Skip to main content
Top
Published in: Journal of Neural Transmission 11/2018

01-11-2018 | Psychiatry and Preclinical Psychiatric Studies - Review Article

On the practical aspects of characterising monoamine oxidase inhibition in vitro

Author: Andrew Holt

Published in: Journal of Neural Transmission | Issue 11/2018

Login to get access

Abstract

The development of novel inhibitors of human monoamine oxidase enzymes with improved pharmacodynamic and pharmacokinetic profiles has, in the past, been hampered by limited access to enzyme, by assay protocols offering limited throughput, and by inappropriate analyses of kinetic data. More recently, high-level expression of human enzymes in yeast has facilitated thorough examinations of steady-state enzyme behaviour that have led to improvements in our understanding of the mathematical underpinnings of kinetic analyses of monoamine oxidases. However, with these improvements have come a realisation that to be useful, more data points across wider concentration ranges are required. In turn, many discontinuous assay approaches, such as those involving radiolabelled substrates or chromatographic separation of product from substrate, have been rendered somewhat obsolete. Justification for the use of a platereader-based approach to assess the effects of novel inhibitors on monamine oxidases is provided, along with details of experimental design optimised to address the unexpectedly complex kinetics followed by these enzymes. Potential sources of error are discussed, and comments provided on techniques that may enhance the quality of experimental data.
Literature
go back to reference Copeland RA (2013) Evaluation of enzyme inhibitors in drug discovery: a guide for medicinal chemists and pharmacologists, 2nd edn. Wiley, HobokenCrossRef Copeland RA (2013) Evaluation of enzyme inhibitors in drug discovery: a guide for medicinal chemists and pharmacologists, 2nd edn. Wiley, HobokenCrossRef
go back to reference Cornish-Bowden A (1995) Analysis of enzyme kinetic data, vol 1. Oxford University Press, Oxford Cornish-Bowden A (1995) Analysis of enzyme kinetic data, vol 1. Oxford University Press, Oxford
go back to reference Cornish-Bowden A (2014) Analysis and interpretation of enzyme kinetic data. Perspect Sci 1:121–125CrossRef Cornish-Bowden A (2014) Analysis and interpretation of enzyme kinetic data. Perspect Sci 1:121–125CrossRef
go back to reference Daum G, Bohni PC, Schatz G (1982) Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem 257:13028–13033PubMed Daum G, Bohni PC, Schatz G (1982) Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem 257:13028–13033PubMed
go back to reference Dixon M, Webb EC (1979) Enzymes, Third edn. Academic Press, New York Dixon M, Webb EC (1979) Enzymes, Third edn. Academic Press, New York
go back to reference Edmondson DE, Bhattacharyya AK, Walker MC (1993) Spectral and kinetic studies of imine product formation in the oxidation of p-(N,N-dimethylamino)benzylamine analogues by monoamine oxidase B. Biochemistry 32:5196–5202CrossRef Edmondson DE, Bhattacharyya AK, Walker MC (1993) Spectral and kinetic studies of imine product formation in the oxidation of p-(N,N-dimethylamino)benzylamine analogues by monoamine oxidase B. Biochemistry 32:5196–5202CrossRef
go back to reference Fowler CJ, Callingham BA, Houslay MD (1977) The effect of tris buffers on rat liver mitochondrial monoamine oxidase. J Pharm Pharmacol 29:411–415CrossRef Fowler CJ, Callingham BA, Houslay MD (1977) The effect of tris buffers on rat liver mitochondrial monoamine oxidase. J Pharm Pharmacol 29:411–415CrossRef
