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

01-11-2018 | Neurology and Preclinical Neurological Studies - Review Article

Monoamine oxidase-A, serotonin and norepinephrine: synergistic players in cardiac physiology and pathology

Authors: Jeanne Mialet-Perez, Yohan Santin, Angelo Parini

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

Login to get access

Abstract

The mitochondrial enzyme monoamine oxidase A (MAO-A) is widely distributed in neuronal, myocyte and non-myocyte cardiac compartments. After the demonstrations that both cardiac neuronal and extraneuronal MAO-A contribute to the degradation of norepinephrine and serotonin, several studies attempted to determine the impact of MAO-A activity in the control of local concentration of the two biogenic amines and in their receptor-mediated effects. From the 2000s, an additional mechanism of action of MAO-A has been proposed. Such mechanism involves hydrogen peroxide (H2O2) production during substrate degradation. This finding stimulated a growing interest on the role of MAO-A-dependent oxidative stress in cardiac pathophysiology. Altogether, the results obtained by different groups showed that MAO-A played a key role in the regulation of physiological cardiac function and in the development of acute and chronic heart diseases through two mechanisms: the regulation of substrate concentrations and the intracellular production of reactive oxygen species. In this review, we will give an overview of the major results on the role of MAO-A in the field of cardiac diseases.
Literature
go back to reference Akiyama T, Yamazaki T (2001) Myocardial interstitial norepinephrine and dihydroxyphenylglycol levels during ischemia and reperfusion. Cardiovasc Res 49(1):78–85CrossRef Akiyama T, Yamazaki T (2001) Myocardial interstitial norepinephrine and dihydroxyphenylglycol levels during ischemia and reperfusion. Cardiovasc Res 49(1):78–85CrossRef
go back to reference Backs J, Haunstetter A, Gerber SH, Metz J, Borst MM, Strasser RH, Kubler W, Haass M (2001) The neuronal norepinephrine transporter in experimental heart failure: evidence for a posttranscriptional downregulation. J Mol Cell Cardiol 33(3):461–472CrossRef Backs J, Haunstetter A, Gerber SH, Metz J, Borst MM, Strasser RH, Kubler W, Haass M (2001) The neuronal norepinephrine transporter in experimental heart failure: evidence for a posttranscriptional downregulation. J Mol Cell Cardiol 33(3):461–472CrossRef
go back to reference Bianchi P, Kunduzova O, Masini E, Cambon C, Bani D, Raimondi L, Seguelas MH, Nistri S, Colucci W, Leducq N, Parini A (2005a) Oxidative stress by monoamine oxidase mediates receptor-independent cardiomyocyte apoptosis by serotonin and postischemic myocardial injury. Circulation 112(21):3297–3305CrossRef Bianchi P, Kunduzova O, Masini E, Cambon C, Bani D, Raimondi L, Seguelas MH, Nistri S, Colucci W, Leducq N, Parini A (2005a) Oxidative stress by monoamine oxidase mediates receptor-independent cardiomyocyte apoptosis by serotonin and postischemic myocardial injury. Circulation 112(21):3297–3305CrossRef
go back to reference de Chaplain J, Krakoff LR, Axelrod J (1968) Increased monoamine oxidase activity during the development of cardiac hypertrophy in the rat. Circ Res 23(3):361–369CrossRef de Chaplain J, Krakoff LR, Axelrod J (1968) Increased monoamine oxidase activity during the development of cardiac hypertrophy in the rat. Circ Res 23(3):361–369CrossRef
go back to reference Dhalla AK, Hill MF, Singal PK (1996) Role of oxidative stress in transition of hypertrophy to heart failure. J Am Coll Cardiol 28(2):506–514CrossRef Dhalla AK, Hill MF, Singal PK (1996) Role of oxidative stress in transition of hypertrophy to heart failure. J Am Coll Cardiol 28(2):506–514CrossRef
