L-DOPA does not enhance hydroxyl radical formation in the nigrostriatal dopamine system of rats with a unilateral 6-hydroxydopamine lesion

Journal of Neurochemistry

Volumn 74, Issue 3, 2000, Pages 1229-1240

  Camp, Dianne M ^a,c   Loeffler, David A ^a   Lewitt, Peter A ^a,b  

^a SINAI GRACE HOSPITAL   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WILLIAM BEAUMONT HOSPITAL   (United States)

Author keywords

Hydroxyl radicals; L DOPA; Microdialysis; Oxidative stress; Parkinson's disease; Salicylate trapping

Indexed keywords

2,3 DIHYDROXYBENZOIC ACID; HYDROXYL RADICAL; LEVODOPA; METHAMPHETAMINE; OXIDOPAMINE; OXYGEN RADICAL; SALICYLIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BRAIN REGION; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DOSE RESPONSE; IN VIVO STUDY; MALE; MICRODIALYSIS; NEUROTOXICITY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; TOXICOKINETICS;

ANIMALIA;

EID: 0033974549     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.741229.x     Document Type: Article

References (101)

1. Abercrombie E. D., Bonatz A. E., and Zigmond M. J. (1990) Effects of L-DOPA on extracellular dopamine in striatum of normal and 6-hydroxydopamine-treated rats. Brain Res. 525, 36-44.
2. Acworth I. N., Bogdanov M. B., McCabe D. R., and Beal M. F. (1999) Estimation of hydroxyl free radical levels in vivo based on liquid chromatography with electrochemical detection. Methods Enzymol. 300, 297-313.
3. Adams J. D. and Odunze I. N. (1991) Oxygen free radicals and Parkinson's disease. Free Radic. Biol. Med. 10, 161-169.
4. Agid Y. (1998) Levodopa: is toxicity a myth? Neurology 50, 858-863.
5. Alam Z. I., Jenner A., Daniel S. E., Lees A. J., Cairns N., Marsden C. D., Jenner P., and Halliwell B. (1997a) Oxidative DNA damage in the parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J. Neurochem. 69, 1196-1203.
6. Alam Z. I., Daniel S. E., Lees A. J., Marsden D. C., Jenner P., and Halliwell B. (1997b) A generalised increase in protein carbonyls in the brain in Parkinson's but not incidental Lewy body disease. J. Neurochem. 69, 1326-1329.
7. Althaus J. S., andrus P. K., Hall E. D., and Von Voigtlander P. F. (1995) Improvements in the salicylate trapping method for measurement of hydroxyl radical levels in the brain, in Central Nervous System Trauma Research Techniques (Ohnishi S. T. and Ohnishi T., eds), pp. 437-444. CRC Press, Boca Raton, Florida.
8. Basma A. N., Morris E. J., Nicklas W. J., and Geller H. M. (1995) L-DOPA cytotoxicity to PC12 cells in culture is via its autoxidation. J. Neurochem. 64, 825-832.
9. 3H-mazindol autoradiography. Neuroscience 43, 95-110.
10. Blunt S. B., Jenner P., and Marsden C. D. (1993) Suppressive effect of L-DOPA on dopamine cells remaining in the ventral tegmental area of rats previously exposed to the neurotoxin 6-hydroxydopamine. Mov. Disord. 8, 129-133.
11. Camp D. M., Browman K. E., and Robinson T. E. (1994) The effects of methamphetamine and cocaine on motor behavior and extracellular dopamine in the ventral striatum of Lewis versus Fischer 344 rats. Brain Res. 668, 180-193.
12. Camp D. M., Collins K. M., Loeffler D. A., and LeWitt P. A. (1997) Effect of L-DOPA on hydroxyl radical formation in the intact and dopamine-denervated striatum of the rat: a microdialysis study. Soc. Neurosci. Abstr. 23, 1370.