go back to reference Green AR, Mitchell BD, Tordoff AF, Youdim MB (1977) Evidence for dopamine deamination by both type A and type B monoamine oxidase in rat brain in vivo and for the degree of inhibition of enzyme necessary for increased functional activity of dopamine and 5-hydroxytryptamine. Br J Pharmacol 60:343–349CrossRef Green AR, Mitchell BD, Tordoff AF, Youdim MB (1977) Evidence for dopamine deamination by both type A and type B monoamine oxidase in rat brain in vivo and for the degree of inhibition of enzyme necessary for increased functional activity of dopamine and 5-hydroxytryptamine. Br J Pharmacol 60:343–349CrossRef
go back to reference Haefely W et al (1992) Biochemistry and pharmacology of moclobemide, a prototype RIMA. Psychopharmacology 106:S6–S14CrossRef Haefely W et al (1992) Biochemistry and pharmacology of moclobemide, a prototype RIMA. Psychopharmacology 106:S6–S14CrossRef
go back to reference Holt A (2007) Practical enzymology. Quantifying enzyme activity and the effects of drugs thereupon. In: Baker GB, Dunn SA, Holt A (eds) Handbook of neurochemistry and molecular neurobiology, vol 18, practical neurochemistry methods, 3rd edn. Kluwer Academic, New York Holt A (2007) Practical enzymology. Quantifying enzyme activity and the effects of drugs thereupon. In: Baker GB, Dunn SA, Holt A (eds) Handbook of neurochemistry and molecular neurobiology, vol 18, practical neurochemistry methods, 3rd edn. Kluwer Academic, New York
go back to reference Holt A, Palcic MM (2006) A peroxidase-coupled continuous absorbance plate-reader assay for flavin monoamine oxidases, copper-containing amine oxidases and related enzymes. Nat Protoc 1:2498–2505CrossRef Holt A, Palcic MM (2006) A peroxidase-coupled continuous absorbance plate-reader assay for flavin monoamine oxidases, copper-containing amine oxidases and related enzymes. Nat Protoc 1:2498–2505CrossRef
go back to reference Holt A, Sharman DF, Baker GB, Palcic MM (1997) A continuous spectrophotometric assay for monoamine oxidase and related enzymes in tissue homogenates. Anal Biochem 244:384–392CrossRef Holt A, Sharman DF, Baker GB, Palcic MM (1997) A continuous spectrophotometric assay for monoamine oxidase and related enzymes in tissue homogenates. Anal Biochem 244:384–392CrossRef
go back to reference Houslay MD, Tipton KF (1975) Rat liver mitochondrial monoamine oxidase. A change in the reaction mechanism on solubilization. Biochem J 145:311–321CrossRef Houslay MD, Tipton KF (1975) Rat liver mitochondrial monoamine oxidase. A change in the reaction mechanism on solubilization. Biochem J 145:311–321CrossRef
go back to reference Hulme EC, Birdsall NJM (1992) Strategy and tactics in receptor binding studies. In: Hulme EC (ed) Receptor–ligand interactions. A practical approach. IRL Press at Oxford University Press, Oxford Hulme EC, Birdsall NJM (1992) Strategy and tactics in receptor binding studies. In: Hulme EC (ed) Receptor–ligand interactions. A practical approach. IRL Press at Oxford University Press, Oxford
go back to reference Husain M, Edmondson DE, Singer TP (1982) Kinetic studies on the catalytic mechanism of liver monoamine oxidase. Biochemistry 21:595–600CrossRef Husain M, Edmondson DE, Singer TP (1982) Kinetic studies on the catalytic mechanism of liver monoamine oxidase. Biochemistry 21:595–600CrossRef
go back to reference Kinemuchi H, Arai Y, Oreland L, Tipton KF, Fowler CJ (1982) Time-dependent inhibition of monoamine oxidase by β-phenethylamine. Biochem Pharmacol 31:959–964CrossRef Kinemuchi H, Arai Y, Oreland L, Tipton KF, Fowler CJ (1982) Time-dependent inhibition of monoamine oxidase by β-phenethylamine. Biochem Pharmacol 31:959–964CrossRef
go back to reference Kitz R, Wilson IB (1962) Esters of methanesulfonic acid as irreversible inhibitors of acetylcholinesterase. J Biol Chem 237:3245–3249PubMed Kitz R, Wilson IB (1962) Esters of methanesulfonic acid as irreversible inhibitors of acetylcholinesterase. J Biol Chem 237:3245–3249PubMed
