Melatonin is protective against 6-hydroxydopamine-induced oxidative stress in a hemiparkinsonian rat model

Free Radical Research

Volumn 49, Issue 8, 2015, Pages 1004-1014

  Ozsoy, O ^a   Yildirim, F B ^a   Ogut, E ^a   Kaya, Y ^a   Tanriover, G ^a   Parlak, H ^a   Agar, A ^a   Aslan, M ^a  

^a AKDENIZ UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; GLUTATHIONE PEROXIDASE; MELATONIN; OXIDOPAMINE; SUPEROXIDE DISMUTASE; TYROSINE 3 MONOOXYGENASE; NEUROPROTECTIVE AGENT; SCAVENGER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LIPID PEROXIDATION; LOCOMOTION; MALE; MEDIAL FOREBRAIN BUNDLE; MOTOR ACTIVITY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; RAT; SUBSTANTIA NIGRA; SUPPLEMENTATION; ANIMAL; CHEMICALLY INDUCED; ENZYMOLOGY; METABOLISM; PARKINSON DISEASE, SECONDARY; PATHOLOGY; PRECLINICAL STUDY; WISTAR RAT;

RATTUS; RATTUS NORVEGICUS;

ANIMALS; CATALASE; DRUG EVALUATION, PRECLINICAL; FREE RADICAL SCAVENGERS; GLUTATHIONE PEROXIDASE; LIPID PEROXIDATION; MALE; MEDIAL FOREBRAIN BUNDLE; MELATONIN; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; OXIDOPAMINE; PARKINSON DISEASE, SECONDARY; RATS, WISTAR; SUBSTANTIA NIGRA; SUPEROXIDE DISMUTASE; TYROSINE 3-MONOOXYGENASE;

EID: 84938385734     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2015.1027198     Document Type: Article

References (98)

