Alpha-lipoic acid differently affects the reserpine-induced oxidative stress in the striatum and prefrontal cortex of rat brain

Neuroscience

Volumn 146, Issue 4, 2007, Pages 1758-1771

  Bilska, A ^a   Dubiel, M ^a   Sokolowska Jezewicz M ^a   Lorenc Koci, E ^b   Wlodek L ^a  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^b INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

lipoic acid; glutathione; nitric oxide; Parkinson's disease; reserpine; S nitrosothiols

Indexed keywords

GAMMA GLUTAMYLTRANSFERASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; NITRIC OXIDE; NITROSOTHIOL; RESERPINE; THIOCTIC ACID; THIOL DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ATTENUATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; MALE; NONHUMAN; OXIDATIVE STRESS; PARKINSONISM; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT;

ANIMALS; ANTIOXIDANTS; ANTIPSYCHOTIC AGENTS; BRAIN CHEMISTRY; CORPUS STRIATUM; DRUG INTERACTIONS; GLUTATHIONE; GLUTATHIONE PEROXIDASE; MALE; NITRIC OXIDE; OXIDATIVE STRESS; PREFRONTAL CORTEX; RATS; RATS, WISTAR; RESERPINE; THIOCTIC ACID;

EID: 34249039316     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.04.002     Document Type: Article

References (90)