go back to reference Li M, Hubálek F, Newton-Vinson P, Edmondson DE (2002) High-level expression of human liver monoamine oxidase A in Pichia pastoris: comparison with the enzyme expressed in Saccharomyces cerevisiae. Protein Expr Purif 24:152–162CrossRef Li M, Hubálek F, Newton-Vinson P, Edmondson DE (2002) High-level expression of human liver monoamine oxidase A in Pichia pastoris: comparison with the enzyme expressed in Saccharomyces cerevisiae. Protein Expr Purif 24:152–162CrossRef
go back to reference Li M, Binda C, Mattevi A, Edmondson DE (2006) Functional role of the “aromatic cage” in human monoamine oxidase B: structures and catalytic properties of Tyr435 mutant proteins. Biochemistry 45:4775–4784CrossRef Li M, Binda C, Mattevi A, Edmondson DE (2006) Functional role of the “aromatic cage” in human monoamine oxidase B: structures and catalytic properties of Tyr435 mutant proteins. Biochemistry 45:4775–4784CrossRef
go back to reference Matsumoto T et al (1985) A sensitive fluorometric assay for serum monoamine oxidase with kynuramine as substrate. Clin Biochem 18:126–129CrossRef Matsumoto T et al (1985) A sensitive fluorometric assay for serum monoamine oxidase with kynuramine as substrate. Clin Biochem 18:126–129CrossRef
go back to reference Matveychuk D, Nunes E, Ullah N, Velazquez-Martinez CA, MacKenzie EM, Baker GB (2013) Comparison of phenelzine and geometric isomers of its active metabolite, beta-phenylethylidenehydrazine, on rat brain levels of amino acids, biogenic amine neurotransmitters and methylamine. J Neural Transm (Vienna) 120:987–996. https://doi.org/10.1007/s00702-013-0978-0 CrossRef Matveychuk D, Nunes E, Ullah N, Velazquez-Martinez CA, MacKenzie EM, Baker GB (2013) Comparison of phenelzine and geometric isomers of its active metabolite, beta-phenylethylidenehydrazine, on rat brain levels of amino acids, biogenic amine neurotransmitters and methylamine. J Neural Transm (Vienna) 120:987–996. https://​doi.​org/​10.​1007/​s00702-013-0978-0 CrossRef
go back to reference McDonald GR et al (2008) Bioactive contaminants leach from disposable laboratory plasticware. Science 322:917CrossRef McDonald GR et al (2008) Bioactive contaminants leach from disposable laboratory plasticware. Science 322:917CrossRef
go back to reference Miller JR, Edmondson DE (1999) Structure–activity relationships in the oxidation of para-substituted benzylamine analogues by recombinant human liver monoamine oxidase A. Biochemistry 38:13670–13683CrossRef Miller JR, Edmondson DE (1999) Structure–activity relationships in the oxidation of para-substituted benzylamine analogues by recombinant human liver monoamine oxidase A. Biochemistry 38:13670–13683CrossRef
go back to reference Morrison JF (1982) The slow-binding and slow, tight-binding inhibition of enzyme-catalysed reactions. Trends Biochem Sci 7:102–105CrossRef Morrison JF (1982) The slow-binding and slow, tight-binding inhibition of enzyme-catalysed reactions. Trends Biochem Sci 7:102–105CrossRef
go back to reference Morrison JF, Stone SR (1985) Approaches to the study and analysis of the inhibition of enzymes by slow- and tight-binding inhibitors. Comments Mol Cell Biophys 2:347–368 Morrison JF, Stone SR (1985) Approaches to the study and analysis of the inhibition of enzymes by slow- and tight-binding inhibitors. Comments Mol Cell Biophys 2:347–368
go back to reference Morrison JF, Walsh CT (1988) The behavior and significance of slow-binding enzyme inhibitors. Adv Enzymol Relat Areas Mol Biol 61:201–301PubMed Morrison JF, Walsh CT (1988) The behavior and significance of slow-binding enzyme inhibitors. Adv Enzymol Relat Areas Mol Biol 61:201–301PubMed
go back to reference Nelson DR, Huggins AK (1974) Interference of 5-hydroxytryptamine in the assay of glucose by glucose oxidase:peroxidase:chromogen based methods. Anal Biochem 59:46–53CrossRef Nelson DR, Huggins AK (1974) Interference of 5-hydroxytryptamine in the assay of glucose by glucose oxidase:peroxidase:chromogen based methods. Anal Biochem 59:46–53CrossRef
