu R, Mizukawa K, Asanuma M, Kohno M and Mori A: Degeneration of dopaminergic neurons and free radicals. Possible participation of levodopa. Adv Neurol (1993) 60: 242-250.
35. Asanuma M, Miyazaki I and Ogawa N: Dopamine- or L-DOPA-induced neurotoxicity: the role of dopamine quinone formation and tyrosinase in a model of Parkinson's disease. Neurotox Res (2003) 5: 165-176.
36. Choi HJ, Kim SW, Lee SY and Hwang O: Dopamine-dependent cytotoxicity of tetrahydrobiopterin: a possible mechanism for selective neurodegeneration in Parkinson's disease. J Neurochem (2003) 86: 143-152.
37. Choi HJ, Lee SY, Cho Y and Hwang O: Inhibition of vesicular monoamine transporter enhances vulnerability of dopaminergic cells: relevance to Parkinson's disease. Neurochem Int (2005) 46: 329-335.
38. LaVoie MJ, Ostaszewski BL, Weihofen A, Schlossmacher MG and Selkoe DJ: Dopamine covalently modifies and functionally inactivates parkin. Nat Med (2005) 11: 1214-1221.
39. Tse DC, McCreery RL and Adams RN: Potential oxidative pathways of brain catecholamines. J Med Chem (1976) 19: 37-40.
40. Hastings TG: Enzymatic oxidation of dopamine: the role of prostaglandin H synthase. J Neurochem (1995) 64: 919-924.
41. Korytowski W, Sarna T, Kalyanaraman B and Sealy RC: Tyrosinase-catalyzed oxidation of dopa and related catechol(amine)s: a kinetic electron spin resonance investigation using spin-stabilization and spin label oximetry. Biochim Biophys Acta (1987) 924: 383-392.
42. Foppoli C, Coccia R, Cini C and Rosei MA: Catecholamines oxidation by xanthine oxidase. Biochim Biophys Acta (1997) 1334: 200-206.
43. Rosei MA, Blarzino C, Foppoli C, Mosca L and Coccia R: Lipoxygenase-catalyzed oxidation of catecholamines. Biochem Biophys Res Commun (1994) 200: 344-350.
44. Fornstedt B, Rosengren E and Carlsson A: Occurrence and distribution of 5-S-cysteinyl derivatives of dopamine, dopa and dopac in the brains of eight mammalian species. Neuropharmacology (1986) 25: 451-454.
45. Ito S and Fujita K: Conjugation of dopa and 5-S-cysteinyldopa with cysteine mediated by superoxide radical. Biochem Pharmacol (1982) 31: 2887-2889.
46. Lai CT and Yu PH: Dopamine- and L-beta-3,4-dihydroxyphenylalanine hydrochloride (L-Dopa)-induced cytotoxicity towards catecholaminergic neuroblastoma SH-SY5Y cells. Effects of oxidative stress and antioxidative factors. Biochem Pharmacol (1997) 53: 363-372.
47. LaVoie MJ and Hastings TG: Peroxynitrite-and nitrite-induced oxidation of dopamine: implications for nitric oxide in dopaminergic cell loss. J Neurochem (1999) 73: 2546-2554.
48. Pardo B, Mena MA, Casarejos MJ, Paino CL and De Yébenes JG: Toxic effects of L-dopa on mesencephalic cell cultures: protection with antioxidants. Brain Res (1995) 682: 133-143.
49. Xu Y, Stokes AH, Roskoski R Jr and Vrana KE: Dopamine, in the presence of tyrosinase, covalently modifies and inactivates tyrosine hydroxylase. J Neurosci Res (1998) 54: 691-697.
50. Kuhn DM, Arthur RE Jr, Thomas DM and Elferink LA: Tyrosine hydroxylase is inactivated by catechol-quinones and converted to a redox-cycling quinoprotein: possible relevance to Parkinson's disease. J Neurochem (1999) 73: 1309-1317.