1. Parkinson J. An essay on the shaking palsy. 1817. J Neuropsychiatry Clin Neurosci 2002; 14: 223-236; discussion 222.
2. Jankovic J. Parkinson's disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 2008; 79: 368-376.
3. Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Seitelberger F. Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J Neurol Sci 1973; 20: 415-455.
4. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, Marsden CD. Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem 1990; 54: 823-827.
5. Ebadi M, Srinivasan SK, Baxi MD. Oxidative stress and antioxidant therapy in Parkinson's disease. Prog Neurobiol 1996; 48: 1-19.
6. Jenner P, Olanow CW. Oxidative stress and the pathogenesis of Parkinson's disease. Neurology 1996; 47: S161-S170.
7. 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.
8. Sofic E, Paulus W, Jellinger K, Riederer P, Youdim MB. Selective increase of iron in substantia nigra zona compacta of parkinsonian brains. J Neurochem 1991; 56: 978-982.
9. Sengstock GJ, Olanow CW, Menzies RA, Dunn AJ, Arendash GW. Infusion of iron into the rat substantia nigra: nigral pathology and dose-dependent loss of striatal dopaminergic markers. J Neurosci Res 1993; 35: 67-82.
10. Ungerstedt U. Postsynaptic supersensitivity after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol Scand Suppl 1971; 367: 69-93.
11. Cohen G, Heikkila RE. The generation of hydrogen peroxide, superoxide radical, and hydroxyl radical by 6-hydroxydopamine, dialuric acid, and related cytotoxic agents. J Biol Chem 1974; 249: 2447-2452.
12. Blum D, Torch S, Lambeng N, Nissou M, Benabid AL, Sadoul R, Verna JM. Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog Neurobiol 2001; 65: 135-172.
13. Monteiro HP, Winterbourn CC. 6-Hydroxydopamine releases iron from ferritin and promotes ferritin-dependent lipid peroxidation. Biochem Pharmacol 1989; 38: 4177-4182.
14. Glinka YY, Youdim MB. Inhibition of mitochondrial complexes I and IV by 6-hydroxydopamine. Eur J Pharmacol 1995; 292: 329-332.
15. de Araujo DP, De Sousa CN, Araujo PV, Menezes CE, Sousa Rodrigues FT, Escudeiro SS, et al. Behavioral and neurochemical effects of alpha-lipoic Acid in the model of Parkinson's disease induced by unilateral stereotaxic injection of 6-ohda in rat. Evid Based Complement Alternat Med 2013; 2013: 571378.
16. Kumar R, Agarwal AK, Seth PK. Free radical-generated neurotoxicity of 6-hydroxydopamine. J Neurochem 1995; 64: 1703-1707.
17. Sedaghat R, Roghani M, Khalili M. Neuroprotective effect of thymoquinone, the nigella sativa bioactive compound, in 6-hydroxydopamine-induced hemi-parkinsonian rat model. Iran J Pharm Res 2014; 13: 227-234.
18. Rezaei M, Alirezaei M. Protective effects of Althaea officinalis L. extract in 6-hydroxydopamine-induced hemi-Parkinsonism model: behavioral, biochemical and histochemical evidence. J Physiol Sci 2014; 64: 171-176.
19. Perumal AS, Gopal VB, Tordzro WK, Cooper TB, Cadet JL. Vitamin E attenuates the toxic effects of 6-hydroxydopamine on free radical scavenging systems in rat brain. Brain Res Bull 1992; 29: 699-701.
20. Esposito E, Cuzzocrea S. Antiinflammatory activity of melatonin in central nervous system. Curr Neuropharmacol 2010; 8: 228-242.
21. Reiter RJ. Melatonin: clinical relevance. Best Pract Res Clin Endocrinol Metab 2003; 17: 273-285.
22. Ianas O, Olinescu R, Badescu I. Melatonin involvement in oxidative processes. Endocrinologie 1991; 29: 147-153.
23. Reiter RJ, Tan DX, Gitto E, Sainz RM, Mayo JC, Leon J, et al. Pharmacological utility of melatonin in reducing oxidative cellular and molecular damage. Pol J Pharmacol 2004; 56: 159-170.
24. Mohanan PV, Yamamoto HA. Preventive effect of melatonin against brain mitochondria DNA damage, lipid peroxidation and seizures induced by kainic acid. Toxicol Lett 2002; 129: 99-105.
25. Acuna-Castroviejo D, Martin M, Macias M, Escames G, Leon J, Khaldy H, Reiter RJ. Melatonin, mitochondria, and cellular bioenergetics. J Pineal Res 2001; 30: 65-74.
26. Leon J, Acuna-Castroviejo D, Escames G, Tan DX, Reiter RJ, Melatonin mitigates mitochondrial malfunction. J Pineal Res 2005; 38: 1-9.
27. Jimenez-Aranda A, Fernandez-Vazquez G, Mohammad ASM, Reiter RJ, Agil A. Melatonin improves mitochondrial function in inguinal white adipose tissue of Zucker diabetic fatty rats. J Pineal Res 2014; 57: 103-109.