1. Alam Z.J., Jenner A., Daniel S.E., Lees A.J., Carins N., Marsden C.D., Jenner P., and Halliwell B. Oxidative DNA damage in the parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J Neurochem 69 (1997) 1196-1203
2. Alam Z.J., Daniel S.E., Lees A.J., Marsden C.D., Jenner P., and Halliwell B. A generalized increase in protein carbonyls in the brain in Parkinson's but not incidental Lewy body disease. J Neurochem 69 (1997) 1326-1329
3. Anderson M.E. Glutathione: an overview of biosynthesis and modulation. Chem Biol Interact 112 (1998) 1-14
4. Anderson M.E., and Meister A. Marked increase of cysteine levels in many regions of the brain after administration of 2-oxothiazolidine-4-carboxylate. FASEB J 3 (1989) 1632-1636
5. Andoh T., Chiueh C.C., and Chock P.B. Cyclic GMP-dependent protein kinase regulates the expression of thioredoxin and thioredoxin peroxidase-1 during hormesis in response to oxidative stress-induced apoptosis. J Biol Chem 278 (2003) 885-890
6. Antkiewicz-Michaluk L., Krygowska-Wajs A., Michaluk J., Romańska I., Szczudlik A., and Vetulani J. Plasticity of extrapyramidal dopamine system in Parkinson's disease: a postmortem study. Neurosci Res Commun 25 (1999) 97-109
7. Arivazhagan P., Ramanathan K., and Panneerselvam C. Effect of DL-alpha-lipoic acid on glutathione metabolic enzymes in aged rats. Exp Gerontol 37 (2001) 81-87
8. Arivazhagan P., Shila S., Kumaran S., and Panneerselvam C. Effect of DL-alpha-lipoic acid on the status of lipid peroxidation and antioxidant enzymes in various brain regions of aged rats. Exp Gerontol 37 (2002) 803-811
9. Arner E.S., and Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267 (2000) 6102-6109
10. Baez S., Segura-Aguilar J., Widersten M., Johansson A.S., and Mannervik B. Glutathione transferases catalyse the detoxication of oxidized metabolites (o-quinones) of catecholamines and may serve as an antioxidant system preventing degenerative cellular processes. Biochem J 324 (1997) 25-28
11. Balazy M., Kaminski P.M., Mao K., Tan J., and Wolin M.S. S-nitroglutathione, a product of the reaction between peroxynitrite and glutathione that generates nitric oxide. J Biol Chem 273 (1998) 32009-32015
12. Bharath S., Cochran B.C., Hsu M., Liu J., Ames B.N., and Andersen J.K. Pre-treatment with R-lipoic acid alleviates the effects of GSH depletion in PC12 cells: implications for Parkinson's disease therapy. Neurotoxicology 23 (2002) 479-486
13. Biewenga G.P., Haenen G.R., and Bast A. The pharmacology of the antioxidant lipoic acid. Gen Pharmacol 29 (1997) 315-331
14. Borges C.R., Geddes T., Watson J.T., and Kuhn D.M. Dopamine biosynthesis is regulated by S-glutathionylation. Potential mechanism of tyrosine hydroxylase inhibition during oxidative stress. J Biol Chem 277 (2002) 48295-48302
15. Busse E., Zimmer G., Schopohl B., and Kornhuber B. Influence of alpha-lipoic acid on intracellular glutathione in vitro and in vivo. Arzneimittelforschung 42 (1992) 829-831
16. Bustamante J., Lodge J.K., Marcocci L., Tritschler H.J., Packer L., and Rihn B.H. Alpha-lipoic acid in liver metabolism and disease. Free Radic Biol Med 24 (1998) 1023-1039
17. Chiueh C.C., Krishna G., Tulsi P., Obata T., Lang K., Huang S.-J., and Murphy D.J. Intracranial microdialysis of salicylic acid to detect hydroxyl radical generation through dopamine autooxidation in the caudate nucleus. Free Radic Biol Med 13 (1992) 581-583
18. Chiueh C.C., and Rauhala P. The redox pathway of S-nitrosoglutathione, glutathione and nitric oxide in cell to neuron communications. Free Radic Res 31 (1999) 641-650
19. Cohen G. The pathobiology of Parkinson's disease: biochemical aspects of dopamine neuron senescence. J Neural Transm Suppl 19 (1983) 89-103
20. Colpaert F.C. Pharmacological characteristics of tremor, rigidity and hypokinesia induced by reserpine in rat. Neuropharmacology 26 (1987) 1431-1440
21. Dagnino-Subiabre A., Cassels B.K., Baez S., Johansson A.S., Mannervik B., and Segura-Aguilar J. Glutathione transferase M2-2 catalyzes conjugation of dopamine and dopa o-quinones. Biochem Biophys Res Commun 274 (2000) 32-36
