Monoamine Oxidase b prompts mitochondrial and cardiac dysfunction in pressure overloaded hearts

Antioxidants and Redox Signaling

Volumn 20, Issue 2, 2014, Pages 267-280

  Kaludercic, Nina ^a   Carpi, Andrea ^b   Nagayama, Takahiro ^c   Sivakumaran, Vidhya ^c   Zhu, Guangshuo ^c   Lai, Edwin W ^d   Bedja, Djahida ^c   De Mario, Agnese ^e   Chen, Kevin ^f   Gabrielson, Kathleen L ^c   Lindsey, Merry L ^g   Pacak, Karel ^d   Takimoto, Eiki ^c   Shih, Jean C ^f,h   Kass, David A ^c   Di Lisa, Fabio ^a,e   Paolocci, Nazareno ^c,i  

^a CNR   (Italy)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^c DEPARTMENT OF PATHOLOGY   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^e UNIVERSITY OF PADOVA   (Italy)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^g UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^h UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

ⁱ UNIVERSITY OF PERUGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE ISOENZYME 2; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; DOPAMINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OLIGOMYCIN; PARGYLINE;

ADULT; ANIMAL CELL; ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; CELL ENERGY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME METABOLISM; HEART LEFT VENTRICLE FUNCTION; HEART LEFT VENTRICLE HYPERTROPHY; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART VENTRICLE OVERLOAD; HEART VENTRICLE PRESSURE; HEART VENTRICLE REMODELING; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TRANSVERSE AORTIC CONSTRICTION; WILD TYPE;

ALDEHYDES; ANIMALS; APOPTOSIS; BLOOD PRESSURE; CARDIOMEGALY; DOPAMINE; ENZYME ACTIVATION; FIBROSIS; MICE; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MONOAMINE OXIDASE; MYOCYTES, CARDIAC; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOSPHORYLATION; RATS; REACTIVE OXYGEN SPECIES; VENTRICULAR DYSFUNCTION; VENTRICULAR FUNCTION, LEFT;

EID: 84891823906     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4616     Document Type: Article

References (43)