51. Whitehead RE, Ferrer JV, Javitch JA and Justice JB: Reaction of oxidized dopamine with endogenous cysteine residues in the human dopamine transporter. J Neurochem (2001) 76: 1242-1251.
52. Machida Y, Chiba T, Takayanagi A, Tanaka Y, Asanuma M, Ogawa N, Koyama A, Iwatsubo T, Ito S, Jansen PH, Shimizu N, Tanaka K, Mizuno Y and Hattori N: Common anti-apoptotic roles of parkin and alpha-synuclein in human dopaminergic cells. Biochem Biophys Res Commun (2005) 332: 233-240.
53. Conway KA, Rochet JC, Bieganski RM and Lansbury PT Jr: Kinetic stabilization of the α-synuclein protofibril by a dopamine-α -synuclein adduct. Science (2001) 294: 1346-1349.
54. Goldberg MS, Lansbury PT Jr and Helfand SL: Is there a cause-and-effect relationship between alpha-synuclein fibrillization and Parkinson's disease? Nat Cell Biol (2000) 2: E115-E119.
55. Conway KA, Lee SJ, Rochet JC, Ding TT, Williamson RE and Lansbury PT Jr: Acceleration of oligomerization, not fibrillization, is a shared property of both α-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc Natl Acad Sci USA (2000) 97: 571-576.
56. Volles MJ, Lee SJ, Rochet JC, Shtilerman MD, Ding TT, Kessler JC and Lansbury PT Jr: Vesicle permeabilization by protofibrillar alpha-synuclein: implications for the pathogenesis and treatment of Parkinson's disease. Biochemistry (2001) 40: 7812-7819.
57. Kuhn DM and Arthur R Jr: Dopamine inactivates tryptophan hydroxylase and forms a redox-cycling quinoprotein: possible endogenous toxin to serotonin neurons. J Neurosci (1998) 18: 7111-7117.
58. Berman SB and Hastings TG: Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: implications for Parkinson's disease. J Neurochem (1999) 73: 1127-1137.
59. Li H and Dryhurst G: Irreversible inhibition of mitochondrial complex I by 7-(2-aminoethyl)- 3,4-dihydro-5-hydroxy-2H-1,4-benzothiazine-3-carboxylic acid (DHBT-1): a putative nigral endotoxin of relevance to Parkinson's disease. J Neurochem (1997) 69: 1530-1541.
60. Kuhn DM, Francescutti-Verbeem DM and Thomas DM: Dopamine quinones activate microglia and induce a neurotoxic gene expression profile: relationship to methamphetamine-induced nerve ending damage. Ann NY Acad Sci (2006) 1074: 31-41.
61. Yoshimoto Y, Nakaso K and Nakashima K: L-dopa and dopamine enhance the formation of aggregates under proteasome inhibition in PC12 cells. FEBS Lett (2005) 579: 1197-1202.
62. Fornai F, Lenzi P, Gesi M, Ferrucci M, Lazzeri G, Busceti CL, Ruffoli R, Soldani P, Ruggieri S, Alessandri MG and Paparelli A: Fine structure and biochemical mechanisms underlying nigrostriatal inclusions and cell death after proteasome inhibition. J Neurosci (2003) 23: 8955-8966.
63. Keller JN, Huang FF, Dimayuga ER and Maragos WF: Dopamine induces proteasome inhibition in neural PC12 cell line. Free Radic Biol Med (2000) 29: 1037-1042.
64. Zafar KS, Siegel D and Ross D: A potential role for cyclized quinones derived from dopamine, DOPA, and 3,4-dihydroxyphenylacetic acid in proteasomal inhibition. Mol Pharmacol (2006) 70: 1079-1086.
65. Kita T, Wagner GC and Nakashima T: Current research on methamphetamine-induced neurotoxicity: animal models of monoamine disruption. J Pharmacol Sci (2003) 92: 178-195.
66. Miyazaki I, Asanuma M, Diaz-Corrales FJ, Fukuda M, Kitaichi K, Miyoshi K and Ogawa N: Methamphetamine-induced dopaminergic neurotoxicity is regulated by quinone formation-related molecules. FASEB J (2006) 20: 571-573.
