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 Radical Research

Volumn 43, Issue 10, 2009, Pages 975-984

  Herraiz, Tomás ^a   Arán, Vicente J ^b   Guillén, Hugo ^a  

^a INSTITUTO DE FERMENTACIONES INDUSTRIALES CSIC   (Spain)

^b INSTITUTO DE QUÍMICA MÉDICA   (Spain)

Author keywords

Antioxidants; Hydroxyl radical scavengers; Monoamine oxidase inhibition; MPTP neurotoxin; Neuroprotection; Nitroindazoles; Parkinson's disease

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 2,3 DIHYDRO 1 METHYL 4 PHENYLPYRIDINIUM; 5 NITROINDAZOLE; 6 NITROINDAZOLE; 7 NITROINDAZOLE; AMINE OXIDASE (FLAVIN CONTAINING); AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; HYDROXYL RADICAL; INDAZOLE DERIVATIVE; MONOAMINE OXIDASE A INHIBITOR; MONOAMINE OXIDASE B INHIBITOR; NITRIC OXIDE SYNTHASE INHIBITOR; PYRIDINIUM DERIVATIVE; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; ARTICLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; ENZYME INHIBITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IC 50; ISOMER; MITOCHONDRION; NEUROPROTECTION;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; FREE RADICAL SCAVENGERS; HUMANS; INDAZOLES; MITOCHONDRIA, LIVER; MONOAMINE OXIDASE; MONOAMINE OXIDASE INHIBITORS; NEUROPROTECTIVE AGENTS; OXIDATION-REDUCTION; PYRIDINIUM COMPOUNDS;

ANIMALIA;

EID: 70450228608     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.1080/10715760903159170     Document Type: Article

References (63)

