Inhibition of the bioactivation of the neurotoxin MPTP by antioxidants, redox agents and monoamine oxidase inhibitors

Food and Chemical Toxicology

Volumn 49, Issue 8, 2011, Pages 1773-1781

  Herraiz, Tomás ^a   Guillén, Hugo ^a  

^a INSTITUTE OF FOOD SCIENCE   (Spain)

Author keywords

Antioxidants; MAO B inhibitors; Mitochondria; Monoamine oxidase; MPTP neurotoxin; Redox agents

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 5 BROMOINDAZOLE; 5 NITROINDAZOLE; 6 BROMOINDAZOLE; 9 METHYL BETA CARBOLINE; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; ANTIOXIDANT; BETA CARBOLINE; CATECHIN; HARMALINE; HARMINE; MELATONIN; MENADIONE; METHYLENE BLUE; MONOAMINE OXIDASE INHIBITOR; QUERCETIN; RESVERATROL; SELEGILINE; TRYPTOLINE; UNCLASSIFIED DRUG;

ARTICLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG STRUCTURE; HUMAN; HUMAN CELL; IC 50; INHIBITION KINETICS; LIVER MITOCHONDRION; NEUROPROTECTION; NEUROTOXICITY; OXIDATIVE STRESS;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANTIOXIDANTS; CARBOLINES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HARMINE; HUMANS; INDAZOLES; MASS SPECTROMETRY; METHYLENE BLUE; MITOCHONDRIA; MONOAMINE OXIDASE; MONOAMINE OXIDASE INHIBITORS; NEUROPROTECTIVE AGENTS; NEUROTOXINS; OXIDATION-REDUCTION; SELEGILINE;

EID: 79958762778     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2011.04.026     Document Type: Article

References (71)