67. Kostrzewa RM, Kostrzewa JP and Brus R: Neuroprotective and neurotoxic roles of levodopa (L-DOPA) in neurodegenerative disorders relating to Parkinson's disease. Amino Acids (2002) 23: 57-63.
68. Basma AN, Morris EJ, Nicklas WJ and Geller HM: L-dopa cytotoxicity to PC12 cells in culture is via its autoxidation. J Neurochem (1995) 64: 825-832.
69. Hastings TG, Lewis DA and Zigmond MJ : Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc Natl Acad Sci USA (1996) 93: 1956-1961.
70. Walkinshaw G and Waters CM: Induction of apoptosis in catecholaminergic PC12 cells by L-DOPA. Implications for the treatment of Parkinson's disease. J Clin Invest (1995) 95: 2458-2464.
71. Haque ME, Asanuma M, Higashi Y, Miyazaki I, Tanaka K and Ogawa N: Apoptosis-inducing neurotoxicity of dopamine and its metabolites via reactive quinone generation in neuroblastoma cells. Biochim Biophys Acta (2003) 1619: 39-52.
72. Ogawa N, Asanuma M, Kondo Y, Kawada Y, Yamamoto M and Mori A: Differential effects of chronic L-dopa treatment on lipid peroxidation in the mouse brain with or without pretreatment with 6-hydroxydopamine. Neurosci Lett (1994) 171: 55-58.
73. Olanow CW and Jankovic J: Neuroprotective therapy in Parkinson's disease and motor complications: a search for a pathogenesis-targeted, disease-modifying strategy. Mov Disord (2005) 20: S3-10.
74. Fahn S, Oakes D, Shoulson I, Kieburtz K, Rudolph A, Lang A, Olanow CW, Tanner C and Marek K: Levodopa and the progression of Parkinson's disease. N Engl J Med (2004) 351: 2498-2508.
75. Asanuma M, Miyazaki I, Diaz-Corrales FJ, Shimizu M, Tanaka K and Ogawa N: Pramipexole has ameliorating effects on levodopa-induced abnormal dopamine turnover in parkinsonian striatum and quenching effects on dopamine-semiquinone generated in vitro. Neurol Res (2005) 27: 533-539.
76. Ogawa N, Tanaka K and Asanuma M: Bromocriptine markedly suppresses levodopa-induced abnormal increase of dopamine turnover in the parkinsonian striatum. Neurochem Res (2000) 25: 755-758.
77. Miyazaki I, Asanuma M, Diaz-Corrales FJ, Miyoshi K and Ogawa N: Dopamine agonist pergolide prevents levodopa-induced quinoprotein formation in parkinsonian striatum and shows quenching effects on dopamine-semiquinone generated in vitro. Clin Neuropharmacol (2005) 28: 155-160.
78. Cadenas E, Mira D, Brunmark A, Lind C, Segura-Aguilar J and Ernster L: Effect of superoxide dismutase on the autoxidation of various hydroquinones-a possible role of superoxide dismutase as a superoxide: semiquinone oxidoreductase. Free Radic Biol Med (1988) 5: 71-79.
79. Offen D, Ziv I, Sternin H, Melamed E and Hochman A: Prevention of dopamine-induced cell death by thiol antioxidants: possible implications for treatment of Parkinson's disease. Exp Neurol (1996) 141: 32-39.
80. Hara H, Ohta M, Ohta K, Kuno S and Adachi T: Increase of anti-oxidative potential by tert-butylhydroquinone protects against cell death associated with 6-hydroxydopamine-induced oxidative stress in neuroblastoma SH-SY5Y cells. Mol Brain Res (2003) 119: 125-131.
81. Munday R, Smith BL and Munday CM: Effects of butylated hydroxyanisole and dicoumarol on the toxicity of menadione to rats. Chem Biol Interact (1998) 108: 155-170.
