MPTP produces differential oxidative stress and antioxidative responses in the nigrostriatal and mesolimbic dopaminergic pathways

Free Radical Biology and Medicine

Volumn 24, Issue 1, 1998, Pages 76-84

  Hung, Hui Chuan ^a   Lee, Eminy H Y ^a  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

Catalase; Glutathione; Glutathione peroxidase; Lipid peroxidation; MPTP; Superoxide dismutase

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; MANGANESE SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; LIPID PEROXIDATION; MALE; MESOLIMBIC DOPAMINERGIC SYSTEM; MOUSE; NEUROTOXICITY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEUS ACCUMBENS; OXIDATIVE STRESS; PRIORITY JOURNAL; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

ANIMALS; ANTIOXIDANTS; BRAIN; CATALASE; CORPUS STRIATUM; DOPAMINE; DOPAMINE AGENTS; GLUTATHIONE; GLUTATHIONE PEROXIDASE; LIMBIC SYSTEM; LIPID PEROXIDATION; MALE; MICE; MICE, INBRED BALB C; MPTP POISONING; SUBSTANTIA NIGRA; SUPEROXIDE DISMUTASE;

ANIMALIA;

EID: 0031983381     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(97)00206-2     Document Type: Article

References (71)

1. Davis G. C., Williams A. C., Markey S. P., Elbert M. H., Caine E. D., Reichert C. M., Kopin I. J. Chronic parkinsonism secondary to intravenous injection of meperidine analogues. Psychiatr. Res. 1:1979;249-254.
2. Burns R. S., Chiueh C. C., Markey S. P., Elbert M. H., Jacobowitz D., Kopin I. J. A primate model of parkinsonism: Selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc. Natl. Acad. Sci. USA. 80:1983;4546-4550.
3. Heikkila R. E., Hess A., Duvoisin R. C. Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mice. Science. 224:1984;467-469.
4. Riachi, N. J.; J. C.; Harik, S. I. Entry of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine into the rat brain. J. Pharmacol. Exp. Ther. 249:744-748; 1989.
5. Chiba K., Trevor A. J., Castagnoli N. Jr. Metabolism of the neurotoxic tertiary amine, MPTP, by brain monoamine oxidase. Biochem. Biophys. Res. Commun. 120:1984;574-578.
6. Javitch J. A., D'Amato R. J., Strittmatter S. M., Snyder S. H. Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: Uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity. Proc. Natl. Acad. Sci. USA. 82:1985;2173-2177.
7. Singer T. P., Castagnoli N., Ramsay R. R., Trevor A. J. Biochemical events in the development of parkinsonism induced by MPTP. J. Neurochem. 49:1987;1-8.
8. Nicklas W. J., Vyas I., Heikkila R. E. Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenylpyridinium, a metabolite of the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Life Sci. 36:1985;2503-2508.
9. Chan P., De Lanney L. E., Irwin I., Langston J. W., Di Monte D. Rapid ATP loss caused by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mouse. J. Neurochem. 57:1991;348-351.
10. 2+ efflux. Biochem. Biophys. Acta. 1035:1990;300-305.
11. +. Free Radic. Biol. Med. 13:1992;581-583.
12. Zang L. Y., Misra H. P. Generation of reactive oxygen species during the monoamine oxidase-catalyzed oxidation of the neurotoxicant, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J. Biol. Chem. 268:1993;16504-16512.
13. +) induces NADH-dependent superoxide formation and enhances NADH-dependent lipid peroxidation in bovine heart submitochondrial particles. Biochem. Biophys. Res. Commun. 170:1990;1049-1055.
14. + induced oxygen radical formation with mitochondrial enzymes. Free Radic. Biol. Med. 15:1993;181-186.
15. Zhang Y., Marcillat O., Giulivi C., Ernster L., Davies K. J. The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 265:1990;16330-16336.
16. Cleeter M. W., Cooper J. M., Schapira A. H. Irreversible inhibition of mitochondrial complex I by 1-methyl-4-phenylpyridinium: evidence for free radical involvement. J. Neurochem. 58:1992;786-789.
17. Moore R., Bloom F. Central catecholamine neuron systems: Anatomy and physiology of the dopamine systems. Annu. Rev. Neurosci. 1:1978;129-169.
18. Uhi G. R., Hedreen J. D., Price D. L. Parkinson's disease: Loss of neurons from the ventral tegmental area contralateral to therapeutic surgical lesions. Neurology. 35:1985;1215-1218.
19. Hirsch E., Graybiel A. M., Agid Y. A. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature. 334:1988;345-348.
20. German D. C., Dubach M., Askari S., Speciale S. G., Bowden D. M. 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonian syndrome in Macaca Fascicularis: Which midbrain dopaminergic neurons are lost? Neuroscience. 24:1988;161-174.