22. Daily D., Vlamis-Gardikas A., Offen D., Mittelman L., Melamed E., Holmgren A., and Barzilai A. Glutaredoxin protects cerebellar granule neurons from dopamine-induced apoptosis by dual activation of the ras-phosphoinositide 3-kinase and jun n-terminal kinase pathways. J Biol Chem 276 (2001) 21618-21626
23. Dexter D.T., Wells F.R., Lee A., Agid Y., Jenner P., and Marsden D. Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson's disease. J Neurochem 52 (1989) 1830-1836
24. 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. Increased levels of lipid hydroperoxides in the parkinsonian substantia nigra: an HPLC and ESR study. Mov Disord 9 (1994) 92-97
25. Dikalov S., Khramtsov V., and Zimmer G. Determination of rate constants of the reactions of thiols with superoxide radical by electron paramagnetic resonance: critical remarks on spectrophotometric approaches. Arch Biochem Biophys 326 (1996) 207-218
26. Di Stefano A., Sozio P., Cocco A., Iannitelli A., Santucci E., Costa M., Pecci L., Nasuti C., Cantalamessa F., and Pinnen F. L-dopa- and dopamine-(R)-alpha-lipoic acid conjugates as multifunctional codrugs with antioxidant properties. J Med Chem 49 (2006) 1486-1493
27. 2 production and S-thiolation. Free Radic Biol Med 27 (1999) 623-635
28. Dringen R. Metabolism and functions of glutathione in brain. Prog Neurobiol 62 (2000) 649-671
29. Dringen R., Gutterer J.M., and Hirrlinger J. Glutathione metabolism in brain metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species. Eur J Biochem 267 (2000) 4912-4916
30. Dringen R., Kranich O., and Hamprecht B. The gamma-glutamyl transpeptidase inhibitor acivicin preserves glutathione released by astroglial cells in culture. Neurochem Res 22 (1997) 727-733
31. Dringen R., Pawlowski P.G., and Hirrlinger J. Peroxide detoxification by brain cells. J Neurosci Res 79 (2005) 157-165
32. Elverfors A., and Nissbrandt H. Reserpine-insensitive dopamine release in the substantia nigra?. Brain Res 557 (1991) 5-12
33. Fahn S., and Cohen G. The oxidant stress hypothesis in Parkinson's disease: evidence supporting it. Ann Neurol 32 (1992) 804-812
34. Farr S.A., Poon H.F., Dogrukol-Ak D., Drake J., Banks W.A., Eyerman E., Butterfield D.A., and Morley J.E. The antioxidants alpha-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice. J Neurochem 84 (2003) 1173-1183
35. Filloux F., and Townsend J.J. Pre- and postsynaptic neurotoxic effects of dopamine demonstrated by intrastriatal injection. Exp Neurol 119 (1993) 79-88
36. Flier J., Van Muiswinkel F.L., Jongenelen C.A., and Drukarch B. The neuroprotective antioxidant alpha-lipoic acid induces detoxication enzymes in cultured astroglial cells. Free Radic Res 36 (2002) 695-699
37. Flohe L., and Gunzler W.A. Assays of glutathione peroxidase. Methods Enzymol 105 (1984) 114-121
38. Fornstedt B., Brun A., Rosengren E., and Carlsson A. The apparent autoxidation rate of catechols in dopamine-rich regions of human brains increases with the degree of depigmentation of substantia nigra. J Neural Transm Park Dis Dement Sect 1 (1989) 279-295
39. Fornstedt B., and Carlsson A. A marked rise in 5-S-cysteinyl-dopamine levels in guinea-pig striatum following reserpine treatment. J Neural Transm 76 (1989) 155-161
40. 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 25 (1986) 451-454
41. Giustarini D., Rossi R., Milzani A., Colombo R., and Dalle-Donne I. S-glutathionylation: from redox regulation of protein functions to human diseases. J Cell Mol Med 8 (2004) 201-212
42. Gow A.J., Buerk D.G., and Ischiropoulos H. A novel reaction mechanism for the formation of S-nitrosothiol in vivo. J Biol Chem 272 (1997) 2841-2845
43. Graham D.G. Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol Pharmacol 14 (1978) 633-643
44. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylopiridine. Anal Biochem 15 (1980) 207-212
45. Habig W.H., Pabst M.J., and Jakoby W.B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 193 (1974) 265-275