82. Duffy S, So A and Murphy TH: Activation of endogenous antioxidant defenses in neuronal cells prevents free radical-mediated damage. J Neurochem (1998) 71: 69-77.
83. Mattammal MB, Strong R, Lakshmi VM, Chung HD and Stephenson AH: Prostaglandin H synthetase-mediated metabolism of dopamine: implication for Parkinson's disease. J Neurochem (1995) 64: 1645-1654.
84. Ferger B, Teismann P, Earl CD, Kuschinsky K and Oertel WH: Salicylate protects against MPTP-induced impairments in dopaminergic neurotransmission at the striatal and nigral level in mice. Naunyn Schmiedebergs Arch Pharmacol (1999) 360: 256-261.
85. Aubin N, Curet O, Deffois A and Carter C: Aspirin and salicylate protect against MPTP-induced dopamine depletion in mice. J Neurochem (1998) 71: 1635-1642.
86. Teismann P and Ferger B: Inhibition of the cyclooxygenase isoenzymes COX-1 and COX-2 provide neuroprotection in the MPTP-mouse model of Parkinson's disease. Synapse (2001) 39: 167-174.
87. Teismann P, Tieu K, Choi DK, Wu DC, Naini A, Hunot S, Vila M, Jackson-Lewis V and Przedborski S: Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc Natl Acad Sci USA (2003) 100: 5473-5478.
88. Asanuma M, Tsuji T, Miyazaki I, Miyoshi K and Ogawa N: Methamphetamine-induced neurotoxicity in mouse brain is attenuated by ketoprofen, a non-steroidal anti-inflammatory drug. Neurosci Lett (2003) 352: 13-16.
89. Asanuma M, Miyazaki I and Ogawa N: Neuroprotective effects of nonsteroidal anti-inflammatory drugs on neurodegenerative diseases. Curr Pharm Des (2004) 10: 695-700.
90. Higashi Y, Asanuma M, Miyazaki I and Ogawa N: Inhibition of tyrosinase reduces cell viability in catecholaminergic neuronal cells. J Neurochem (2000) 75: 1771-1774.
91. Penkowa M: Metallothioneins are multipurpose neuroprotectants during brain pathology. FEBS J (2006) 273: 1857-1870.
92. Xie T, Tong L, McCann UD, Yuan J, Becker KG, Mechan AO, Cheadle C, Donovan DM and Ricaurte GA: Identification and characterization of metallothionein-1 and -2 gene expression in the context of (+/-) 3,4-methylenedioxymethamphetamine-induced toxicity to brain dopaminergic neurons. J Neurosci (2004) 24: 7043-7050.
93. Aschner M: Metallothionein (MT) isoforms in the central nervous system (CNS): regional and cell-specific distribution and potential functions as an antioxidant. Neurotoxicology (1998) 19: 653-660.
94. Penkowa M, Carrasco J, Giralt M, Moos T and Hidalgo J: CNS wound healing is severely depressed in metallothionein I- and II-deficient mice. J Neurosci (1999) 19: 2535-2545.
95. Miura T, Muraoka S and Ogiso T: Antioxidant activity of metallothionein compared with reduced glutathione. Life Sci (1997) 60: PL 301-309.
96. Hussain S, Slikker W Jr and Ali SF: Role of metallothionein and other antioxidants in scavenging superoxide radicals and their possible role in neuroprotection. Neurochem Int (1996) 29: 145-152.
97. Ebadi M, Ramana Kumari MV, Hiramatsu M, Hao R, Pfeiffer RF and Rojas P: Metallothionein, neurotrophins and selegiline in providing neuroprotection in Parkinson's disease. Restor Neurol Neurosci (1998) 12: 103-111.
98. Sato M and Bremner I: Oxygen free radicals and metallothionein. Free Radic Biol Med (1993) 14: 325-337.
99. Miyazaki I, Asanuma M, Hozumi H, Miyoshi K and Sogawa N: Protective effects of metallothionein against dopamine quinone-induced dopaminergic neurotoxicity. FEBS Lett (2007) 581: 5003-5008.