13. Cassarino D. S., Fall C. P., Smith T. S., and Bennett J. P. Jr. (1998) Pramipexole reduces reactive oxygen species production in vivo and in vitro and inhibits the mitochondrial permeability transition produced by the parkinsonian neurotoxin methylpyridinium ion. J. Neurochem. 71, 295-301.
14. Chiueh C. C., Huang S.-J., and Murphy D. L. (1992a) Enhanced hydroxyl radical generation by 2′-methyl analog of MPTP: suppression by clorgyline and deprenyl. Synapse 11, 346-348.
15. +. Free Radic. Biol. Med. 13, 581-583.
16. Cohen G. (1986) Monoamine oxidase, hydrogen peroxide, and Parkinson's disease. Adv. Neurol. 45, 119-125.
17. Cohen G. and Spina M. B. (1989) Deprenyl suppresses the oxidant stress associated with increased dopamine turnover. Ann. Neurol. 26, 689-690.
18. Connor J. R. and Benkovic S. A. (1992) Iron regulation in the brain: histochemical, biochemical, and molecular considerations. Ann. Neurol. 32 (Suppl), S51-S61.
19. Cooper J. M., Daniel S. E., Marsden C. D., and Schapira A. H. V. (1995) L-Dihydroxyphenylalanine and complex I deficiency in Parkinson's disease brain. Mov. Disord. 10, 295-297.
20. Dexter D. T., Carter C. J., Wells F. R., Javoy-Agid F., Agid Y., Lees A., Jenner P., and Marsden C. D. (1989) Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J. Neurochem. 52, 381-389.
21. Dexter D. T., Carayon A., Javoy-Agid F., Agid Y., Wells F. R., Daniel S. E., Lees A. J., Jenner P., and Marsden C. D. (1991) Alterations in the levels of iron, ferritin and other trace metals in Parkinson's disease and other neurodegenerative diseases affecting the basal ganglia. Brain 114, 1953-1975.
22. Dexter D. T., Holley A. E., Flitter W. D., Slater T. F., Wells F. R., Daniel S. E., Lees A. J., Jenner P., and Marsden C. D. (1994) Increased levels of lipid hydroperoxides in the parkinsonian substantia nigra: an HPLC and ESR study. Mov. Disord. 9, 92-97.
23. Fahn S. (1996) Is levodopa toxic? Neurology 47 (Suppl. 3), S184-S195.
24. Fahn S. and Cohen G. (1992) The oxidant stress hypothesis in Parkinson's disease: evidence supporting it. Ann. Neurol. 32, 804-812.
25. Fleckenstein A. E., Wilkins D. G., Gibb J. W., and Hanson G. R. (1997) Interaction between hyperthermia and oxygen radical formation in the 5-hydroxytryptaminergic response to a single methamphetamine administration. J. Pharmacol. Exp. Ther. 283, 281-285.
26. Floyd R. A. and Carney J. M. (1992) Free radical damage to protein and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann. Neurol. 32, 522-527.
27. Floyd R. A., Watson J. J. and Wong P. K. (1984) Sensitive assay of hydroxyl free radical formation utilizing high pressure liquid chromatography with electrochemical detection of phenol and salicylate hydroxylation products. J. Biochem. Biophys. Methods 10, 221-235.
28. Fumagalli F., Gainetdinov R. R., Valenzano K. J., and Caron M. G. (1998) Role of dopamine transporter in methamphetamine-induced neurotoxicity: evidence from mice lacking the transporter. J. Neurosci. 18, 4861-4869.
29. Giovanni A., Liang L. P., Hastings T. G., and Zigmond M. J. (1995) Estimating hydroxyl radical content in rat brain using systemic and intraventricular salicylate: impact of methamphetamine. J. Neurochem. 64, 1819-1825.
30. Globus M. Y.-T., Busto R., Lin B., Schnippering H., and Ginsberg M. D. (1995) Detection of free radical activity during transient global ischemia and recirculation: effects of intraischemic brain temperature modulation. J. Neurochem. 65, 1250-1256.
31. Graham D. G. (1978) Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol. Pharmacol. 14, 633-643.