1. Alnouti Y and Klaassen CD. Tissue distribution, ontogeny, and regulation of aldehyde dehydrogenase (Aldh) enzymes mRNA by prototypical microsomal enzyme inducers in mice. Toxicol Sci 101: 51-64, 2008.
2. Aries A, Paradis P, Lefebvre C, Schwartz RJ, and Nemer M. Essential role of GATA-4 in cell survival and drug-induced cardiotoxicity. Proc Natl Acad Sci U S A 101: 6975-6980, 2004.
3. Backs J, Haunstetter A, Gerber SH, Metz J, Borst MM, Strasser RH, Kubler W, and Haass M. The neuronal norepinephrine transporter in experimental heart failure: evidence for a posttranscriptional downregulation. J Mol Cell Cardiol 33: 461-472, 2001.
4. Beau SL and Saffitz JE. Transmural heterogeneity of norepinephrine uptake in failing human hearts. J Am Coll Cardiol 23: 579-585, 1994.
5. Bianchi P, Kunduzova O, Masini E, Cambon C, Bani D, Raimondi L, Seguelas MH, Nistri S, Colucci W, Leducq N, and Parini A. Oxidative stress by monoamine oxidase mediates receptor-independent cardiomyocyte apoptosis by serotonin and postischemic myocardial injury. Circulation 112: 3297-3305, 2005.
6. Bianchi P, Pimentel DR, Murphy MP, Colucci WS, and Parini A. A new hypertrophic mechanism of serotonin in cardiac myocytes: receptor-independent ROS generation. FASEB J 19: 641-643, 2005.
7. Bortolato M, Chen K, and Shih JC. Monoamine oxidase inactivation: from pathophysiology to therapeutics. Adv Drug Deliv Rev 60: 1527-1533, 2008.
8. Bueno OF, De Windt LJ, Tymitz KM, Witt SA, Kimball TR, Klevitsky R, Hewett TE, Jones SP, Lefer DJ, Peng CF, Kitsis RN, and Molkentin JD. The MEK1-ERK1/2 signaling pathway promotes compensated cardiac hypertrophy in transgenic mice. EMBO J 19: 6341-6350, 2000.
9. Burke WJ, Li SW, Chung HD, Ruggiero DA, Kristal BS, Johnson EM, Lampe P, Kumar VB, Franko M, Williams EA, and Zahm DS. Neurotoxicity of MAO metabolites of catecholamine neurotransmitters: role in neurodegenerative diseases. Neurotoxicology 25: 101-115, 2004.
10. Carpi A, Menabo R, Kaludercic N, Pelicci P, Di Lisa F, and Giorgio M. The cardioprotective effects elicited by p66(Shc) ablation demonstrate the crucial role of mitochondrial ROS formation in ischemia/reperfusion injury. Biochim Biophys Acta 1787: 774-780, 2009.
11. Chen CH, Budas GR, Churchill EN, Disatnik MH, Hurley TD, and Mochly-Rosen D. Activation of aldehyde dehydrogenase-2 reduces ischemic damage to the heart. Science 321: 1493-1495, 2008.
12. Chen CH, Sun L, and Mochly-Rosen D. Mitochondrial aldehyde dehydrogenase and cardiac diseases. Cardiovasc Res 88: 51-57, 2010.
13. Cingolani OH and Kass DA. Pressure-volume relation analysis of mouse ventricular function. Am J Physiol Heart Circ Physiol 301: H2198-H2206, 2011.
14. Diwan A and Dorn GW. Decompensation of cardiac hypertrophy: cellular mechanisms and novel therapeutic targets. Physiology (Bethesda) 22: 56-64, 2007.
15. Dorris RL. A simple method for screening monoamine oxidase (MAO) inhibitory drugs for type preference. J Pharmacol Methods 7: 133-137, 1982.
16. Eisenhofer G. The role of neuronal and extraneuronal plasma membrane transporters in the inactivation of peripheral catecholamines. Pharmacol Ther 91: 35-62, 2001.
17. Eisenhofer G, Friberg P, Rundqvist B, Quyyumi AA, Lambert G, Kaye DM, Kopin IJ, Goldstein DS, and Esler MD. Cardiac sympathetic nerve function in congestive heart failure. Circulation 93: 1667-1676, 1996.
18. Eisenhofer G, Goldstein DS, Stull R, Keiser HR, Sunderland T, Murphy DL, and Kopin IJ. Simultaneous liquid-chromatographic determination of 3,4-dihydroxyphenylglycol, catecholamines, and 3,4-dihydroxyphenylalanine in plasma, and their responses to inhibition of monoamine oxidase. Clin Chem 32: 2030-2033, 1986.
19. Georgakopoulos D and Kass DA. Protocols for hemodynamic assessment of transgenic mice in vivo. Methods Mol Biol 219: 233-243, 2003.
20. Grimsby J, Toth M, Chen K, Kumazawa T, Klaidman L, Adams JD, Karoum F, Gal J, and Shih JC. Increased stress response and beta-phenylethylamine in MAOB-deficient mice. Nat Genet 17: 206-210, 1997.
21. Hauptmann N, Grimsby J, Shih JC, and Cadenas E. The metabolism of tyramine by monoamine oxidase A/B causes oxidative damage to mitochondrial DNA. Arch Biochem Biophys 335: 295-304, 1996.
22. Himura Y, Felten SY, Kashiki M, Lewandowski TJ, Delehanty JM, and Liang CS. Cardiac noradrenergic nerve terminal abnormalities in dogs with experimental congestive heart failure. Circulation 88: 1299-1309, 1993.
23. Irwin WA, Bergamin N, Sabatelli P, Reggiani C, Megighian A, Merlini L, Braghetta P, Columbaro M, Volpin D, Bressan GM, Bernardi P, and Bonaldo P. Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat Genet 35: 367-371, 2003.