1. Adams J.J.D., Klaidman L.K., Leung A.C. MPP+ and MPDP+ induced oxygen radical formation with mitochondrial enzymes. Free Radic. Biol. Med. 1993, 15:181-186.
2. Atamna H., Nguyen A., Schultz C., Boyle K., Newberry J., Kato H., Ames B.N. Methylene blue delays cellular senescence and enhances key mitochondrial biochemical pathways. Faseb J. 2008, 22:703-712.
3. Ben-Shlomo Y., Bhatia K. Using monoamine oxidase type B inhibitors in Parkinson's disease: They are effective and safe, at least when used alone. Brt. Med. J. 2004, 329:581-582.
4. Borah A., Mohanakumar K.P. Melatonin inhibits 6-hydroxydopamine production in the brain to protect against experimental parkinsonism in rodents. J. Pineal Res. 2009, 47:293-300.
5. Castagnoli K., Murugesan T. Tobacco leaf, smoke and smoking, MAO inhibitors, Parkinson's disease and neuroprotection; Are there links?. Neurotoxicology 2004, 25:279-291.
6. Castagnoli K., Palmer S., Anderson A., Bueters T., Castagnoli N. The neuronal nitric oxide synthase inhibitor 7-nitroindazole also inhibits the monoamine oxidase-B-catalyzed oxidation of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine. Chem. Res. Toxicol. 1997, 10:364-368.
7. Chen L.J., Gao Y.Q., Li X.J., Shen D.H., Sun F.Y. Melatonin protects against MPTP/MPP+-induced mitochondrial DNA oxidative damage in vivo and in vitro. J. Pineal Res. 2005, 39:34-42.
8. Chiba K., Trevor A., Castagnoli N. Metabolism of the neurotoxic tertiary amine, MPTP, by brain monoamine oxidase. Biochem. Biophys. Res. Commun. 1984, 120:574-578.
9. Chimenti F., Cottiglia F., Bonsignore L., Casu L., Casu M., Floris C., Secci D., Bolasco A., Chimenti P., Granese A., Befani O., Turini P., Alcaro S., Ortuso F., Trombetta G., Loizzo A., Guarino I. Quercetin as the active principle of Hypericum hircinum exerts a selective inhibitory activity against MAO-A: Extraction, biological analysis, and computational study. J. Nat. Prod. 2006, 69:945-949.
10. Chiueh C.C., Krishna G., Tulsi P., Obata T., Lang K., Huang S.J., Murphy D.L. Intracranial microdialysis of salicylic acid to detect hydroxyl radical generation through dopamine autooxidation in the caudate nucleus. Effects of MPP+. Free Radic. Biol. Med 1992, 13:581-583.
11. Choi W.T., Youn Y.C., Han E.S., Lee C.S. Protective effect of 1-methylated beta-carbolines against 3-morpholinosydnonimine-induced mitochondrial damage and cell viability loss in PC12 cells. Neurochem. Res. 2004, 29:1807-1816.
12. Cohen G., Farooqui R., Kesler N. Parkinson disease: A new link between monoamine oxidase and mitochondrial electron flow. Proc. Natl. Acad. Sci. USA 1997, 94:4890-4894.
13. Cortes A., Cascante M., Cardenas M.L., Cornish-Bowden A. Relationships between inhibition constants, inhibitor concentrations for 50% inhibition and types of inhibition: new ways of analysing data. Biochem. J. 2001, 357:263-268.
14. Desvignes C., Bert L., Vinet L., Denoroy L., Renaud B., Lambas-Senas L. Evidence that the neuronal nitric oxide synthase inhibitor 7-nitroindazole inhibits monoamine oxidase in the rat: in vivo effects on extracellular striatal dopamine and 3, 4-dihydroxyphenylacetic acid. Neurosci. Lett. 1999, 261:175-178.
15. Di Monte D.A., Royland J.E., Anderson A., Castagnoli K., Castagnoli N., Langston J.W. Inhibition of monoamine oxidase contributes to the protective effect of 7-nitroindazole against MPTP neurotoxicity. J. Neurochem. 1997, 69:1771-1773.
16. Drechsel D.A., Patel M. Role of reactive oxygen species in the neurotoxicity of environmental agents implicated in Parkinson's disease. Free Radic. Biol. Med. 2008, 44:1873-1886.
17. Dreiseitel A., Korte G., Schreier P., Oehme A., Locher S., Domani M., Hajak G., Sand P.G. Berry anthocyanins and their aglycons inhibit monoamine oxidases A and B. Pharmacol. Res. 2009, 59:306-311.