28. Tan DX, Reiter RJ, Manchester LC, Yan MT, El-Sawi M, Sainz RM, et al. Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger. Curr Top Med Chem 2002; 2: 181-197.
29. Pieri C, Marra M, Moroni F, Recchioni R, Marcheselli F. Melatonin: a peroxyl radical scavenger more effective than vitamin E. Life Sci 1994; 55: PL271-PL276.
30. Galano A, Tan DX, Reiter RJ. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
31. Galano A, Tan DX, Reiter RJ. On the free radical scavenging activities of melatonin's metabolites, AFMK and AMK. J Pineal Res 2013; 54: 245-257.
32. Reiter RJ, Tan DX, Manchester LC, Qi W. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochem Biophys 2001; 34: 237-256.
33. Limson J, Nyokong T, Daya S. The interaction of melatonin and its precursors with aluminium, cadmium, copper, iron, lead, and zinc: an adsorptive voltammetric study. J Pineal Res 1998; 24: 15-21.
34. Lin AM, Ho LT. Melatonin suppresses iron-induced neurodegeneration in rat brain. Free Radic Biol Med 2000; 28: 904-911.
35. Kabuto H, Yokoi I, Ogawa N. Melatonin inhibits iron-induced epileptic discharges in rats by suppressing peroxidation. Epilepsia 1998; 39: 237-243.
36. Tomas-Zapico C, Coto-Montes A. A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. J Pineal Res 2005; 39: 99-104.
37. Mayo JC, Tan DX, Sainz RM, Lopez-Burillo S, Reiter RJ. Oxidative damage to catalase induced by peroxyl radicals: functional protection by melatonin and other antioxidants. Free Radic Res 2003; 37: 543-553.
38. Acuna-Castroviejo D, Escames G, Macias M, Munoz Hoyos A, Molina Carballo A, Arauzo M, Montes R. Cell protective role of melatonin in the brain. J Pineal Res 1995; 19: 57-63.
39. Sharma R, McMillan CR, Tenn CC, Niles LP. Physiological neuroprotection by melatonin in a 6-hydroxydopamine model of Parkinson's disease. Brain Res 2006; 1068: 230-236.
40. Jin BK, Shin DY, Jeong MY, Gwag MR, Baik HW, Yoon KS, et al. Melatonin protects nigral dopaminergic neurons from 1-methyl-4-phenylpyridinium (MPP+) neurotoxicity in rats. Neurosci Lett 1998; 245: 61-64.
41. Kim YS, Joo WS, Jin BK, Cho YH, Baik HH, Park CW. Melatonin protects 6-OHDA-induced neuronal death of nigrostriatal dopaminergic system. Neuroreport 1998; 9: 2387-2390.
42. Dabbeni-Sala F, Di Santo S, Franceschini D, Skaper SD, Giusti P. Melatonin protects against 6-OHDA-induced neurotoxicity in rats: a role for mitochondrial complex I activity. FASEB J 2001; 15: 164-170.
43. Capitelli C, Sereniki A, Lima MM, Reksidler AB, Tufik S, Vital MA. Melatonin attenuates tyrosine hydroxylase loss and hypolocomotion in MPTP-lesioned rats. Eur J Pharmacol 2008; 594: 101-108.
44. Ma J, Shaw VE, Mitrofanis J. Does melatonin help save dopaminergic cells in MPTP-treated mice? Parkinsonism Relat Disord 2009; 15: 307-314.
45. Antolin I, Mayo JC, Sainz RM, del Brio Mde L, Herrera F, Martin V, Rodriguez C. Protective effect of melatonin in a chronic experimental model of Parkinson's disease. Brain Res 2002; 943: 163-173.
46. Thomas B, Mohanakumar KP. Melatonin protects against oxidative stress caused by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in the mouse nigrostriatum. J Pineal Res 2004; 36: 25-32.
47. Acuna-Castroviejo D, Coto-Montes A, Gaia Monti M, Ortiz GG, Reiter RJ. Melatonin is protective against MPTPinduced striatal and hippocampal lesions. Life Sci 1997; 60: PL23-PL29.
48. Saravanan KS, Sindhu KM, Mohanakumar KP. Melatonin protects against rotenone-induced oxidative stress in a hemiparkinsonian rat model. J Pineal Res 2007; 42: 247-253.
49. Mayo JC, Sainz RM, Antolin I, Rodriguez C. Ultrastructural confirmation of neuronal protection by melatonin against the neurotoxin 6-hydroxydopamine cell damage. Brain Res 1999; 818: 221-227.
50. Grealish S, Xie L, Kelly M, Dowd E. Unilateral axonal or terminal injection of 6-hydroxydopamine causes rapid-onset nigrostriatal degeneration and contralateral motor impairments in the rat. Brain Res Bull 2008; 77: 312-319.
51. Paxinos G, Watson C, Pennisi M, Topple A. Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of diff erent sex, strain and weight. J Neurosci Methods 1985; 13: 139-143.
52. Hacioglu G, Seval-Celik Y, Tanriover G, Ozsoy O, Saka-Topcuoglu E, Balkan S, Agar A. Docosahexaenoic acid provides protective mechanism in bilaterally MPTP-lesioned rat model of Parkinson's disease. Folia Histochem Cytobiol 2012; 50: 228-238.