go back to reference Eisenhofer G, Friberg P, Rundqvist B, Quyyumi AA, Lambert G, Kaye DM, Kopin IJ, Goldstein DS, Esler MD (1996) Cardiac sympathetic nerve function in congestive heart failure. Circulation 93(9):1667–1676CrossRef Eisenhofer G, Friberg P, Rundqvist B, Quyyumi AA, Lambert G, Kaye DM, Kopin IJ, Goldstein DS, Esler MD (1996) Cardiac sympathetic nerve function in congestive heart failure. Circulation 93(9):1667–1676CrossRef
go back to reference Ganguly PK, Dhalla KS, Innes IR, Beamish RE, Dhalla NS (1986) Altered norepinephrine turnover and metabolism in diabetic cardiomyopathy. Circ Res 59(6):684–693CrossRef Ganguly PK, Dhalla KS, Innes IR, Beamish RE, Dhalla NS (1986) Altered norepinephrine turnover and metabolism in diabetic cardiomyopathy. Circ Res 59(6):684–693CrossRef
go back to reference Guffroy C, Strolin Benedetti M (1984) Monoamine oxidase and semicarbazide-sensitive amine oxidase in spontaneously hypertensive and in normotensive control rats. Life Sci 34(6):535–545CrossRef Guffroy C, Strolin Benedetti M (1984) Monoamine oxidase and semicarbazide-sensitive amine oxidase in spontaneously hypertensive and in normotensive control rats. Life Sci 34(6):535–545CrossRef
go back to reference Kaludercic N, Takimoto E, Nagayama T, Feng N, Lai EW, Bedja D, Chen K, Gabrielson KL, Blakely RD, Shih JC, Pacak K, Kass DA, Di Lisa F, Paolocci N (2010) Monoamine oxidase A-mediated enhanced catabolism of norepinephrine contributes to adverse remodeling and pump failure in hearts with pressure overload. Circ Res 106(1):193–202CrossRef Kaludercic N, Takimoto E, Nagayama T, Feng N, Lai EW, Bedja D, Chen K, Gabrielson KL, Blakely RD, Shih JC, Pacak K, Kass DA, Di Lisa F, Paolocci N (2010) Monoamine oxidase A-mediated enhanced catabolism of norepinephrine contributes to adverse remodeling and pump failure in hearts with pressure overload. Circ Res 106(1):193–202CrossRef
go back to reference Katayama M, Kobayashi S, Oguchi K, Yasuhara H (1984) Properties of monoamine oxidase in monkey heart. Jpn J Pharmacol 35(4):425–431CrossRef Katayama M, Kobayashi S, Oguchi K, Yasuhara H (1984) Properties of monoamine oxidase in monkey heart. Jpn J Pharmacol 35(4):425–431CrossRef
go back to reference Levy FO, Qvigstad E, Krobert KA, Skomedal T, Osnes JB (2008) Effects of serotonin in failing cardiac ventricle: signalling mechanisms and potential therapeutic implications. Neuropharmacology 55(6):1066–1071CrossRef Levy FO, Qvigstad E, Krobert KA, Skomedal T, Osnes JB (2008) Effects of serotonin in failing cardiac ventricle: signalling mechanisms and potential therapeutic implications. Neuropharmacology 55(6):1066–1071CrossRef
go back to reference Lowe MC, Horita A (1970) Stability of cardiac monoamine oxidase activity after chemical sympathectomy with 6-hydroxydopamine. Nature 228(5267):175–176CrossRef Lowe MC, Horita A (1970) Stability of cardiac monoamine oxidase activity after chemical sympathectomy with 6-hydroxydopamine. Nature 228(5267):175–176CrossRef
go back to reference Lowe MC, Reichenbach DD, Horita A (1975) Extraneuronal monoamine oxidase in rat heart: biochemical characterization and electron microscopic localization. J Pharmacol Exp Ther 194(3):522–536PubMed Lowe MC, Reichenbach DD, Horita A (1975) Extraneuronal monoamine oxidase in rat heart: biochemical characterization and electron microscopic localization. J Pharmacol Exp Ther 194(3):522–536PubMed
go back to reference Lyles GA, McAuslane JA, Fitzpatrick CM (1984) Monoamine oxidase activities of dissociated cell fractions from rat ventricular muscle. Biochem Pharmacol 33(16):2569–2574CrossRef Lyles GA, McAuslane JA, Fitzpatrick CM (1984) Monoamine oxidase activities of dissociated cell fractions from rat ventricular muscle. Biochem Pharmacol 33(16):2569–2574CrossRef