32. Graham D. G., Tiffany S. M., Bell W. R. Jr., and Gutknecht W. F. (1978) Autoxidation versus covalent binding of quinones as the mechanism of toxicity of dopamine, 6-hydroxydopamine, and related compounds toward C1300 neuroblastoma cells in vitro. Mol. Pharmacol. 14, 644-653.
33. Halliwell B. (1989) Oxidants and the central nervous system: some fundamental questions. Acta Neurol. Scand. 126, 23-33.
34. Halliwell B., Kaur H., and Ingelman-Sundberg M. (1991) Hydroxylation of salicylate as an assay for hydroxyl radicals: a cautionary note. Free Radic. Biol. Med. 10, 439-441.
35. Hammer B., Parker W. D. Jr., and Bennett J. P. Jr. (1993) NMDA receptors increase OH radicals in vivo by using nitric oxide synthase and protein kinase C. Neuroreport 5, 72-74.
36. Han S.-K., Mytilineou C., and Cohen G. (1996) L-DOPA up-regulates glutathione and protects mesencephalic cultures against oxidative stress. J. Neurochem. 66, 501-510.
37. Hefti F., Melamed E., Bhawan J., and Wurtman R. J. (1981a) Long-term administration of L-DOPA does not damage dopaminergic neurons in the mouse. Neurology 31, 1194-1195.
38. Hefti F., Melamed E., and Wurtman R. J. (1981b) The site of dopamine formation in rat striatum after L-DOPA administration. J. Pharmacol. Exp. Ther. 217, 189-197.
39. Huang N.-K., Wan F.-J., Tseng C-J., and Tung C.-S. (1997) Amphetamine induces hydroxyl radical formation in the striatum of rats. Life Sci. 61, 2219-2229.
40. Jenner P. G. and Brin M. F. (1998) Levodopa neurotoxicity: experimental studies versus clinical relevance. Neurology 50 (Suppl. 6), S39-S43.
41. Jenner P. G. and Olanow C. W. (1996) Pathological evidence for oxidative stress in Parkinson's disease and related degenerative disorders, in Neurodegeneration and Neuroprotection in Parkinson's Disease (Olanow C. W., Jenner P., and Youdim M., eds), pp. 23-45. Academic Press, San Diego.
42. Jenner P. G. and Olanow C. W. (1998) Understanding cell death in Parkinson's disease. Ann. Neurol. 44 (Suppl. 1), S72-S84.
43. Kil H. Y., Zhang J., and Piantadosi C. A. (1996) Brain temperature alters hydroxyl radical production during cerebral ischemia/reperfusion in rats. J. Cereb. Blood Flow Metab. 16, 100-106.
44. Kondo T., Ito T., and Sugita Y. (1994) Bromocriptine scavenges methamphetamine-induced hydroxyl radicals and attenuates dopamine depletion in mouse striatum. Ann. NY Acad. Sci. 738, 222-229.
45. Lancelot E., Callebert J., Revaud M.-L., Boulu R. G., and Plotkine M. (1995a) Detection of hydroxyl radicals in rat striatum during transient focal cerebral ischemia: possible implication in tissue damage. Neurosci. Lett. 197, 85-88.
46. Lancelot E., Callebert J., Lerouet L., Revaud M.-L., Boulu R. G., and Plotkine M. (1995b) Role of the L-arginine-nitric oxide pathway in the basal hydroxyl radical production in the striatum of awake rats as measured by brain microdialysis. Neurosci. Lett. 202, 21-24.
47. LeWitt P. A. (1989) The pharmacology of levodopa in treatment of Parkinson's disease: an update, in Handbook of Experimental Pharmacology, Vol. 88: Drugs for the Treatment of Parkinson's Disease (Calne D. B., ed), pp. 325-384. Springer-Verlag, Berlin.
48. Li C-L., Werner P., and Cohen G. (1995) Lipid peroxidation in brain: interactions of L-DOPA/dopamine with ascorbate and iron. Neurodegeneration 4, 147-153.
49. Loeffler D. A., DeMaggio A. J., Juneau P. L., Havaich M. K., and LeWitt P. A. (1994) Effects of enhanced striatal dopamine turnover in vivo on glutathione oxidation. Clin, Neuropharmacol. 17, 370-379.