18. Fowler J.S., Volkow N.D., Wang G.J., Pappas N., Logan J., MacGregor R., Alexoff D., Shea C., Schlyer D., Wolf A.P., Warner D., Zezulkova I., Cilento R. Inhibition of monoamine oxidase B in the brains of smokers. Nature 1996, 379:733-736.
19. Fuller R.W., Hemrickluecke S.K. Influence of selective, reversible inhibitors of monoamine oxidase on the prolonged depletion of striatal dopamine by 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine in mice. Life Sci. 1985, 37:1089-1096.
20. Gearhart D.A., Collins M.A., Lee J.M., Neafsey E.J. Increased β-carboline 9N-methyltransferase activity in the frontal cortex in Parkinson's disease. Neurobiol. Dis. 2000, 7:201-211.
21. Gonzalez-Polo R.A., Soler G., Rodriguez Martin A., Moran J.M., Fuentes J.M. Protection against MPP+ neurotoxicity in cerebellar granule cells by antioxidants. Cell Biol. Int. 2004, 28:373-380.
22. Gupta M., Gupta B.K., Thomas R., Bruemmer V., Sladek J.R., Felten D.L. Aged mice are more sensitive to 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine treatment than young adults. Neurosci. Lett. 1986, 70:326-331.
23. Hantraye P., Brouillet E., Ferrante R., Palfi S., Dolan R., Matthews R.T., Beal M.F. Inhibition of neuronal nitric oxide synthase prevents MPTP-induced parkinsonism in baboons. Nat. Med. 1996, 2:1017-1021.
24. Harvey B.H., Duvenhage I., Viljoen F., Scheepers N., Malan S.F., Wegener G., Brink C.B., Petzer J.P. Role of monoamine oxidase, nitric oxide synthase and regional brain monoamines in the antidepressant-like effects of methylene blue and selected structural analogues. Biochem. Pharmacol. 2010, 80:1580-1591.
25. Hauptmann N., Grimsby J., Shih J.C., Cadenas E. The metabolism of tyramine by monoamine oxidase A/B causes oxidative damage to mitochondrial DNA. Arch. Biochem. Biophys. 1996, 335:295-304.
26. Heikkila R.E., Manzino L., Cabbat F.S., Duvoisin R.C. Protection against the dopaminergic neurotoxicity of 1-methyl-4-phenyl-1, 2, 5, 6-tetrahydropyridine by monoamine oxidase inhibitors. Nature 1984, 311:467-469.
27. Henchcliffe C., Beal M.F. Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nat. Clin. Pract. Neurol. 2008, 4:600-609.
28. Herraiz T. Relative exposure to β-carbolines norharman and harman from foods and tobacco smoke. Food Addit. Contam. 2004, 21:1041-1050.
29. Herraiz T., Arán V.J., Guillén H. Nitroindazole compounds inhibit the oxidative activation of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP) neurotoxin to neurotoxic pyridinium cations by human monoamine oxidase (MAO). Free Radic. Res. 2009, 43:975-984.
30. Herraiz T., Chaparro C. Human monoamine oxidase is inhibited by tobacco smoke: β-carboline alkaloids act as potent and reversible inhibitors. Biochem. Biophys. Res. Commun. 2005, 326:378-386.
31. Herraiz T., Chaparro C. Analysis of monoamine oxidase enzymatic activity by reversed-phase high performance liquid chromatography and inhibition by β-carboline alkaloids occurring in foods and plants. J. Chromatogr. A 2006, 1120:237-243.
32. Herraiz T., Chaparro C. Human monoamine oxidase enzyme inhibition by coffee and β-carbolines norharman and harman isolated from coffee. Life Sci. 2006, 78:795-802.
33. Herraiz T., Galisteo J. Tetrahydro-β-carboline alkaloids that occur in foods and biological systems act as radical scavengers and antioxidants in the ABTS assay. Free Radic. Res. 2002, 36:923-928.
34. Herraiz T., González D., Ancín-Azpilicueta C., Arán V.J., Guillén H. Beta-Carboline alkaloids in Peganum harmala and inhibition of human monoamine oxidase (MAO). Food Chem. Toxicol. 2010, 48:839-845.