1. Kalgutkar AS, Dalvie DK, Castagnoli N, Taylor TJ. Interactions of nitrogen-containing xenobiotics with monoamine oxidase (MAO) isozymes A and B: SAR studies on MAO substrates and inhibitors. Chem Res Toxicol 2001;14:1139-1162.
2. Youdim MBH, Edmondson D, Tipton KF. The therapeutic potential of monoamine oxidase inhibitors. Nat Rev Neurosci 2006;7:295-309.
3. Shih JC, Chen K, Ridd MJ. Monoamine oxidase: from genes to behavior. Ann Rev Neurosci 1999;22:197-217.
4. Yamada M, Yasuhara H. Clinical pharmacology of MAO inhibitors: safety and future. Neurotoxicology 2004;25: 215-221.
5. Samantaray S, Knaryan VH, Butler JT, Ray SK, Banik NL. Spinal cord degeneration in C57BL/6N mice following induction of experimental parkinsonism with MPTP. J Neurochem 2008;104:1309-1320.
6. Lee DW, Sohn HO, Lim HB, Lee YG, Kim YS, Carp RI, Wisniewski HM. Alteration of free radical metabolism in the brain of mice infected with scrapie agent. Free Radic Res 1999;30:499-507.
7. 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
8. 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.
9. Youdim MBH, Lavie L. Selective MAO-A and MAO-B inhibitors, radical scavengers and nitric oxide synthase inhibitors in Parkinson's disease. Life Sci 1994;55: 2077-2082.
10. 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.
11. Herraiz T, Guillen H, Aran VJ, Idle JR, Gonzalez FJ. Comparative aromatic hydroxylation and N-demethylation of MPTP neurotoxin and its analogs, N-methylated P-carbo-line and isoquinoline alkaloids, by human cytochrome P450 2D6. Toxicol Appl Pharmacol 2006;216:387-398.
12. Herraiz T, Guillen H, Galisteo J. N-Methyltetrahydro-P-carboline analogs of 1-methyl-4-phenyl-1,2,3,6-tetrahydro-pyridine (MPTP) neurotoxin are oxidized to neurotoxic β-carbolinium cations by heme peroxidases. Biochem Biophys Res Commun 2007;356:118-123.
13. 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.
14. Davis GC, Williams AC, Markey SP, Ebert MH, Caine ED, Reichert CM, Kopin IJ. Chronic Parkinsonism secondary to intravenous injection of meperidine analogs. Psychiatry Res 1979;1:249-254.
15. Markey SP, Johannessen JN, Chiueh CC, Burns RS, Herken-ham MA. Intraneuronal generation of a pyridinium metabolite may cause drug-induced Parkinsonism. Nature 1984;311:464-467
16. Chiueh CC, Krishna G, Tulsi P, Obata T, Lang K, Huang SJ, Murphy DL. Intracranial microdialysis of salicylic acid to detect hydroxyl radical generation through dopamine auto-oxidation in the caudate nucleus. Effects of MPP+. Free Radic Biol Med 1992;13:581-583.
17. Obata T Role of hydroxyl radical formation in neurotoxicity as revealed by in vivo free radical trapping. Toxicol Lett 2002;132:83-93.
18. 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.
19. Gonzalez-Polo RA, Soler G, Rodriguez Martin A, Moran JM, Fuentes JM. Protection against MPP+ neurotoxicity in cerebellar granule cells by antioxidants. Cell Biol Int 2004;28:373-380. (Pubitemid 38748927)
20. Jackson-Lewis V, Przedborski S. Protocol for the MPTP mouse model of Parkinson's disease. Nat Protoc 2007;2: 141-151.
21. Nolen WA, Hoencamp E, Bouvy PF, Haffmans PMJ. Reversible monoamine oxidase-A inhibitors in resistant major depression. Clin Neuropharmacol 1993;16:S69-S76.
22. 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. BMJ 2004;329:581-582.
23. Herraiz T, Chaparro C. Human monoamine oxidase is inhibited by tobacco smoke: P-carboline alkaloids act as potent and reversible inhibitors. Biochem Biophys Res Commun 2005;326:378-386.
24. Castagnoli K, Murugesan T Tobacco leaf, smoke and smoking, MAO inhibitors, Parkinson's disease and neuroprotection; are there links? Neurotoxicology 2004;25:279-291.
25. Fowler JS, Volkow ND, Wang GJ, Pappas N, Logan J, Shea C, Alexoff D, MacGregor RR, Schlyer DJ, Zezulkova I, Wolf AP. Brain monoamine oxidase A inhibition in cigarette smokers. Proc Natl Acad Sci USA 1996;93:14065-14069. (Pubitemid 26424246)
26. Fowler JS, Volkow ND, Wang GJ, Pappas N, Logan J, MacGregor R, Alexoff D, Shea C, Schlyer D, Wolf AP, Warner D, Zezulkova I, Cilento R. Inhibition of monoamine oxidase B in the brains of smokers. Nature 1996;379: 733-736. (Pubitemid 26061736)
27. Parain K, Hapdey C, Rousselet E, Marchand V, Dumery B, Hirsch EC. Cigarette smoke and nicotine protect dopaminergic neurons against the 1-methyl-4-phenyl-1,2,3,6-tetra-hydropyridine Parkinsonian toxin. Brain Res 2003;984: 224-232.
28. 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.
29. Grandi T, Sparatore F, Gnerre C, Crivori P, Carrupt PA, Testa B. Monoamine oxidase inhibitory properties of some benzazoles: structure-activity relationships. AAPS Pharmsci 1999;1:1-.
30. Cerecetto H, Gerpe A, Gonzalez M, Aran VJ, Ochoa de Ocariz C. Pharmacological properties of indazole derivatives: recent developments. Mini-Rev Med Chem 2005;5:869-878. (Pubitemid 41300735)
31. Babbedge RC, Blandward PA, Hart SL, Moore PK. Inhibition of rat cerebellar nitric oxide synthase by 7-nitroindazole and related substituted indazoles. Br J Pharmacol 1993;110: 225-228.
32. Wolff DJ, Gribin BJ. The Inhibition of the constitutive and inducible nitric-oxide synthase isoforms by indazole agents. Arch Biochem Biophys 1994;311:300-306.