go back to reference Palfreyman MG, McDonald IA, Bey P, Danzin C, Zreika M, Lyles GA, Fozard JR (1986) The rational design of suicide substrates of amine oxidases. Biochem Soc Trans 14:410–413CrossRef Palfreyman MG, McDonald IA, Bey P, Danzin C, Zreika M, Lyles GA, Fozard JR (1986) The rational design of suicide substrates of amine oxidases. Biochem Soc Trans 14:410–413CrossRef
go back to reference Pearce LB, Roth JA (1985) Human brain monoamine oxidase type B: mechanism of deamination as probed by steady-state methods. Biochemistry 24:1821–1826CrossRef Pearce LB, Roth JA (1985) Human brain monoamine oxidase type B: mechanism of deamination as probed by steady-state methods. Biochemistry 24:1821–1826CrossRef
go back to reference Ramsay RR (1991) Kinetic mechanism of monoamine oxidase A. Biochemistry 30:4624–4629CrossRef Ramsay RR (1991) Kinetic mechanism of monoamine oxidase A. Biochemistry 30:4624–4629CrossRef
go back to reference Ramsay RR (2013) Inhibitor design for monoamine oxidases. Curr Pharm Des 19:2529–2539CrossRef Ramsay RR (2013) Inhibitor design for monoamine oxidases. Curr Pharm Des 19:2529–2539CrossRef
go back to reference Ramsay RR, Koerber SC, Singer TP (1987) Stopped-flow studies on the mechanism of oxidation of N-methyl-4-phenyltetrahydropyridine by bovine liver monoamine oxidase B. Biochemistry 26:3045–3050CrossRef Ramsay RR, Koerber SC, Singer TP (1987) Stopped-flow studies on the mechanism of oxidation of N-methyl-4-phenyltetrahydropyridine by bovine liver monoamine oxidase B. Biochemistry 26:3045–3050CrossRef
go back to reference Roth JA, Eddy BJ (1980) Kinetic properties of membrane-bound and Triton X-100-solubilized human brain monoamine oxidase. Arch Biochem Biophys 205:260–266CrossRef Roth JA, Eddy BJ (1980) Kinetic properties of membrane-bound and Triton X-100-solubilized human brain monoamine oxidase. Arch Biochem Biophys 205:260–266CrossRef
go back to reference Sculley MJ, Morrison JF (1986) The determination of kinetic constants governing the slow, tight-binding inhibition of enzyme-catalysed reactions. Biochim Biophys Acta 874:44–53CrossRef Sculley MJ, Morrison JF (1986) The determination of kinetic constants governing the slow, tight-binding inhibition of enzyme-catalysed reactions. Biochim Biophys Acta 874:44–53CrossRef
go back to reference Segel IH (1993) Enzyme kinetics. Behavior and analysis of rapid equilibrium and steady-state enzyme systems. Wiley Classics Library Edition edn. Wiley, New York Segel IH (1993) Enzyme kinetics. Behavior and analysis of rapid equilibrium and steady-state enzyme systems. Wiley Classics Library Edition edn. Wiley, New York
go back to reference Silverman RB (1995) Mechanism-based enzyme inactivators. Methods Enzymol 249:240–283CrossRef Silverman RB (1995) Mechanism-based enzyme inactivators. Methods Enzymol 249:240–283CrossRef
go back to reference Szutowicz A, Kobes RD, Orsulak PJ (1984) Colorimetric assay for monoamine oxidase in tissues using peroxidase and 2,2′-azinodi(3-ethylbenzthiazoline-6-sulfonic acid) as chromogen. Anal Biochem 138:86–94CrossRef Szutowicz A, Kobes RD, Orsulak PJ (1984) Colorimetric assay for monoamine oxidase in tissues using peroxidase and 2,2′-azinodi(3-ethylbenzthiazoline-6-sulfonic acid) as chromogen. Anal Biochem 138:86–94CrossRef
go back to reference Tabor CW, Tabor H, Rosenthal SM (1954) Purification of amine oxidase from beef plasma. J Biol Chem 208:645–661PubMed Tabor CW, Tabor H, Rosenthal SM (1954) Purification of amine oxidase from beef plasma. J Biol Chem 208:645–661PubMed
go back to reference Tan AK, Ramsay RR (1993) Substrate-specific enhancement of the oxidative half-reaction of monoamine oxidase. Biochemistry 32:2137–2143CrossRef Tan AK, Ramsay RR (1993) Substrate-specific enhancement of the oxidative half-reaction of monoamine oxidase. Biochemistry 32:2137–2143CrossRef
