Evaluation of the oxidation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) to toxic pyridinium cations by monoamine oxidase (MAO) enzymes and its use to search for new MAO inhibitors and protective agents

References

• Youdim MB, Edmondson D, Tipton KF. The therapeutic potential of monoamine oxidase inhibitors. Nat Rev Neurosci 2006;7:295–309.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Vindis C, Séguélas MH, 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.
   PubMedGoogle Scholar
• Siddiqui A, Mallajosyula JK, Rane A, Andersen JK. Ability to delay neuropathological events associated with astrocytic MAO-B increase in a Parkinsonian mouse model: implications for early intervention on disease progression. Neurobiol Dis 2010;40:444–448.
   PubMed Web of Science ®Google Scholar
• Youdim MB, Lavie L. Selective MAO-A and B inhibitors, radical scavengers and nitric oxide synthase inhibitors in Parkinson’s disease. Life Sci 1994;55:2077–2082.
   PubMed Web of Science ®Google Scholar
• Mallajosyula JK, Kaur D, Chinta SJ, Rajagopalan S, Rane A, Nicholls DG et al. MAO-B elevation in mouse brain astrocytes results in Parkinson’s pathology. PLoS ONE 2008;3:e1616.
   PubMed Web of Science ®Google Scholar
• Drechsel DA, 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.
   PubMed Web of Science ®Google Scholar
• Langston JW, Ballard P, Tetrud JW, Irwin I. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 1983;219:979–980.
   PubMed Web of Science ®Google Scholar
• Jackson-Lewis V, Przedborski S. Protocol for the MPTP mouse model of Parkinson’s disease. Nat Protoc 2007;2:141–151.
   PubMed Web of Science ®Google Scholar
• Langston JW, Irwin I, Langston EB, Forno LS. 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.
   PubMed Web of Science ®Google Scholar
• Herraiz T, Guillén 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.
   PubMedGoogle Scholar
• Thomas B, Saravanan KS, Mohanakumar KP. 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.
   PubMed Web of Science ®Google Scholar
• Seet RC, Lee CY, Lim EC, Tan JJ, Quek AM, Chong WL et al. Oxidative damage in Parkinson disease: Measurement using accurate biomarkers. Free Radic Biol Med 2010;48:560–566.
   PubMed Web of Science ®Google Scholar
• González-Polo RA, Soler G, Rodríguezmartín A, Morán JM, Fuentes JM. Protection against MPP+ neurotoxicity in cerebellar granule cells by antioxidants. Cell Biol Int 2004;28:373–380.
   PubMedGoogle Scholar
• Herraiz T, Guillén H, Arán VJ, Idle JR, Gonzalez FJ. 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.
   PubMed Web of Science ®Google Scholar
• Hauptmann N, Grimsby J, Shih JC, Cadenas E. The metabolism of tyramine by monoamine oxidase A/B causes oxidative damage to mitochondrial DNA. Arch Biochem Biophys 1996;335:295–304.
   PubMed Web of Science ®Google Scholar
• Heikkila RE, Manzino L, Cabbat FS, Duvoisin RC. Protection against the dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine by monoamine oxidase inhibitors. Nature 1984;311:467–469.
   PubMed Web of Science ®Google Scholar
• Sonsalla PK, Wong LY, 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.
   PubMed Web of Science ®Google Scholar
• Herraiz T, Arán VJ, 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.
   PubMed Web of Science ®Google Scholar
• Reznichenko L, Kalfon L, Amit T, Youdim MB, Mandel SA. Low dosage of rasagiline and epigallocatechin gallate synergistically restored the nigrostriatal axis in MPTP-induced parkinsonism. Neurodegener Dis 2010;7:219–231.
   PubMed Web of Science ®Google Scholar
• Bolasco A, Carradori S, Fioravanti R. Focusing on new monoamine oxidase inhibitors. Expert Opin Ther Pat 2010;20:909–939.
   PubMed Web of Science ®Google Scholar
• Desideri N, Bolasco A, Fioravanti R, Monaco LP, Orallo F, Yáñez M et al. Homoisoflavonoids: natural scaffolds with potent and selective monoamine oxidase-B inhibition properties. J Med Chem 2011;54:2155–2164.
   PubMed Web of Science ®Google Scholar
• Chimenti F, Secci D, Bolasco A, Chimenti P, Granese A, Carradori S et al. Synthesis, semipreparative HPLC separation, biological evaluation, and 3D-QSAR of hydrazothiazole derivatives as human monoamine oxidase B inhibitors. Bioorg Med Chem 2010;18:5063–5070.
   PubMed Web of Science ®Google Scholar
• Deeb O, Alfalah S, Clare BW. QSAR of aromatic substances: MAO inhibitory activity of xanthone derivatives. J Enzyme Inhib Med Chem 2007;22:277–286.
   PubMed Web of Science ®Google Scholar
• Dar A, Khan KM, Ateeq HS, Khan S, Rahat S, Perveen S et al. Inhibition of monoamine oxidase-A activity in rat brain by synthetic hydrazines: structure-activity relationship (SAR). J Enzyme Inhib Med Chem 2005;20:269–274.
   PubMed Web of Science ®Google Scholar
• Pisani L, Muncipinto G, Miscioscia TF, Nicolotti O, Leonetti F, Catto M et al. Discovery of a novel class of potent coumarin monoamine oxidase B inhibitors: development and biopharmacological profiling of 7-[(3-chlorobenzyl)oxy]-4-[(methylamino)methyl]-2H-chromen-2-one methanesulfonate (NW-1772) as a highly potent, selective, reversible, and orally active monoamine oxidase B inhibitor. J Med Chem 2009;52:6685–6706.