21. Waters C. M., Hunt S. P., Jenner P., Marsden C. D. An immunohistochemical study of the acute and long-term effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in the marmoset. Neuroscience. 23:1987;1025-1039.
22. German D. C., Manaye K., Smith W. K., Woodward D. J., Saper C. B. Midbrain dopaminergic cell loss in Parkinson's disease: Computer visualization. Ann. Neurol. 26:1989;507-514.
23. Jacobowitz D. M., Burns R. S., Chiueh C. C., Irwin J. K. N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) causes destruction of the nigrostriatal but not the mesolimbic dopamine system in the monkey. Psychopharmacol. Bull. 20:1984;416-423.
24. Sundstrom E., Fredriksson A., Archer T. Chronic neurochemical and behavioral changes in MPTP-lesioned C57BL/6 mice: A model for Parkinson's disease. Brain Res. 528:1990;181-188.
25. + in the nigrostriatal and mesolimbic dopaminergic pathways. Neurosci. Lett. 196:1995;93-96.
26. + toxicity: Role of BDNF gene expression. Mol. Brain Res. 41:1996;16-26.
27. Reiter R. J. Oxidative processes and antioxidative defense mechanisms in the aging brain. FASEB J. 9:1995;526-533.
28. Winkler B. S., Orsell S. M., Rex T. S. The redox couple between glutathione and ascorbic acid: A chemical and physiological perspective. Free Radic. Biol. Med. 17:1994;333-349.
29. Halliwell B. Oxygen radicals as key mediators in neurological disease: fact or fiction? Ann. Neurol. 32:1992;S10-S15.
30. Niki E., Noguchi N., Gotoh N. Dynamics of lipid peroxidation and its inhibition by antioxidants. Biochem. Soc. Trans. 21:1993;313-317.
31. Esterbauer H., Cheeseman K. H. Determination of aldehydic lipid peroxidation products: Malonaldehyde and 4-hydroxynonenal. Methods Enzymol. 186:1990;407-438.
32. Marzatico F., Cafe C., Taborelli M., Benzi G. Experimental Parkinson's disease in monkey. Effect of Ergot alkaloid derivative on lipid peroxidation in different brain areas. Neurochem. Res. 18:1993;1101-1106.
33. Corsini G. U., Pintus S., Chiueh C. C., Weiss J. F., Kopin I. J. 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) neurotoxicity in mice is enhanced by pretreatment with diethyldithiocarbamate. Eur. J. Pharmacol. 119:1985;127-128.
34. Adams J. D., Odunze I. N., Sevanian A. Induction by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine of lipid peroxidation in vivo in vitamin E deficient mice. Biochem. Pharmacol. 39:1989;R5-R8.
35. + toxicity in nigral dopaminergic neurons. Neuroreport. 7:1996;921-923.
36. Anderson M. E. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol. 113:1985;548-555.
37. Aebi H. Catalase in vitro. Methods Enzymol. 105:1984;121-126.
38. Flohe L., Gunzler W. A. Assays of glutathione peroxidase. Methods Enzymol. 105:1984;114-121.
39. Misra H. P., 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.
40. Fridovich I. Superoxide dismutase. J. Biol. Chem. 264:1989;7761-7764.
41. Weisiger R. A., Fridovich I. Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J. Biol. Chem. 248:1973;4793-4796.
42. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. Current protocol. Analysis of proteins. 1991;10.6-10.8 John Wiley & Sons, Inc, New york.
43. Cappelletti G., Camatini M., Brambilla E., Maci R. N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) induces cytoskeletal alterations on "Swiss 3T3′" mouse fibroblasts. Neurosci. Lett. 129:1991;149-152.
44. Urani C., Brambilla E., Santagostino A., Camatini M. 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) affects the actin cytoskeleton and calcium level of Swiss 3T3 mouse fibroblasts. Toxicology. 91:1994;117-126.
45. Bradford M. M. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
46. Dexter D. T., Carter C. J., Wells F. R., Javoy-Agid F., Agid Y., Lees A., Jenner P., Marsden C. D. Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J. Neurochem. 52:1989;381-389.
47. Perry T. L., Godin D. V., Hansen S. Parkinson's disease: A disorder due to nigral glutathione deficiency? Neurosci. Lett. 33:1983;305-310.
48. Riederer P., Sofic E., Rausch W. D., Schmidt B., Reynolds G. P., Jellinger K., Youdim M. B. Transition metals, ferritin, glutathione, and ascorbic acid in parkinsonian brains. J. Neurochem. 52:1989;515-520.
49. Saggu H., Cooksey J., Dexter D., Wells F. R., Lees A., Jenner P., Marsden C. D. A selective increase in particulate superoxide dismutase ctivity in parkinsonian substantia nigra. J. Neurochem. 53:1989;692-697.
50. + administration to mice. Pharmacol. Toxicol. 72:1993;364-368.
51. + in the rat. Neurosci. Lett. 118:1990;151-154.