35. Herraiz T., Guillén H., Arán V.J., Idle J.R., Gonzalez F.J. Comparative aromatic hydroxylation and N-demethylation of MPTP neurotoxin and its analogs, N-methylated β-carboline and isoquinoline alkaloids, by human cytochrome P450 2D6. Toxicol. Appl. Pharmacol. 2006, 216:387-398.
36. Herraiz T., Guillen H., Galisteo J. N-methyltetrahydro-β-carboline analogs of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP) neurotoxin are oxidized to neurotoxic β-carbolinium cations by heme peroxidases. Biochem. Biophys. Res. Commun. 2007, 356:118-123.
37. Jackson-Lewis V., Przedborski S. Protocol for the MPTP mouse model of Parkinson's disease. Nat. Protoc. 2007, 2:141-151.
38. Jenner P. Oxidative stress in Parkinson's disease. Ann. Neurol. 2003, 53:S26-S36.
39. Kalivendi S.V., Yedlapudi D., Hillard C.J., Kalyanaraman B. Oxidants induce alternative splicing of [α]-synuclein: Implications for Parkinson's disease. Free Radic. Biol. Med. 2010, 48:377-383.
40. Langston J.W., Ballard P., Tetrud J.W., Irwin I. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 1983, 219:979-980.
41. Langston J.W., Irwin I., Langston E.B., Forno L.S. 1-Methyl-4-phenylpyridinium ion (MPP+): Identification of a metabolite of MPTP, a toxin selective to the substantia nigra. Neurosci. Lett. 1984, 48:87-92.
42. Lee, C. S., Han, E. S., Jang, Y. Y., Han, J. H., Ha, H. W. and Kim, D. E., 2000. Protective effect of harmalol and harmaline on MPTP neurotoxicity in the mouse and dopamine-induced damage of brain mitochondria and PC12 cells. 75, 521-531.
43. Lee D.-H., Kim C.-S., Lee Y.J. Astaxanthin protects against MPTP/MPP+-induced mitochondrial dysfunction and ROS production in vivo and in vitro. Food Chem Toxicol. 2011, 49:271-280.
44. Lee M.-H., Lin R.-D., Shen L.-Y., Yang L.-L., Yen K.-Y., Hou W.-C. Monoamine oxidase B and free radical scavenging activities of natural flavonoids in Melastoma candidum D. Don. J. Agric. Food Chem. 2001, 49:5551-5555.
45. Lu K.-T., Ko M.-C., Chen B.-Y., Huang J.-C., Hsieh C.-W., Lee M.-C., Chiou R.Y.Y., Wung B.-S., Peng C.-H., Yang Y.-L. Neuroprotective effects of resveratrol on MPTP-induced neuron loss mediated by free radical scavenging. J. Agric. Food Chem. 2008, 56:6910-6913.
46. Mallajosyula J.K., Kaur D., Chinta S.J., Rajagopalan S., Rane A., Nicholls D.G., Di Monte D.A., Macarthur H., Andersen J.K. MAO-B elevation in mouse brain astrocytes results in Parkinson's pathology. PLoS One 2008, 3:e1616.
47. Mandel S., Youdim M.B.H. Catechin polyphenols: neurodegeneration and neuroprotection in neurodegenerative diseases. Free Radic. Biol. Med. 2004, 37:304-317.
48. Markey S.P., Johannessen J.N., Chiueh C.C., Burns R.S., Herkenham M.A. Intraneuronal generation of a pyridinium metabolite may cause drug-induced Parkinsonism. Nature 1984, 311:464-467.
49. Matsubara K., Gonda T., Sawada H., Uezono T., Kobayashi Y., Kawamura T., Ohtaki K., Kimura K., Akaike A. Endogenously occurring β-carboline induces parkinsonism in nonprimate animals: A possible causative protoxin in idiopathic Parkinson's disease. J. Neurochem. 1998, 70:727-735.
50. Naylor G.J., Smith A.H.W., Connelly P. A controlled trial of methylene blue in severe depressive illness. Biol. Psychiatry 1987, 22:657-659.
51. Oxenkrug G.R., Sablin S.O., Requintina P.J. Effect of methylene blue and related redox dyes on monoamine oxidase activity; rat pineal content of N-acetylserotonin, melatonin, and related indoles; and righting reflex in melatonin-primed frogs. Ann. New York Acad. Sci. 2007, 1122:245-252.
52. Parain K., Hapdey C., Rousselet E., Marchand V., Dumery B., Hirsch E.C. Cigarette smoke and nicotine protect dopaminergic neurons against the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine Parkinsonian toxin. Brain Res. 2003, 984:224-232.