go back to reference Manni ME, Rigacci S, Borchi E, Bargelli V, Miceli C, Giordano C, Raimondi L, Nediani C (2016) Monoamine oxidase is overactivated in left and right ventricles from ischemic hearts: an intriguing therapeutic target. Oxidative Med Cell Longev 2016:4375418. https://doi.org/10.1155/2016/4375418 CrossRef Manni ME, Rigacci S, Borchi E, Bargelli V, Miceli C, Giordano C, Raimondi L, Nediani C (2016) Monoamine oxidase is overactivated in left and right ventricles from ischemic hearts: an intriguing therapeutic target. Oxidative Med Cell Longev 2016:4375418. https://​doi.​org/​10.​1155/​2016/​4375418 CrossRef
go back to reference Maurel A, Hernandez C, Kunduzova O, Bompart G, Cambon C, Parini A, Frances B (2003) Age-dependent increase in hydrogen peroxide production by cardiac monoamine oxidase A in rats. Am J Physiol Heart Circ Physiol 284(4):H1460–H1467CrossRef Maurel A, Hernandez C, Kunduzova O, Bompart G, Cambon C, Parini A, Frances B (2003) Age-dependent increase in hydrogen peroxide production by cardiac monoamine oxidase A in rats. Am J Physiol Heart Circ Physiol 284(4):H1460–H1467CrossRef
go back to reference Meco M, Bonifati V, Collier WL, Ramacci MT, Amenta F (1987) Enzyme histochemistry of monoamine oxidase in the heart of aged rats. Mech Ageing Dev 38(2):145–155CrossRef Meco M, Bonifati V, Collier WL, Ramacci MT, Amenta F (1987) Enzyme histochemistry of monoamine oxidase in the heart of aged rats. Mech Ageing Dev 38(2):145–155CrossRef
go back to reference Pchejetski D, Kunduzova O, Dayon A, Calise D, Seguelas MH, Leducq N, Seif I, Parini A, Cuvillier O (2007) Oxidative stress-dependent sphingosine kinase-1 inhibition mediates monoamine oxidase A-associated cardiac cell apoptosis. Circ Res 100(1):41–49CrossRef Pchejetski D, Kunduzova O, Dayon A, Calise D, Seguelas MH, Leducq N, Seif I, Parini A, Cuvillier O (2007) Oxidative stress-dependent sphingosine kinase-1 inhibition mediates monoamine oxidase A-associated cardiac cell apoptosis. Circ Res 100(1):41–49CrossRef
go back to reference Pino R, Failli P, Mazzetti L, Buffoni F (1997) Monoamine oxidase and semicarbazide-sensitive amine oxidase activities in isolated cardiomyocytes of spontaneously hypertensive rats. Biochem Mol Med 62(2):188–196CrossRef Pino R, Failli P, Mazzetti L, Buffoni F (1997) Monoamine oxidase and semicarbazide-sensitive amine oxidase activities in isolated cardiomyocytes of spontaneously hypertensive rats. Biochem Mol Med 62(2):188–196CrossRef
go back to reference Pirzgalska RM, Seixas E, Seidman JS, Link VM, Sanchez NM, Mahu I, Mendes R, Gres V, Kubasova N, Morris I, Arus BA, Larabee CM, Vasques M, Tortosa F, Sousa AL, Anandan S, Tranfield E, Hahn MK, Iannacone M, Spann NJ, Glass CK, Domingos AI (2017) Sympathetic neuron-associated macrophages contribute to obesity by importing and metabolizing norepinephrine. Nat Med 23(11):1309–1318. https://doi.org/10.1038/nm.4422 CrossRefPubMed Pirzgalska RM, Seixas E, Seidman JS, Link VM, Sanchez NM, Mahu I, Mendes R, Gres V, Kubasova N, Morris I, Arus BA, Larabee CM, Vasques M, Tortosa F, Sousa AL, Anandan S, Tranfield E, Hahn MK, Iannacone M, Spann NJ, Glass CK, Domingos AI (2017) Sympathetic neuron-associated macrophages contribute to obesity by importing and metabolizing norepinephrine. Nat Med 23(11):1309–1318. https://​doi.​org/​10.​1038/​nm.​4422 CrossRefPubMed
go back to reference Rodriguez MJ, Saura J, Billett EE, Finch CC, Mahy N (2001) Cellular localization of monoamine oxidase A and B in human tissues outside of the central nervous system. Cell Tissue Res 304(2):215–220CrossRef Rodriguez MJ, Saura J, Billett EE, Finch CC, Mahy N (2001) Cellular localization of monoamine oxidase A and B in human tissues outside of the central nervous system. Cell Tissue Res 304(2):215–220CrossRef