50. Loeffler D. A., LeWitt P. A., Juneau P. L., Camp D. M., Arnold L. A., and Hyland K. (1999) Time-dependent effects of levodopa on regional brain dopamine metabolism and lipid peroxidation. Brain Res. Bull. 47, 663-667.
51. Makar T. K., Nedergaard M., Preuss A., Gelbard A. S., Perumal A. S., and Cooper A. J. (1994) 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, 45-53.
52. Marshall J. F. and Ungerstedt U. (1977) Supersensitivity to apomorphine following destruction of the ascending dopamine neurons: quantification using the rotational model. Eur. J. Pharmacol. 41, 361-367.
53. McCabe D. R., Maher T. J., and Acworth I. N. (1997) Improved method for the estimation of hydroxyl free radical levels in vivo based on liquid chromatography with electrochemical detection. J. Chromatogr. B 691, 23-32.
54. Mena M. A., Pardo B., Casarejos M. J., Fahn S., and de Yebenes J. G. (1992) Neurotoxicity of levodopa on catecholamine-rich neurons. Mov. Disord. 7, 23-31.
55. Mena M. A., Pardo B., Paino C. L., and de Yebenes J. G. (1993) Levodopa toxicity in foetal rat midbrain neurones in culture: modulation by ascorbic acid. Neuroreport 4, 438-440.
56. Mena M. A., Casarejos M. J., Paino C. L., and de Yebenes J. G. (1996) Glia conditioned medium protects fetal rat midbrain neurones in culture from L-DOPA toxicity. Neuroreport 7, 441-445.
57. Mena M. A., Casarejos M. J., Carazo A., Paino C. L., and de Yebenes J. G. (1997a) Glia protect fetal midbrain dopamine neurons in culture from L-DOPA toxicity through multiple mechanisms. J. Neural Transm. 104, 317-328.
58. Mena M. A., Davila V., and Sulzer D. (1997b) Neurotrophic effects of L-DOPA in postnatal midbrain dopamine neuron/cortical astrocyte cocultures. J. Neurochem. 69, 1398-1408.
59. Montgomery J., Ste.-Marie L., Boismenu D., and Vachon L. (1995) Hydroxylation of aromatic compounds as indices of hydroxyl radical production: a cautionary note revisited. Free Radic. Biol. Med. 19, 927-933.
60. Morimoto T., Globus M. Y.-T., Busto R., Martinez E., and Ginsberg M. D. (1996) Simultaneous measurement of salicylate hydroxylation and glutamate release in the penumbral cortex following transient middle cerebral artery occlusion in rats. J. Cereb. Blood Flow Metab. 16, 92-99.
61. Murer M. G., Dziewczapolski G., Menalled L. B., Garcia M. C., Agid Y., Gershanik O., and Raisman-Vozari R. (1998) Chronic levodopa is not toxic for remaining dopamine neurons, but instead promotes their recovery, in rats with moderate nigrostriatal lesions. Ann. Neurol. 43, 561-575.
62. Mytilineou C. Han S.-K., and Cohen G. (1993) Toxic and protective effects of L-DOPA on mesencephalic cell cultures. J. Neurochem. 61, 1470-1478.
63. + J. Neural Transm. Gen. Sect. 89, 139-145.
64. Obata T. and Yamanaka Y. (1995) Intracranial microdialysis of salicylic acid to detect hydroxyl radical generation by monoamine oxidase inhibitor in the rat. Neurosci. Lett. 188, 13-16.
65. Obata T. and Yamanaka Y. (1996) Protective effect of carbidopa on hydroxyl radical generation in the rat striatum by dopamine. Neurosci. Lett. 221, 13-16.
66. Ogawa N., Edamatsu R., Mizukawa K., Asanuma M., Kohno M., and Mori A. (1993) Degeneration of dopaminergic neurons and free radicals: possible participation of levodopa. Adv. Neurol. 60, 242-250.