46. Han D., Handelman G., Marcocci L., Sen C.K., Roy S., Kobuchi H., Tritschler H.J., Flohe L., and Packer L. Alpha-lipoic acid increases de novo synthesis of cellular glutathione by improving cystine utilization. Biofactors 6 (1997) 321-338
47. Handelman G.J., Han D., Tritschler H., and Packer L. Alpha-lipoic acid reduction by mammalian cells to the dithiol form, and release into the culture medium. Biochem Pharmacol 47 (1994) 1725-1730
48. Hastings T.G., Lewis D.A., and Zigmond M.J. Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc Natl Acad Sci U S A 93 (1996) 1956-1961
49. Hayes J.D., Flanagan J.U., and Jowsey I.R. Glutathione transferases. Annu Rev Pharmacol Toxicol 45 (2005) 51-88
50. Hirrlinger J., Konig J., Keppler D., Lindenau J., Schulz J.B., and Dringen R. The multidrug resistance protein MRP1 mediates the release of glutathione disulfide from rat astrocytes during oxidative stress. J Neurochem 76 (2001) 627-636
51. Hornykiewicz O., and Kish S.J. Biochemical pathophysiology of Parkinson's disease. Adv Neurol 45 (1987) 19-34
52. Hou Y., Guo Z., Li J., and Wang P.G. Seleno-compounds and glutathione peroxidase catalyzed decomposition of S-nitrosothiols. Biochem Biophys Res Commun 228 (1996) 88-93
53. Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol 53 Suppl 3 (2003) 26-38
54. Kagan V.E., Kozlov A.V., Tyurina Y.Y., Shedova W., and Yalowich J.C. Antioxidant mechanism of nitric oxide against iron-catalysed oxidative stress in cells. Antioxid Redox Signal 3 (2001) 189-202
55. Kanner J., Harel S., and Granit R. Nitric oxide as an antioxidant. Arch Biochem Biophys 289 (1991) 130-136
56. Kenchappa R.S., and Ravindranath V. Glutaredoxin is essential for maintenance of brain mitochondrial complex I: studies with MPTP. FASEB J 17 (2003) 717-719
57. Klatt P., and Lamas S. Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267 (2000) 4928-4944
58. Kozlov A.V., Gille L., Staniek K., and Pohl H. Dihydrolipoic acid maintains ubiquinone in the antioxidant active form by two-electron reduction of ubiquinone and one-electron reduction of ubisemiquinone. Arch Biochem Biophys 363 (1999) 148-154
59. Kuhn D.M., Aretha C.W., and Geddes T.J. Peroxynitrite inactivation of tyrosine hydroxylase: mediation by sulfhydryl oxidation, not tyrosine nitration. J Neurosci 19 (1999) 10289-10294
60. Kuhn D.M., Arthur Jr. R.E., Thomas D.M., and Elferink L.A. Tyrosine hydroxylase is inactivated by catechol-quinones and converted to a redox-cycling quinoprotein: possible relevance to Parkinson's disease. J Neurochem 73 (1999) 1309-1317
61. LaVoie M.J., and Hastings T.G. Peroxynitrite- and nitrite-induced oxidation of dopamine: implication for nitric oxide in dopaminergic cell loss. J Neurochem 73 (1999) 2546-2554
62. Linderson Y., Baez S., and Segura-Aguilar J. The protective effect of superoxide dismutase and catalase against formation of reactive oxygen species during reduction of cyclized norepinephrine ortho-quinone by DT-diaphorase. Biochim Biophys Acta 1200 (1994) 197-204
63. Lorenc-Koci E., Ossowska K., Wardas J., and Wolfarth S. Does reserpine induce parkinsonian rigidity?. J Neural Transm Park Dis Dement Sect 9 (1995) 211-223
64. Marzinzig M., Nussler A.K., Stadler J., Marzinzig E., Barthlen W., Nussler N.C., Berger H.G., Morris S.M., and Brickner U.B. Improved methods to measure end products of nitric oxide in biological fluids: nitrite, nitrate and S-nitrosothiols. Nitric Oxide 1 (1997) 177-189
65. Mena M.A., Pardo B., Casarejos M.J., Fahn S., and Garcia de Yebenes J. Neurotoxicity of levodopa on catecholamine-rich neurons. Mov Disord 7 (1992) 23-31
66. Minich T., Riemer J., Schulz J.B., Wielinga P., Wijnholds J., and Dringen R. The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J Neurochem 97 (2006) 373-384
67. Okamoto T., Akaike T., Sawa T., Miyamoto Y., van der Vliet A., and Maeda H. Activation of matrix metalloproteinases by peroxynitrite-induced protein S-glutathiolation via disulfide S-oxide formation. J Biol Chem 276 (2001) 29596-29602
68. Orlowski M., and Meister A. Isolation of γ-glutamyl transpeptidase from dog kidney. J Biol Chem 240 (1966) 338-340