go back to reference Rouzaud-Laborde C, Delmas C, Pizzinat N, Tortosa F, Garcia C, Mialet-Perez J, Payrastre B, Sie P, Spreux-Varoquaux O, Sallerin B, Carrie D, Galinier M, Parini A, Lairez O (2015) Platelet activation and arterial peripheral serotonin turnover in cardiac remodeling associated to aortic stenosis. Am J Hematol 90(1):15–19. https://doi.org/10.1002/ajh.23855 CrossRefPubMed Rouzaud-Laborde C, Delmas C, Pizzinat N, Tortosa F, Garcia C, Mialet-Perez J, Payrastre B, Sie P, Spreux-Varoquaux O, Sallerin B, Carrie D, Galinier M, Parini A, Lairez O (2015) Platelet activation and arterial peripheral serotonin turnover in cardiac remodeling associated to aortic stenosis. Am J Hematol 90(1):15–19. https://​doi.​org/​10.​1002/​ajh.​23855 CrossRefPubMed
go back to reference Saito J, Suzuki E, Tajima Y, Takami K, Horikawa Y, Takeda J (2016) Increased plasma serotonin metabolite 5-hydroxyindole acetic acid concentrations are associated with impaired systolic and late diastolic forward flows during cardiac cycle and elevated resistive index at popliteal artery and renal insufficiency in type 2 diabetic patients with microalbuminuria. Endocr J 63(1):69–76. https://doi.org/10.1507/endocrj.EJ15-0343 CrossRefPubMed Saito J, Suzuki E, Tajima Y, Takami K, Horikawa Y, Takeda J (2016) Increased plasma serotonin metabolite 5-hydroxyindole acetic acid concentrations are associated with impaired systolic and late diastolic forward flows during cardiac cycle and elevated resistive index at popliteal artery and renal insufficiency in type 2 diabetic patients with microalbuminuria. Endocr J 63(1):69–76. https://​doi.​org/​10.​1507/​endocrj.​EJ15-0343 CrossRefPubMed
go back to reference Santin Y, Sicard P, Vigneron F, Guilbeau-Frugier C, Dutaur M, Lairez O, Couderc B, Manni D, Korolchuk VI, Lezoualc’h F, Parini A, Mialet-Perez J (2016) Oxidative stress by monoamine oxidase-A impairs transcription factor EB activation and autophagosome clearance, leading to cardiomyocyte necrosis and heart failure. Antioxid Redox Signal 25(1):10–27. https://doi.org/10.1089/ars.2015.6522 CrossRefPubMed Santin Y, Sicard P, Vigneron F, Guilbeau-Frugier C, Dutaur M, Lairez O, Couderc B, Manni D, Korolchuk VI, Lezoualc’h F, Parini A, Mialet-Perez J (2016) Oxidative stress by monoamine oxidase-A impairs transcription factor EB activation and autophagosome clearance, leading to cardiomyocyte necrosis and heart failure. Antioxid Redox Signal 25(1):10–27. https://​doi.​org/​10.​1089/​ars.​2015.​6522 CrossRefPubMed
go back to reference Saura J, Richards JG, Mahy N (1994a) Age-related-changes on MAO in Bl/C57 mouse-tissues—a quantitative autoradiographic study. J Neural Transm Suppl 41:89–94PubMed Saura J, Richards JG, Mahy N (1994a) Age-related-changes on MAO in Bl/C57 mouse-tissues—a quantitative autoradiographic study. J Neural Transm Suppl 41:89–94PubMed
go back to reference Saura J, Richards JG, Mahy N (1994c) Differential age-related changes of MAO-A and MAO-B in mouse brain and peripheral organs. Neurobiol Aging 15(4):399–408CrossRef Saura J, Richards JG, Mahy N (1994c) Differential age-related changes of MAO-A and MAO-B in mouse brain and peripheral organs. Neurobiol Aging 15(4):399–408CrossRef
go back to reference Saura J, Nadal E, van den Berg B, Vila M, Bombi JA, Mahy N (1996) Localization of monoamine oxidases in human peripheral tissues. Life Sci 59(16):1341–1349CrossRef Saura J, Nadal E, van den Berg B, Vila M, Bombi JA, Mahy N (1996) Localization of monoamine oxidases in human peripheral tissues. Life Sci 59(16):1341–1349CrossRef
go back to reference Shih JC, Chen K, Ridd MJ (1999b) Role of MAO A and B in neurotransmitter metabolism and behavior. Pol J Pharmacol 51(1):25–29PubMed Shih JC, Chen K, Ridd MJ (1999b) Role of MAO A and B in neurotransmitter metabolism and behavior. Pol J Pharmacol 51(1):25–29PubMed
go back to reference Siddiqui A, Hanson I, Andersen JK (2012) MAO-B elevation decreases parkin’s ability to efficiently clear damaged mitochondria: protective effects of rapamycin. Free Radic Res 46(8):1011–1018CrossRef Siddiqui A, Hanson I, Andersen JK (2012) MAO-B elevation decreases parkin’s ability to efficiently clear damaged mitochondria: protective effects of rapamycin. Free Radic Res 46(8):1011–1018CrossRef