53. Ramsay R.R., Dunford C., Gillman P.K. Methylene blue and serotonin toxicity: inhibition of monoamine oxidase A (MAO A) confirms a theoretical prediction. Br. J. Pharmacol. 2007, 152:946-951.
54. Reznichenko L., Kalfon L., Amit T., Youdim M.B.H., Mandel S.A. Low dosage of rasagiline and epigallocatechin gallate synergistically restored the nigrostriatal axis in MPTP-induced Parkinsonism. Neurodegener. Dis. 2010, 7:219-231.
55. Rojas J.C., Simola N., Kermath B.A., Kane J.R., Schallert T., Gonzalez-Lima F. Striatal neuroprotection with methylene blue. Neuroscience 2009, 163:877-889.
56. Rommelspacher H., Meier-Henco M., Smolka M., Kloft C. The levels of norharman are high enough after smoking to affect monoamineoxidase B in platelets. Eur. J. Pharmacol. 2002, 441:115-125.
57. Saaby L., Rasmussen H.B., Jager A.K. MAO-A inhibitory activity of quercetin from Calluna vulgaris (L.) hull. J. Ethnopharmacol. 2009, 121:178-181.
58. Seet R.C.S., Lee C.-Y.J., Lim E.C.H., Tan J.J.H., Quek A.M.L., Chong W.-L., Looi W.-F., Huang S.-H., Wang H., Chan Y.-H., Halliwell B. Oxidative damage in Parkinson disease: Measurement using accurate biomarkers. Free Radic. Biol. Med. 2010, 48:560-566.
59. Smith T.S., Bennett J.P. Mitochondrial toxins in models of neurodegenerative diseases.1. In vivo brain hydroxyl radical production during systemic MPTP treatment or following microdialysis infusion of methylpyridinium or azide ions. Brain Res. 1997, 765:183-188.
60. Sonsalla P.K., Wong L.Y., Winnik B., Buckley B. The antiepileptic drug zonisamide inhibits MAO-B and attenuates MPTP toxicity in mice. Clinical relevance. Exp. Neurol. 2010, 221:329-334.
61. Thomas B., Saravanan K.S., Mohanakumar K.P. In vitro and in vivo evidences that antioxidant action contributes to the neuroprotective effects of the neuronal nitric oxide synthase and monoamine oxidase-B inhibitor, 7-nitroindazole. Neurochem. Int. 2008, 52:990-1001.
62. Vindis C., Seguelas M.H., Bianchi P., Parini A., Cambon C. Monoamine oxidase B induces ERK-dependent cell mitogenesis by hydrogen peroxide generation. Biochem. Biophys. Res Commun. 2000, 271:181-185.
63. Watanabe H., Muramatsu Y., Kurosaki R., Michimata M., Matsubara M., Imai Y., Araki T. Protective effects of neuronal nitric oxide synthase inhibitor in mouse brain against MPTP neurotoxicity: an immunohistological study. Eur. Neuropsychopharmacol. 2004, 14:93-104.
64. Wei Q., Yeung M., Jurma O.P., Andersen J.K. Genetic elevation of monoamine oxidase levels in dopaminergic PC12 cells results in increased free radical damage and sensitivity to MPTP. J. Neurosci. Res. 1996, 46:666-673.
65. Wernicke C., Hellmann J., Zieba B., Kuter K., Ossowska K., Frenzel M., Dencher N.A., Rommelspacher H. 9-Methyl-beta-carboline has restorative effects in an animal model of Parkinson's disease. Pharmacol. Rep. 2010, 62:35-53.
66. Wernicke C., Schott Y., Enzensperger C., Schulze G., Lehmann J., Rommelspacher H. Cytotoxicity of beta-carbolines in dopamine transporter expressing cells: Structure-activity relationships. Biochem. Pharmacol. 2007, 74:1065-1077.
67. Yamada M., Yasuhara H. Clinical pharmacology of MAO inhibitors: Safety and future. Neurotoxicology 2004, 25:215-221.
68. Youdim M.B.H., Bar Am O., Yogev-Falach M., Weinreb O., Maruyama W., Naoi M., Amit T. Rasagiline: neurodegeneration, neuroprotection, and mitochondrial permeability transition. J. Neurosci. Res. 2005, 79:172-179.
69. Youdim M.B.H., Edmondson D., Tipton K.F. The therapeutic potential of monoamine oxidase inhibitors. Nat. Rev. Neurosci. 2006, 7:295-309.
70. Youdim M.B.H., Lavie L. Selective MAO-A and MAO-B inhibitors, radical scavengers and nitric oxide synthase inhibitors in Parkinsońs disease. Life Sci 1994, 55:2077-2082.
71. 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. 1993, 268:16504-16512.