   PubMed Web of Science ®Google Scholar
• Zhou M, Panchuk-Voloshina N. A one-step fluorometric method for the continuous measurement of monoamine oxidase activity. Anal Biochem 1997;253:169–174.
   PubMed Web of Science ®Google Scholar
• Albers AE, Rawls KA, Chang CJ. Activity-based fluorescent reporters for monoamine oxidases in living cells. Chem Commun (Camb) 2007;44:4647–4649.
   PubMedGoogle Scholar
• Yan Z, Caldwell GW, Zhao B, Reitz AB. A high-throughput monoamine oxidase inhibition assay using liquid chromatography with tandem mass spectrometry. Rapid Commun Mass Spectrom 2004;18:834–840.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Hu K, Zhang L, Li X, Zhao S. Rapid screening of monoamine oxidase B inhibitors in natural extracts by capillary electrophoresis after enzymatic reaction at capillary inlet. J Chromatogr B Analyt Technol Biomed Life Sci 2010;878:3156–3160.
   PubMedGoogle Scholar
• Shinka T, Castagnoli N Jr, Wu EY, Hoag MK, Trevor AJ. Cation-exchange high-performance liquid chromatography assay for the nigrostriatal toxicant 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine and its monoamine oxidase B generated metabolites in brain tissues. J Chromatogr 1987;398:279–287.
   PubMed Web of Science ®Google Scholar
• Herraiz T, Guillén H. Inhibition of the bioactivation of the neurotoxin MPTP by antioxidants, redox agents and monoamine oxidase inhibitors. Food Chem Toxicol 2011;49:1773–1781.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Di Monte DA, Wu EY, Irwin I, Delanney LE, Langston JW. Biotransformation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in primary cultures of mouse astrocytes. J Pharmacol Exp Ther 1991;258:594–600.
   PubMedGoogle Scholar
• Heikkila RE, Kindt MV, Sonsalla PK, Giovanni A, Youngster SK, McKeown KA et al. Importance of monoamine oxidase A in the bioactivation of neurotoxic analogs of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc Natl Acad Sci USA 1988;85:6172–6176.
   PubMed Web of Science ®Google Scholar
• Youngster SK, McKeown KA, Jin YZ, Ramsay RR, Heikkila RE, Singer TP. Oxidation of analogs of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine by monoamine oxidases A and B and the inhibition of monoamine oxidases by the oxidation products. J Neurochem 1989;53:1837–1842.
   PubMed Web of Science ®Google Scholar
• Wernicke C, Hellmann J, Zieba B, Kuter K, Ossowska K, Frenzel M et al. 9-Methyl-β-carboline has restorative effects in an animal model of Parkinson’s disease. Pharmacol Rep 2010;62:35–53.
   PubMed Web of Science ®Google Scholar
• Kim DH, Jang YY, Han ES, Lee CS. Protective effect of harmaline and harmalol against dopamine- and 6-hydroxydopamine-induced oxidative damage of brain mitochondria and synaptosomes, and viability loss of PC12 cells. Eur J Neurosci 2001;13:1861–1872.
   PubMedGoogle Scholar
• Cheng Y, Prusoff WH. Relationship between the inhibition constant (Ki) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 1973;22:3099–3108.
   PubMed Web of Science ®Google Scholar
• Fowler JS, Volkow ND, Wang GJ, Pappas N, Logan J, MacGregor R et al. Inhibition of monoamine oxidase B in the brains of smokers. Nature 1996;379:733–736.
   PubMed Web of Science ®Google Scholar
• Fowler JS, Logan J, Wang GJ, Volkow ND. Monoamine oxidase and cigarette smoking. Neurotoxicology 2003;24:75–82.
   PubMed Web of Science ®Google Scholar
• Pryor WA. Cigarette smoke radicals and the role of free radicals in chemical carcinogenicity. Environ Health Perspect 1997;105 Suppl 4:875–882.
   PubMedGoogle Scholar
• Nolen WA, Hoencamp E, Bouvy PF, Haffmans PM. Reversible monoamine oxidase-A inhibitors in resistant major depression. Clin Neuropharmacol 1993;16 Suppl 2:S69–S76.
   PubMed Web of Science ®Google Scholar
• Castagnoli K, Palmer S, Anderson A, Bueters T, Castagnoli N Jr. 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.
   PubMed Web of Science ®Google Scholar
• Herraiz T. β-Carboline alkaloids.(2008) In Gilbert, J., S¸enyuva, HZ., eds. Bioactive Compounds in Foods. UK: Blackwell, Oxford, 199–218.
   Google Scholar
• Kim H, Sablin SO, Ramsay RR. Inhibition of monoamine oxidase A by β-carboline derivatives. Arch Biochem Biophys 1997;337:137–142.
   PubMed Web of Science ®Google Scholar
• Krueger MJ, Mazouz F, Ramsay RR, Milcent R, Singer TP. Dramatic species differences in the susceptibility of monoamine oxidase B to a group of powerful inhibitors. Biochem Biophys Res Commun 1995;206:556–562.
   PubMed Web of Science ®Google Scholar
• Novaroli L, Daina A, Favre E, Bravo J, Carotti A, Leonetti F et al. Impact of species-dependent differences on screening, design, and development of MAO B inhibitors. J Med Chem 2006;49:6264–6272.
   PubMed Web of Science ®Google Scholar