go back to reference Tesson F et al (1995) Localization of I2-imidazoline binding sites on monoamine oxidases. J Biol Chem 270:9856–9861CrossRef Tesson F et al (1995) Localization of I2-imidazoline binding sites on monoamine oxidases. J Biol Chem 270:9856–9861CrossRef
go back to reference Upadhyay AK, Borbat PP, Wang J, Freed JH, Edmondson DE (2008) Determination of the oligomeric states of human and rat monoamine oxidases in the outer mitochondrial membrane and octyl beta-d-glucopyranoside micelles using pulsed dipolar electron spin resonance spectroscopy. Biochemistry 47:1554–1566. https://doi.org/10.1021/bi7021377 CrossRefPubMed Upadhyay AK, Borbat PP, Wang J, Freed JH, Edmondson DE (2008) Determination of the oligomeric states of human and rat monoamine oxidases in the outer mitochondrial membrane and octyl beta-d-glucopyranoside micelles using pulsed dipolar electron spin resonance spectroscopy. Biochemistry 47:1554–1566. https://​doi.​org/​10.​1021/​bi7021377 CrossRefPubMed
go back to reference Van Woert MH, Cotzias GC (1966) Anion inhibition of monoamine oxidase. Biochem Pharmacol 15:275–285CrossRef Van Woert MH, Cotzias GC (1966) Anion inhibition of monoamine oxidase. Biochem Pharmacol 15:275–285CrossRef
go back to reference Walker B, Elmore DT (1984) The irreversible inhibition of urokinase, kidney-cell plasminogen activator, plasmin and β-trypsin by 1-(N-6-amino-n-hexyl)carbamoylimidazole. Biochem J 221:277–280CrossRef Walker B, Elmore DT (1984) The irreversible inhibition of urokinase, kidney-cell plasminogen activator, plasmin and β-trypsin by 1-(N-6-amino-n-hexyl)carbamoylimidazole. Biochem J 221:277–280CrossRef
go back to reference Weissbach H, Smith TE, Daly JW, Witkop B, Udenfriend S (1960) A rapid spectrophotometric assay of monoamine oxidase based on the rate of disappearance of kynuramine. J Biol Chem 235:1160–1163PubMed Weissbach H, Smith TE, Daly JW, Witkop B, Udenfriend S (1960) A rapid spectrophotometric assay of monoamine oxidase based on the rate of disappearance of kynuramine. J Biol Chem 235:1160–1163PubMed
go back to reference Weyler W, Titlow CC, Salach JI (1990) Catalytically active monoamine oxidase type A from human liver expressed in Saccharomyces cerevisiae contains covalent FAD. Biochem Biophys Res Commun 173:1205–1211CrossRef Weyler W, Titlow CC, Salach JI (1990) Catalytically active monoamine oxidase type A from human liver expressed in Saccharomyces cerevisiae contains covalent FAD. Biochem Biophys Res Commun 173:1205–1211CrossRef
go back to reference Youdim MB, Tipton KF (2002) Rat striatal monoamine oxidase-B inhibition by l-deprenyl and rasagiline: its relationship to 2-phenylethylamine-induced stereotypy and Parkinson’s disease. Parkinson Relat Disord 8:247–253CrossRef Youdim MB, Tipton KF (2002) Rat striatal monoamine oxidase-B inhibition by l-deprenyl and rasagiline: its relationship to 2-phenylethylamine-induced stereotypy and Parkinson’s disease. Parkinson Relat Disord 8:247–253CrossRef
go back to reference Yu PH, Tipton KF (1989) Deuterium isotope effect of phenelzine on the inhibition of rat liver mitochondrial monoamine oxidase activity. Biochem Pharmacol 38:4245–4251CrossRef Yu PH, Tipton KF (1989) Deuterium isotope effect of phenelzine on the inhibition of rat liver mitochondrial monoamine oxidase activity. Biochem Pharmacol 38:4245–4251CrossRef
Metadata
Title
On the practical aspects of characterising monoamine oxidase inhibition in vitro
Author
Andrew Holt
Publication date
01-11-2018
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue 11/2018
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-018-1943-8

Other articles of this Issue 11/2018

Journal of Neural Transmission 11/2018 Go to the issue

Psychiatry and Preclinical Psychiatric Studies - Review Article

Monoamine oxidase isoenzymes: genes, functions and targets for behavior and cancer therapy

Neurology and Preclinical Neurological Studies - Review Article

90 years of monoamine oxidase: some progress and some confusion