53. Tanriover G, Seval-Celik Y, Ozsoy O, Akkoyunlu G, Savcioglu F, Hacioglu G, et al. The effects of docosahexaenoic acid on glial derived neurotrophic factor and neurturin in bilateral rat model of Parkinson's disease. Folia Histochem Cytobiol 2010; 48: 434-441.
54. Patki G, Lau YS. Melatonin protects against neurobehavioral and mitochondrial deficits in a chronic mouse model of Parkinson's disease. Pharmacol Biochem Behav 2011; 99: 704-711.
55. Kayir H, Goktalay G, Yildirim M, Uzbay TI. Clozapine inhibits development and expression of nicotine-induced locomotor sensitization in rats. Synapse 2009; 63: 15-21.
56. Wasowicz W, Neve J, Peretz A. Optimized steps in fluorometric determination of thiobarbituric acid-reactive substances in serum: importance of extraction pH and influence of sample preservation and storage. Clin Chem 1993; 39: 2522-2526.
57. Alam ZI, Jenner A, Daniel SE, Lees AJ, Cairns N, Marsden CD, et al. Oxidative DNA damage in the parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J Neurochem 1997; 69: 1196-1203.
58. Tan D, Chen LD, Poeggeler B, Manchester LC, Reiter, RJ. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocrine J 1993; 1: 57-60.
59. Joo WS, Jin BK, Park CW, Maeng SH, Kim YS. Melatonin increases striatal dopaminergic function in 6-OHDA-lesioned rats. Neuroreport 1998; 9: 4123-4126.
60. Aguiar LM, Vasconcelos SM, Sousa FC, Viana GS. Melatonin reverses neurochemical alterations induced by 6-OHDA in rat striatum. Life Sci 2002; 70: 1041-1051.
61. Rodriguez C, Mayo JC, Sainz RM, Antolin I, Herrera F, Martin V, Reiter RJ. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36: 1-9.
62. Vega-Naredo I, Poeggeler B, Sierra-Sanchez V, Caballero B, Tomas-Zapico C, Alvarez-Garcia O, et al. Melatonin neutralizes neurotoxicity induced by quinolinic acid in brain tissue culture. J Pineal Res 2005; 39: 266-275.
63. Li LY, Zhao XL, Fei XF, Gu ZL, Qin ZH, Liang ZQ. Bilobalide inhibits 6-OHDA-induced activation of NF-kappaB and loss of dopaminergic neurons in rat substantia nigra. Acta Pharmacol Sin 2008; 29: 539-547.
64. Rauch F, Schwabe K, Krauss JK. Effect of deep brain stimulation in the pedunculopontine nucleus on motor function in the rat 6-hydroxydopamine Parkinson model. Behav Brain Res 2010; 210: 46-53.
65. Rizelio V, Szawka RE, Xavier LL, Achaval M, Rigon P, Saur L, et al. Lesion of the subthalamic nucleus reverses motor deficits but not death of nigrostriatal dopaminergic neurons in a rat 6-hydroxydopamine-lesion model of Parkinson's disease. Braz J Med Biol Res 2010; 43: 85-95.
66. Anton-Tay F, Diaz JL, Fernandez-Guardiola A. On the effect of melatonin upon human brain. Its possible therapeutic implications. Life Sci I 1971; 10: 841-850.
67. Cotzias GC, Tang LC, Miller ST, Ginos JZ. Melatonin and abnormal movements induced by L-dopa in mice. Science 1971; 173: 450-452.
68. Shaw KM, Stern GM, Sandler M. Melatonin and parkinsonism. Lancet 1973; 1: 271.
69. Papavasiliou PS, Cotzias GC, Duby SE, Steck AJ, Bell M, Lawrence WH. Melatonin and parkinsonism. JAMA 1972; 221: 88-89.
70. Zaitone SA, Hammad LN, Farag NE. Antioxidant potential of melatonin enhances the response to L-dopa in 1-methyl 4-phenyl 1,2,3,6-tetrahydropyridine-parkinsonian mice. Pharmacol Rep 2013; 65: 1213-1226.
71. Khaldy H, Escames G, Leon J, Bikjdaouene L, Acuna-Castroviejo D. Synergistic effects of melatonin and deprenyl against MPTP-induced mitochondrial damage and DA depletion. Neurobiol Aging 2003; 24: 491-500.
72. Singhal NK, Srivastava G, Patel DK, Jain SK, Singh MP. Melatonin or silymarin reduces maneb- and paraquat-induced Parkinson's disease phenotype in the mouse. J Pineal Res 2011; 50: 97-109.
73. Sharma R, McMillan CR, Niles LP. Neural stem cell transplantation and melatonin treatment in a 6-hydroxydopamine model of Parkinson's disease. J Pineal Res 2007; 43: 245-254.
74. Willis GL, Armstrong SM. A therapeutic role for melatonin antagonism in experimental models of Parkinson's disease. Physiol Behav 1999; 66: 785-795.
75. Iacovitti L, Stull ND, Johnston K. Melatonin rescues dopamine neurons from cell death in tissue culture models of oxidative stress. Brain Res 1997; 768: 317-326.