67. Ogawa N., Asanuma M., Kondo Y., Kawada Y., Yamamoto M., and Mori A. (1994) Differential effects of chronic L-DOPA treatment on lipid peroxidation in the mouse brain with or without pretreatment with 6-hydroxydopamine. Neurosci. Lett. 171, 55-58.
68. Olanow C. W. (1992) An introduction to the tree radical hypothesis in Parkinson's disease. Ann. Neurol. 32 (Suppl.), S2-S9.
69. Olney J. W., Zorumski C. F., Stewart G. R., Price M. T., Wang G., and Labruyere J. (1990) Excitotoxicity of L-DOPA and 6-OH-DOPA: implications for Parkinson's and Huntington's diseases. Exp. Neurol. 108, 269-272.
70. Orosz D. and Bennett J. P. (1992) Simultaneous microdialysis in striatum and substantia nigra suggests that the nigra is a major site of action of L-dihydroxyphenylalanine in the "hemiparkinsonian" rat. Exp. Neurol. 115, 388-393.
71. Pardo B., Mena M. A., Casarejos M. J., Paino C. L., and de Yebenes J. G. (1995a) Toxic effects of L-DOPA on mesencephalic cell cultures: protection with antioxidants. Brain Res. 682, 133-143.
72. Pardo B., Mena M. A., and de Yebenes J. G. (1995b) L-DOPA inhibits complex IV of the electron transport chain in catecholamine-rich human neuroblastoma NB69 cells. J. Neurochem. 64, 576-582.
73. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
74. Perry T. L., Yong V. W., Ito M., Foulks J. G., Wall R. A., Godin D. V., and Clavier R. M. (1984) Nigrostriatal dopamine neurons remain undamaged in rats given high doses of L-DOPA and carbidopa chronically. J. Neurochem. 43, 990-993.
75. Przedborski S., Jackson-Lewis V., Muthane U., Jiang H., Ferreira M., Naini A. B., and Fahn S. (1993) Chronic levodopa administration alters cerebral mitochondrial respiratory chain activity. Ann. Neural. 34, 715-723.
76. Quinn N., Parkes D., Janoto J., and Marsden C. D. (1986) Preservation of the substantia nigra and locus coeruleus in a patient receiving levodopa (2 kg) plus decarboxylase inhibitor over a four-year period. Mov. Disord. 1, 65-68.
77. Rajput A. H., Fenton M. E., Birdi S., and Macaulay R. (1997) Is levodopa toxic to human substantia nigra? Mov. Disord. 12, 634-638.
78. Riederer P., Sofic E., and Rausch W.-D. (1989) Transition metals, ferritin, glutathione, and ascorbic acid in parkinsonian brains. J. Neurochem. 52, 515-520.
79. Robinson T. E. and Camp D. M. (1991) The feasibility of repeated microdialysis for within-subjecls design experiments: studies on the mesostriatal dopamine system, in Microdialysis in the Neurosciences (Robinson T. E. and Justice J. B. Jr., eds), pp. 189-234. Elsevier, Amsterdam.
80. Sahakian B. J., Carlson K. R., DeGirolami U., and Bhawan J. (1980) Functional and structural consequences of long-term dietary L-DOPA treatment in mice. Commun. Psychopharmacol. 4, 169-176.
81. Sarre S., Herregodts P., Deleu D., Devrieze A., De Klippel N., Ebinger G., and Michotte Y. (1992) Biotransformation of L-DOPA in striatum and substantia nigra of rats with a unilateral, nigrostriatal lesion: a microdialysis study. Naunyn Schmiedebergs Arch. Pharmacol. 346, 277-285.
82. Seiden L. S. and Ricaurte G. A. (1987) Neurotoxicity of methamphetamine and related drugs, in Psychopharmacology: The Third Generation of Progress (Meltzer H. Y., ed), pp. 359-366. Raven Press, New York.
83. Seiden L. S. and Sabol K. E. (1996) Methamphetamine and methylenedioxymethamphetamine neurotoxicity: possible mechanisms of cell destruction. NIDA Res. Monogr. 163, 251-276.