go back to reference Toussaint O, Royer V, Salmon M, Remacle J (2002) Stress-induced premature senescence and tissue ageing. Biochem Pharmacol 64(5–6):1007–1009CrossRef Toussaint O, Royer V, Salmon M, Remacle J (2002) Stress-induced premature senescence and tissue ageing. Biochem Pharmacol 64(5–6):1007–1009CrossRef
go back to reference Trendelenburg U (1984) The influence of inhibition of catechol-O-methyl transferase or of monoamine oxidase on the extraneuronal metabolism of 3H-(-)-noradrenaline in the rat heart. Naunyn Schmiedebergs Arch Pharmacol 327(4):285–292CrossRef Trendelenburg U (1984) The influence of inhibition of catechol-O-methyl transferase or of monoamine oxidase on the extraneuronal metabolism of 3H-(-)-noradrenaline in the rat heart. Naunyn Schmiedebergs Arch Pharmacol 327(4):285–292CrossRef
go back to reference Villeneuve C, Guilbeau-Frugier C, Sicard P, Lairez O, Ordener C, Duparc T, De Paulis D, Couderc B, Spreux-Varoquaux O, Tortosa F, Garnier A, Knauf C, Valet P, Borchi E, Nediani C, Gharib A, Ovize M, Delisle MB, Parini A, Mialet-Perez J (2013) p53-PGC-1alpha pathway mediates oxidative mitochondrial damage and cardiomyocyte necrosis induced by monoamine oxidase-A upregulation: role in chronic left ventricular dysfunction in mice. Antioxid Redox Signal 18(1):5–18. https://doi.org/10.1089/ars.2011.4373 CrossRefPubMedPubMedCentral Villeneuve C, Guilbeau-Frugier C, Sicard P, Lairez O, Ordener C, Duparc T, De Paulis D, Couderc B, Spreux-Varoquaux O, Tortosa F, Garnier A, Knauf C, Valet P, Borchi E, Nediani C, Gharib A, Ovize M, Delisle MB, Parini A, Mialet-Perez J (2013) p53-PGC-1alpha pathway mediates oxidative mitochondrial damage and cardiomyocyte necrosis induced by monoamine oxidase-A upregulation: role in chronic left ventricular dysfunction in mice. Antioxid Redox Signal 18(1):5–18. https://​doi.​org/​10.​1089/​ars.​2011.​4373 CrossRefPubMedPubMedCentral
go back to reference Zhu Y, Tchkonia T, Pirtskhalava T, Gower AC, Ding H, Giorgadze N, Palmer AK, Ikeno Y, Hubbard GB, Lenburg M, O’Hara SP, LaRusso NF, Miller JD, Roos CM, Verzosa GC, LeBrasseur NK, Wren JD, Farr JN, Khosla S, Stout MB, McGowan SJ, Fuhrmann-Stroissnigg H, Gurkar AU, Zhao J, Colangelo D, Dorronsoro A, Ling YY, Barghouthy AS, Navarro DC, Sano T, Robbins PD, Niedernhofer LJ, Kirkland JL (2015) The Achilles’ heel of senescent cells: from transcriptome to senolytic drugs. Aging cell 14(4):644–658. https://doi.org/10.1111/acel.12344 CrossRefPubMedPubMedCentral Zhu Y, Tchkonia T, Pirtskhalava T, Gower AC, Ding H, Giorgadze N, Palmer AK, Ikeno Y, Hubbard GB, Lenburg M, O’Hara SP, LaRusso NF, Miller JD, Roos CM, Verzosa GC, LeBrasseur NK, Wren JD, Farr JN, Khosla S, Stout MB, McGowan SJ, Fuhrmann-Stroissnigg H, Gurkar AU, Zhao J, Colangelo D, Dorronsoro A, Ling YY, Barghouthy AS, Navarro DC, Sano T, Robbins PD, Niedernhofer LJ, Kirkland JL (2015) The Achilles’ heel of senescent cells: from transcriptome to senolytic drugs. Aging cell 14(4):644–658. https://​doi.​org/​10.​1111/​acel.​12344 CrossRefPubMedPubMedCentral
Metadata
Title
Monoamine oxidase-A, serotonin and norepinephrine: synergistic players in cardiac physiology and pathology
Authors
Jeanne Mialet-Perez
Yohan Santin
Angelo Parini
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/s00702-018-1908-y

Other articles of this Issue 11/2018

Journal of Neural Transmission 11/2018 Go to the issue

Psychiatry and Preclinical Psychiatric Studies - Review Article

On the practical aspects of characterising monoamine oxidase inhibition in vitro

Neurology and Preclinical Neurological Studies - Review Article

Kinetics, mechanism, and inhibition of monoamine oxidase