33. Schulz JB, Matthews RT, Muqit MMK, Browne SE, Beal MF. Inhibition of neuronal nitric oxide synthase by 7-nitroindazole protects against MPTP-induced neurotoxicity in mice. J Neurochem 1995;64:936-939.
34. Boireau A, Dubedat P, Bordier F, Imperato A, Moussaoui S. The protective effect of riluzole in the MPTP model of Parkinson's disease in mice is not due to a decrease in MPP + accumulation. Neuropharmacology 2000;39:1016-1020.
35. Hantraye P, Brouillet E, Ferrante R, Palfi S, Dolan R, Matthews RT, Beal MF Inhibition of neuronal nitric oxide synthase prevents MPTP-induced parkinsonism in baboons. Nat Med 1996;2:1017-1021.
36. 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 Neuropsy-chopharmacol 2004;14:93-104.
37. Di Monte DA, Royland JE, Anderson A, Castagnoli K, Castagnoli N, Langston JW. Inhibition of monoamine oxidase contributes to the protective effect of 7-nitroindazole against MPTP neurotoxicity. J Neurochem 1997;69:1771-1773.
38. 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. (Pubitemid 29104973)
39. Muramatsu Y, Kurosaki R, Mikami T, Michimata M, Matsubara M, Imai Y, Kato H, Itoyama Y, Araki T Therapeutic effect of neuronal nitric oxide synthase inhibitor (7-nitroindazole) against MPTP neurotoxicity in mice. Metab Brain Dis 2002;17:169-182.
40. Royland JE, Delfani K, Langston JW, Janson AM, Di Monte DA. 7-Nitroindazole prevents 1-methyl-4-phenyl-1,2,3,6-tet-rahydropyridine-induced ATP loss in the mouse striatum. Brain Res 1999;839:41-48
41. Rojas P, Rojas C, Ebadi M, Montes S, Monroy-Noyola A, Serrano-Garcia N. EGb761 pretreatment reduces monoamine oxidase activity in mouse corpus striatum during 1-methyl-4-phenylpyridinium neurotoxicity. Neurochem Res 2004;29:1417-1423.
42. Fuller RW, Hemrickluecke SK. 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.
43. Matsumura N, Kikuchi-Utsumi K, Nakaki T Activities of 7-nitroindazole and 1-(2-(trifluoromethylphenyl)-imidazole independent of neuronal nitric-oxide synthase inhibition. J Pharmacol Exp Ther 2008;325:357-362.
44. Aran VJ, Flores M, Munoz P, Paez JA, Sanchez-Verdu P, Stud M. Analogues of cytostatic, fused indazolinones: Synthesis, conformational analysis and cytostatic activity against HeLa cells of some 1-substituted indazolols, 2-substituted indazolinones, and related compounds. Liebigs Ann 1996;683-691.
45. Aran VJ, Asensio JL, Ruiz JR, Stud M. Reactivity of 1,1-disubstituted indazol-3-ylio oxides*synthesis of some substituted indazolols and indazolinones. J Chem Soc Perkin Trans 1 1993;1119-1127.
46. Herraiz T, Chaparro C. Analysis of monoamine oxidase enzymatic activity by reversed-phase high performance liquid chromatography and inhibition by P-carboline alkaloids occurring in foods and plants. J Chromatogr A 2006;1120: 237-243.
47. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 1999;26:1231-1237.
48. Herraiz T, Galisteo J. Endogenous and dietary indoles: a class of antioxidants and radical scavengers in the ABTS assay. Free Radic Res 2004;38:323-331.
49. Halliwell B, Gutteridge JMC. Role of free radicals and catalytic metal ions in human disease: an overview. Meth Enzymol 1990;186:1-85.
50. Gutteridge JMC. Ferrous-salt-promoted damage to deoxyr-ibose and benzoate. The increased effectiveness of hydroxyl radical scavangers in the presence of EDTA. Biochem J 1987;243:709-714.
51. Cheng Y-C, Prussoff WF. 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.
52. Halliwell B, Gutteridge JMC, Aruoma OI. The deoxyribose method: a simple test-tube assay for determination of rate constants for reactions of hydroxyl radicals. Anal Biochem 1987;165:215-219.
53. 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
54. 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.
55. Cutillas B, Espejo M, Ambrosio S. 7-Nitroindazole prevents dopamine depletion caused by low concentrations of MPP+ in rat striatal slices. Neurochem Int 1998;33:35-40
56. Di Matteo V, Benigno A, Pierucci M, Giuliano DA, Cresci-manno G, Esposito E, Di Giovanni G. 7-Nitroindazole protects striatal dopaminergic neurons against MPP+-induced degeneration: an in vivo microdialysis study. Ann NY Acad Sci 2006;1089:462-471 (Pubitemid 47092070)
57. Binda C, Newton-Vinson P, Hubalek F, Edmondson DE, Mattevi A. Structure of human monoamine oxidase B, a drug target for the treatment of neurological disorders. Nat Struct Biol 2002;9:22-26.
58. 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.
59. Cleeter MWJ, Cooper JM, Schapira AHV. Nitric oxide enhances MPP+ inhibition of complex I. FEBS Lett 2001;504:50-52.
60. Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol 2003;53:S26-S36.
61. Bostanci MO, Bagirici F Neuroprotection by 7-nitroindazole against iron-induced hippocampal neurotoxicity. Cell Mol Neurobiol 2007;27:933-941.
62. Reiter RJ, Tan DX, Allegra M. Melatonin: reducing molecular pathology and dysfunction due to free radicals and associated reactants. Neuroendocrinol Lett 2002;23:3-8.
63. Watanabe Y, Kato H, Araki T Protective action of neuronal nitric oxide synthase inhibitor in the MPTP mouse model of Parkinson's disease. Metab Brain Dis 2008;23:51-69.