84. Sian J., Dexter D. T., Lees A. J., Daniel S., Agid Y., Javoy-Agid F., Jenner P., and Marsden C. D. (1994) Alterations in glutathione levels in Parkinson's disease and other neurodegenerative disorders affecting basal ganglia. Ann. Neurol. 36, 348-355.
85. Smith T. S., Parker W. D. Jr., and Bennett J. P. Jr. (1994a) L-DOPA increases nigral production of hydroxyl radicals in vivo: potential L-DOPA toxicity? Neuroreport 5, 1009-1011.
86. +-induced hydroxyl radical formation and nigrostriatal MPTP toxicity by inhibiting nitric oxide synthase. Neuroreport 5, 2598-2600.
87. Sofic E., Paulus W., Jellinger K., Riederer P., and Youdim M. B. H. (1991) Selective increase of iron in substantia nigra zona compacta of parkinsonian brains. J. Neurochem. 56, 978-982.
88. Sofic E., Lange K. W., Jellinger K., and Riederer P. (1992) Reduced oxidized glutathione in the substantia nigra of patients with Parkinson's disease. Neurosci. Lett. 142, 128-130.
89. Spencer J. P. E., Jenner P., and Halliwell B. (1995) Superoxide-dependent depletion of reduced glutathione by L-DOPA and dopamine: relevance to Parkinson's disease. Neuroreport 6, 1480-1484.
90. Spencer J. P. E., Jenner A., Butler J., Aruoma O. I., Dexter D. T., Jenner P., and Halliwell B. (1996) Evaluation of the prooxidant and antioxidant actions of L-DOPA and dopamine in vitro: implications for Parkinson's disease. Free Radic. Res. 24, 95-105.
91. Spina M. B. and Cohen G. (1988) Exposure of striatal synaptosomes to L-DOPA increases levels of oxidized glutathione. J. Pharmacol. Exp. Ther. 247, 502-507.
92. Spina M. B. and Cohen O. (1989) Dopamine turnover and glutathione oxidation: implications for Parkinson's disease. Proc. Natl. Acad. Sci. USA 86, 1398-1400.
93. Steece-Collier K., Collier T. J., Sladek C. D., and Sladek J. R. (1990) Chronic levodopa impairs morphological development of grafted embryonic dopamine neurons. Exp. Neurol. 110, 201-208.
94. Steece-Collier K., Yurek D. M., Collier T. J., Junn F. S., and Sladek J. R. Jr. (1995) The detrimental effect of levodopa on behavioral efficacy of fetal dopamine neuron grafts in rats is reversible following prolonged withdrawal of chronic dosing. Brain Res. 676, 404-408.
95. Stephans S. E. and Yamamoto B. K. (1994) Methamphetamine-induced neurotoxicity: roles for glutamate and dopamine efflux. Synapse 17, 203-209.
96. Tanaka M., Sotomatsu A., Kanai H., and Hirai S. (1991) Dopa and dopamine cause cultured neuronal death in the presence of iron. J. Neurol. Sci. 101, 198-203.
97. Yamamoto B. K. and Zhu W. (1998) The effects of methamphetamine on the production of free radicals and oxidative stress. J. Pharmacol. Exp. Ther. 287, 107-114.
98. Yang C.-S., Tsai P.-J., Lin N.-N., Liu L., and Kuo J.-S. (1995) Elevated extracellular glutamate levels increased the formation of hydroxyl radical in the striatum of anesthetized rat. Free Radic. Biol. Med. 19, 453-459.
99. Yang C.-S., Lin N.-N., Tsai P.-J., Liu L., and Kuo J.-S., (1996) In vivo evidence of hydroxyl radical formation induced by elevation of extracellular glutamate after cerebral ischemia in the cortex of anesthetized rats. Free Radic. Biol. Med. 20, 245-250.
100. Zhang J. and Piantadosi C. A. (1994) Prolonged production of hydroxyl radical in rat hippocampus after brain ischemia-reperfusion is decreased by 21-aminosteroids. Neurosci. Lett. 177, 127-130.
101. Zigmond M. J., Hastings T. G., and Abercrombie E. D. (1992) Neurochemical responses to 6-hydroxydopamine and L-DOPA therapy: implications for Parkinson's disease. Ann. NY Acad. Sci. 648, 71-86.