24. Kaludercic N, Carpi A, Menabo R, Di Lisa F, and Paolocci N. Monoamine oxidases (MAO) in the pathogenesis of heart failure and ischemia/reperfusion injury. Biochim Biophys Acta 1813: 1323, 2011.
25. 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, and Paolocci N. Monoamine oxidase A-mediated enhanced catabolism of norepinephrine contributes to adverse remodeling and pump failure in hearts with pressure overload. Circ Res 106: 193-202, 2010.
26. Kehat I and Molkentin JD. Extracellular signal-regulated kinase 1/2 (ERK1/2) signaling in cardiac hypertrophy. Ann N Y Acad Sci 1188: 96-102, 2010.
27. Lairez O, Calise D, Bianchi P, Ordener C, Spreux-Varoquaux O, Guilbeau-Frugier C, Escourrou G, Seif I, Roncalli J, Pizzinat N, Galinier M, Parini A, and Mialet-Perez J. Genetic deletion of MAO-A promotes serotonin-dependent ventricular hypertrophy by pressure overload. J Mol Cell Cardiol 46: 587-595, 2009.
28. Liang CS, Fan TH, Sullebarger JT, and Sakamoto S. Decreased adrenergic neuronal uptake activity in experimental right heart failure. A chamber-specific contributor to betaadrenoceptor downregulation. J Clin Invest 84: 1267-1275, 1989.
29. Maser RE and Lenhard MJ. Cardiovascular autonomic neuropathy due to diabetes mellitus: clinical manifestations, consequences, and treatment. J Clin Endocrinol Metab 90: 5896-5903, 2005.
30. Nozawa T, Igawa A, Yoshida N, Maeda M, Inoue M, Yamamura Y, Asanoi H, and Inoue H. Dual-tracer assessment of coupling between cardiac sympathetic neuronal function and downregulation of beta-receptors during development of hypertensive heart failure of rats. Circulation 97: 2359-2367, 1998.
31. Pchejetski D, Kunduzova O, Dayon A, Calise D, Seguelas MH, Leducq N, Seif I, Parini A, and Cuvillier O. Oxidative stress-dependent sphingosine kinase-1 inhibition mediates monoamine oxidase A-Associated cardiac cell apoptosis. Circ Res 100: 41-49, 2007.
32. Pop-Busui R, Kirkwood I, Schmid H, Marinescu V, Schroeder J, Larkin D, Yamada E, Raffel DM, and Stevens MJ. Sympathetic dysfunction in type 1 diabetes: association with impaired myocardial blood flow reserve and diastolic dysfunction. J Am Coll Cardiol 44: 2368-2374, 2004.
33. Purcell NH, Wilkins BJ, York A, Saba-El-Leil MK, Meloche S, Robbins J, and Molkentin JD. Genetic inhibition of cardiac ERK1/2 promotes stress-induced apoptosis and heart failure but has no effect on hypertrophy in vivo. Proc Natl Acad Sci U S A 104: 14074-14079, 2007.
34. Rees JN, Florang VR, Eckert LL, and Doorn JA. Protein reactivity of 3,4-dihydroxyphenylacetaldehyde, a toxic dopamine metabolite, is dependent on both the aldehyde and the catechol. Chem Res Toxicol 22: 1256-1263, 2009.
35. Sivasubramaniam SD, Finch CC, Rodriguez MJ, Mahy N, and Billett EE. A comparative study of the expression of monoamine oxidase-A and -B mRNA and protein in non-CNS human tissues. Cell Tissue Res 313: 291-300, 2003.
36. Takimoto E, Champion HC, Li M, Belardi D, Ren S, Rodriguez ER, Bedja D, Gabrielson KL, Wang Y, and Kass DA. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 11: 214-222, 2005.
37. Takimoto E, Champion HC, Li M, Ren S, Rodriguez ER, Tavazzi B, Lazzarino G, Paolocci N, Gabrielson KL, Wang Y, and Kass DA. Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 115: 1221-1231, 2005.
38. Takimoto E and Kass DA. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 49: 241-248, 2007.
39. Takimoto E, Yao A, Toko H, Takano H, Shimoyama M, Sonoda M, Wakimoto K, Takahashi T, Akazawa H, Mizukami M, Nagai T, Nagai R, and Komuro I. Sodium calcium exchanger plays a key role in alteration of cardiac function in response to pressure overload. FASEB J 16: 373-378, 2002.
40. Teiger E, Than VD, Richard L, Wisnewsky C, Tea BS, Gaboury L, Tremblay J, Schwartz K, and Hamet P. Apoptosis in pressure overload-induced heart hypertrophy in the rat. J Clin Invest 97: 2891-2897, 1996.
41. Villeneuve C, Guilbeau-Frugier C, Sicard P, Lairez O, Ordener C, Duparc T, De PD, 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, and Mialet-Perez J. 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: 5-18, 2013.
42. Youdim MB, Edmondson D, and Tipton KF. The therapeutic potential of monoamine oxidase inhibitors. Nat Rev Neurosci 7: 295-309, 2006.
43. Zhang Y, Babcock SA, Hu N, Maris JR, Wang H, and Ren J. Mitochondrial aldehyde dehydrogenase (ALDH2) protects against streptozotocin-induced diabetic cardiomyopathy: role of GSK3beta and mitochondrial function. BMC Med 10: 40, 2012.