52. Ferraro T. N., Golden G. T., De Mattei M., Hare T. A., Fariello R. G. Effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) on levels of glutathione in the extrapyramidal system of the mouse. Neuropharmacology. 25:1986;1071-1074.
53. Yong V. W., Perry T. L., Krisman A. A. Depletion of glutathione in brainstem of mice caused by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine is prevented by antioxidant pretreatment. Neurosci. Lett. 63:1986;56-60.
54. Raps S. P., Lai J. C. K., Hertz L., Cooper A. J. L. Glutathione is present in high concentrations in cultured astrocytes but not in cultured neurons. Brain Res. 493:1989;398-401.
55. Makar T. K., Nedergaard M., Preuss A., Gelbard A. S., Perumal A. S., Cooper A. J. Vitamin E, ascorbate, glutathione, glutathione disulfide, and enzymes of glutathione metabolism in cultures of chick astrocytes and neurons: evidence that astrocytes play an important role in antioxidative processes in the brain. J. Neurochem. 62:1994;45-53.
56. Shull S., Heintz N. H., Periasamy M., Manohar M., Janssen Y. M. W., Marsh J. P., Mossman B. T. Differential regulation of antioxidant enzymes in response to oxidants. J. Biol. Chem. 266:1991;24398-24403.
57. Mokuno K., Ohtani K., Suzumura A., Kiyosawa K., Hirose Y., Kawai K., Kato K. Induction of manganese superoxide dismutase by cytokines and lipopolysaccharide in cultured mouse astrocytes. J. Neurochem. 63:1994;612-616.
58. Przedborski S., Lostic V., Jackson-Lewis V., Naini A. B., Simonetti S., Fahn S., Carlson E., Epstein C. J., Cadet J. L. Transgenic mice with increased Cu/Zn-superoxide dismutase activity are resistant to N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity. J. Neurosci. 12:1992;1658-1667.
59. Markey B. A., Phan S. H., Varani J., Ryan U. S., Ward P. A. Inhibition of cytotoxicity by intracellular superoxide dismutase supplementation. Free Radic. Biol. Med. 9:1990;307-314.
60. Matsuyama T., Michishita H., Nakamura H., Tsuchiyama M., Shimizu S., Watanabe K., Sugita M. Indution of copper-zinc superoxide dismutase in gerbil hippocampus after ischemia. J. Cereb. Blood Flow Metab. 13:1993;135-144.
61. Zhang P., Damier P., Hirsch E. C., Agid Y., Ceballos-Picot I., Sinet P. M., Nicole A., Laurent M., Javoy-Agid F. Preferential expression of superoxide dismutase messenger RNA in melanized neurons in human mesencephalon. Neuroscience. 55:1993;167-175.
62. Halliwell B., Gutteridge J. M. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem. J. 219:1984;11-14.
63. Huang T. T., Carlson E. J., Leadon S. A., Epstein C. J. Relationship of resistance to oxygen free radicals to CuZn-superoxide dismutase activity in transgenic, transfected, and trisomic cells. FASEB J. 6:1992;903-910.
64. Brooksbank B. W., Balazs R. Superoxide dismutase, glutathione peroxidase and lipoperoxidation in Down's syndrome fetal brain. Dev. Brain Res. 16:1984;37-44.
65. Hayn M., Kremser K., Singewald N., Cairns N., Nemethova M., Lubec B., Lubec G. Evidence against the involvement of reactive oxygen species in the pathogenesis of neuronal death in Down's syndrome and Alzheimer's disease. Life Sci. 59:1996;537-544.
66. Epstein C. J., Avraham K. B., Lovett M., Smith S., Elroy-Stein O., Rotman G., Bry C., Groner Y. Transgenic mice with increased Cu/Zn-superoxide dismutase activity: Animal model of dosage defects in Down syndrome. Proc. Natl. Acad. Sci. USA. 84:1987;8044-8048.
67. Bonnes-Taourel D., Guerin M. C., Torreilles J., Ceballos-Picot I., De Paulet A. C. 4-Hydroxynonenal content lower in brains of 25 month old transgenic mice carrying the human CuZn superoxide dismutase gene than in brains of their nontransgenic littermates. J. Lipid Med. 8:1993;111-120.
68. Ceballos-Picot I., Nicole A., Briand P., Grimber G., Delacourte A., Defossez A., Javoy-Agid F., Lafon M., Blouin J. L., Sinet P. M. Neuronal-specific expression of human copper-zinc superoxide dismutase gene in transgenic mice: Animal model of gene dosage effects in Down' s syndrome. Brain Res. 552:1991;198-214.
69. Elroy-Stein O., Bernstein Y., Groner Y. Overproduction of human Cu/Zn-superoxide dismutase in transfected cells: Extenuation of paraquat-mediated cytotoxicity and enhancement of lipid peroxidation. EMBO J. 5:1986;615-622.
70. Temlett J. A., Landsberg J. P., Watt F., Grime G. W. Increased iron in the substantia nigra compacta of the MPTP-lesioned hemiparkinsonian African green monkey: Evidence from proton microprobe elemental microanalysis. J. Neurochem. 62:1994;134-146.
71. Sutton G. C., Winterbourn C. C. On the participation of higher oxidation states of iron and copper in Fenton reactions. Free Radic. Biol. Med. 6:1989;53-60.