69. Packer L., Tritschler H.J., and Wessel K. Neuroprotection by the metabolic antioxidant alpha-lipoic acid. Free Radic Biol Med 22 (1997) 359-378
70. Panigrahi M., Sadguna Y., Shivakumar B.R., Kolluri S.V., Roy S., Packer L., and Ravindranath V. alpha-Lipoic acid protects against reperfusion injury following cerebral ischemia in rats. Brain Res 717 (1996) 184-188
71. Pileblad E., and Magnusson T. Increase in rat brain glutathione following intracerebroventricular administration of gamma-glutamylcysteine. Biochem Pharmacol 44 (1992) 895-903
72. Przedborski S., Jackson-Lewis V., Yokoyama R., Shibata T., Dawson V.L., and Dawson T.M. Role of neuronal nitric oxide in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced dopaminergic neurotoxicity. Proc Natl Acad Sci U S A 93 (1996) 4565-4571
73. Rauhala P., Andoh T., and Chiueh C.C. Neuroprotective properties of nitric oxide and S-nitrosoglutathione. Toxicol Appl Pharmacol 207 (2005) 91-95
74. Rauhala P., Lin A.M., and Chiueh C.C. Neuroprotection by S-nitrosoglutathione of brain dopamine neurons from oxidative stress. FASEB J 112 (1998) 165-173
75. Rauhala P., Sziraki I., and Chiueh C.C. Peroxidation of brain lipids in vitro: nitric oxide versus hydroxyl radicals. Free Radic Biol Med 21 (1996) 391-394
76. Rossi R., Cardaioli E., Scaloni A., Amiconi G., and Di Simplicio P. Thiol groups in proteins as endogenous reductants to determine glutathione-protein mixed disulphides in biological systems. Biochim Biophys Acta 1243 (1995) 230-238
77. Segura-Aguilar J., Baez S., Widersten M., Welch C.J., and Mannervik B. Human class Mu glutathione transferases, in particular isoenzyme M2-2, catalyze detoxication of the dopamine metabolite aminochrome. J Biol Chem 272 (1997) 5727-5731
78. Sharpe M.A., Robb S.J., and Clark J.B. Nitric oxide and Fenton/Haber-Weiss chemistry: nitric oxide is a potent antioxidant at physiological concentrations. J Neurochem 87 (2003) 386-394
79. Sian J., Dexter D.T., Lees A.J., Daniel S., Jenner P., and Marsden C.D. Glutathione-related enzymes in brain in Parkinson's disease. Ann Neurol 36 (1994) 356-361
80. Smith A.R., Shenvi S.V., Widlansky M., Suh J.H., and Hagen T.M. Lipoic acid as a potential therapy for chronic diseases associated with oxidative stress. Curr Med Chem 11 (2004) 1135-1146
81. Spina M.B., and Cohen G. Exposure of striatal synaptosomes to L-dopa increases levels of oxidized glutathione. J Pharmacol Exp Ther 247 (1988) 502-507
82. Spina M.B., and Cohen G. Dopamine turnover and glutathione oxidation: implications for Parkinson disease. Proc Natl Acad Sci U S A 86 (1989) 1389-1400
83. Stakhiv T.M., Mesia-Vela S., and Kauffman F.C. Phase II antioxidant enzyme activities in brain of male and female ACI rats treated chronically with estradiol. Brain Res 1104 (2006) 80-91
84. Suh J.H., Zhu B.Z., deSzoeke E., Frei B., and Hagen T.M. Dihydrolipoic acid lowers the redox activity of transition metal ions but does not remove them from the active site of enzymes. Redox Rep 9 (2004) 57-61
85. Tanaka M., Sotomatsu A., Kanai H., and Hirai S. Dopa and dopamine cause cultured neuronal death in the presence of iron. J Neurol Sci 101 (1991) 198-203
86. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27 (1969) 502-522
87. Van der Vliet A., Hoen P.A., Wong P.S., Bast A., and Cross C.E. Formation of S-nitrosothiols via direct nucleophilic nitrosation of thiols by peroxynitrite with elimination of hydrogen peroxide. J Biol Chem 273 (1998) 30255-30262
88. van Muiswinkel F.L., Riemers F.M., Peters G.J., LaFleur M.V., Siegel D., Jongenelen C.A., and Drukarch B. L-Dopa stimulates expression of the antioxidant enzyme NAD(P)H:quinone oxidoreductase (NQO) in cultured astroglial cells. Free Radic Biol Med 29 (2000) 442-453
89. Vriesman M.F., Haenen G.R., Westerveld G.J., Paquay J.B., Voss H.P., and Bast A. A method for measuring nitric oxide radical scavenging activity. Scavenging properties of sulfur-containing compounds. Pharm Word Sci 19 (1997) 283-286
90. Zhang J., Perry G., Smith M.A., Robertson D., Olson S.J., Graham D.G., and Montine T.J. Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am J Pathol 154 (1999) 1423-1429