76. Venero JL, Absi el-H, Cano J, Machado A. Melatonin induces tyrosine hydroxylase mRNA expression in the ventral mesencephalon but not in the hypothalamus. J Pineal Res 2002; 32: 6-14.
77. Schober A. Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell Tissue Res 2004; 318: 215-224.
78. Mayo JC, Sainz RM, Uria H, Antolin I, Esteban MM, Rodriguez C. Inhibition of cell proliferation: a mechanism likely to mediate the prevention of neuronal cell death by melatonin. J Pineal Res 1998; 25: 12-18.
79. Miller E, Walczak A, Majsterek I, Kedziora J. Melatonin reduces oxidative stress in the erythrocytes of multiple sclerosis patients with secondary progressive clinical course. J Neuroimmunol 2013; 257: 97-101.
80. Ortiz GG, Benitez-King GA, Rosales-Corral SA, Pacheco-Moises FP, Velazquez-Brizuela IE. Cellular and biochemical actions of melatonin which protect against free radicals: role in neurodegenerative disorders. Curr Neuropharmacol 2008; 6: 203-214.
81. Bai J, Dong L, Song Z, Ge H, Cai X, Wang G, Liu P. The role of melatonin as an antioxidant in human lens epithelial cells. Free Radic Res 2013; 47: 635-642.
82. Kilic U, Kilic E, Tuzcu Z, Tuzcu M, Ozercan IH, Yilmaz O, et al. Melatonin suppresses cisplatin-induced nephrotoxicity via activation of Nrf-2/HO-1 pathway. Nutr Metab (Lond) 2013; 10: 7.
83. Antolin I, Rodriguez C, Sainz RM, Mayo JC, Uria H, Kotler ML, et al. Neurohormone melatonin prevents cell damage: effect on gene expression for antioxidant enzymes. FASEB J 1996; 10: 882-890.
84. Sian J, Dexter DT, Lees AJ, Daniel S, Agid Y, Javoy-Agid F, et al. Alterations in glutathione levels in Parkinson's disease and other neurodegenerative disorders aff ecting basal ganglia. Ann Neurol 1994; 36: 348-355.
85. Magalingam KB, Radhakrishnan A, Haleagrahara N. Protective effects of flavonol isoquercitrin, against 6-hydroxy dopamine (6-OHDA)-induced toxicity in PC12 cells. BMC Res Notes 2014; 7: 49.
86. Liu F, Ng TB. Effect of pineal indoles on activities of the antioxidant defense enzymes superoxide dismutase, catalase, and glutathione reductase, and levels of reduced and oxidized glutathione in rat tissues. Biochem Cell Biol 2000; 78: 447-453.
87. Reiter RJ, Tan DX, Manchester LC, Paredes SD, Mayo JC, Sainz RM. Melatonin and reproduction revisited. Biol Reprod 2009; 81: 445-456.
88. Mayo JC, Sainz RM, Antoli I, Herrera F, Martin V, Rodriguez C. Melatonin regulation of antioxidant enzyme gene expression. Cell Mol Life Sci 2002; 59: 1706-1713.
89. Kotler M, Rodriguez C, Sainz RM, Antolin I, Menendez-Pelaez A. Melatonin increases gene expression for antioxidant enzymes in rat brain cortex. J Pineal Res 1998; 24: 83-89.
90. Muralikrishnan D, Mohanakumar KP. Neuroprotection by bromocriptine against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity in mice. FASEB J 1998; 12: 905-912.
91. Thomas B, Muralikrishnan D, Mohanakumar KP. In vivo hydroxyl radical generation in the striatum following systemic administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridi ne in mice. Brain Res 2000; 852: 221-224.
92. Thiff ault C, Aumont N, Quirion R, Poirier J. Effect of MPTP and L-deprenyl on antioxidant enzymes and lipid peroxidation levels in mouse brain. J Neurochem 1995; 65: 2725-2733.
93. Mayo JC, Sainz RM, Uria H, Antolin I, Esteban MM, Rodriguez C. Melatonin prevents apoptosis induced by 6-hydroxydopamine in neuronal cells: implications for Parkinson's disease. J Pineal Res 1998; 24: 179-192.
94. Morgan WW, Nelson JF. Chronic administration of pharmacological levels of melatonin does not ameliorate the MPTPinduced degeneration of the nigrostriatal pathway. Brain Res 2001; 921: 115-121.
95. van der Schyf CJ, Castagnoli K, Palmer S, Hazelwood L, Castagnoli N, Jr. Melatonin fails to protect against long-term MPTP-induced dopamine depletion in mouse striatum. Neurotox Res 2000; 1: 261-269.
96. Tapias V, Cannon JR, Greenamyre JT. Melatonin treatment potentiates neurodegeneration in a rat rotenone Parkinson's disease model. J Neurosci Res 2010; 88: 420-427.
97. Horstink MW, Morrish PK. Preclinical diagnosis of Parkinson's disease. Adv Neurol 1999; 80: 327-333.
98. Uz T, Arslan AD, Kurtuncu M, Imbesi M, Akhisaroglu M, Dwivedi Y, et al. The regional and cellular expression profile of the melatonin receptor MT1 in the central dopaminergic system. Brain Res Mol Brain Res 2005; 136: 45-53.