Mitochondrial dysfunction causing cardiac sodium channel downregulation in cardiomyopathy

Journal of Molecular and Cellular Cardiology

Volumn 54, Issue 1, 2013, Pages 25-34

  Liu, Man ^a,b   Gu, Lianzhi ^a,b   Sulkin, Matthew S ^c   Liu, Hong ^a,b   Jeong, Euy Myoung ^a   Greener, Ian ^a   Xie, An ^a   Efimov, Igor R ^c   Dudley, Samuel C ^a,b  

^a UNIVERSITY OF ILLINOIS   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

^c WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

Heart failure; Mitochondria; NAD+; Oxidative stress; Sodium channel

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SODIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL PRESSURE; ARTICLE; CELL LEVEL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; ENZYME ACTIVATION; HEART EJECTION FRACTION; HEART LEFT VENTRICLE VOLUME; HUMAN; HUMAN TISSUE; INTRACELLULAR SIGNALING; MOLECULAR PATHOLOGY; MOUSE; NERVE CONDUCTION; NONHUMAN; NONISCHEMIC CARDIOMYOPATHY; OXIDATIVE STRESS; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN FUNCTION; SODIUM CURRENT;

ACTION POTENTIALS; ANIMALS; ANTIGENS, CD38; BENZOPHENANTHRIDINES; CARDIOMYOPATHIES; DOWN-REGULATION; FORSKOLIN; HEART CONDUCTION SYSTEM; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; NAD; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; ORGANOPHOSPHORUS COMPOUNDS; OXIDATIVE STRESS; PATCH-CLAMP TECHNIQUES; PIPERIDINES; REACTIVE OXYGEN SPECIES;

ANIMALIA; MUS;

EID: 84869869380     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2012.10.011     Document Type: Article

References (57)

1. Bardy G.H., Lee K.L., Mark D.B., Poole J.E., Packer D.L., Boineau R., et al. Amiodarone or an implantable cardioverter-defibrillator for congestive heart failure. N Engl J Med 2005, 352:225-237.
2. Kamphuis H.C.M., de Leeuw J.R.J., Derksen R., Hauer R.N.W., Winnubst J.A.M. Implantable cardioverter defibrillator recipients: quality of life in recipients with and without ICD shock delivery. Europace 2003, 5:381-389.
3. Thomas S.A., Friedmann E., Kao C.W., Inguito P., Metcalf M., Kelley F.J., et al. Quality of life and psychological status of patients with implantable cardioverter defibrillators. Am J Crit Care 2006, 15:389-398.
4. Valdivia C.R., Chu W.W., Pu J., Foell J.D., Haworth R.A., Wolff M.R., et al. Increased late sodium current in myocytes from a canine heart failure model and from failing human heart. J Mol Cell Cardiol 2005, 38:475-483.
5. Ufret-Vincenty C.A., Baro D.J., Lederer W.J., Rockman H.A., Quinones L.E., Santana L.F. Role of sodium channel deglycosylation in the genesis of cardiac arrhythmias in heart failure. J Biol Chem 2001, 276:28197-28203.
6. + currents in myocytes from epicardial border zone of the infarcted heart. A possible ionic mechanism for reduced excitability and postrepolarization refractoriness. Circ Res 1997, 81:110-119.
7. + channel function in epicardial border zone cells that survive in the infarcted canine heart?. Cardiovasc Res 2004, 64:260-267.
8. Shaw R.M., Rudy Y. Ionic mechanisms of propagation in cardiac tissue: roles of the sodium and L-type calcium currents during reduced excitability and decreased gap junction coupling. Circ Res 1997, 81:727-741.
9. + current regulation by pyridine nucleotides. Circ Res 2009, 105:737-745.
10. Liu M., Liu H., Dudley S.C. Reactive oxygen species originating from mitochondria regulate the cardiac sodium channel. Circ Res 2010, 107:967-974.
11. Aon M.A., Cortassa S., Marban E., O'Rourke B. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J Biol Chem 2003, 278:44735-44744.
12. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem 2001, 276:2571-2575.
13. Lu T., Lee H., Kabat J., Shibata E.F. Modulation of rat cardiac sodium channel by the stimulatory G protein α-subunit. J Physiol 1999, 518:371-384.
14. + regulates intracellular calcium levels and induces activation of human granulocytes. Biochem J 2006, 393:697-704.
15. + induces calcium signaling and apoptosis in human osteoblastic cells. Biochem Biophys Res Commun 2001, 285:1226-1231.
16. + repletion prevents PARP-1-induced glycolytic blockade and cell death in cultured mouse astrocytes. Biochem Biophys Res Commun 2003, 308:809-813.
17. Silberman G.A., Fan T.-H., Liu H., Jiao Z., Xiao H.D., Lovelock J.D., et al. Uncoupled cardiac nitric oxide synthase mediates diastolic dysfunction. Circulation 2010, 121:519-528.
18. O'Connor D.T., Rodrigo M., Simpson P. Isolation and culture of adult mouse cardiac myocytes. Methods Mol Biol 2007, 357:271-296.
19. 2+ exchanger: molecular partners in pacemaker regulation. Circ Res 2001, 88:1254-1258.
20. + current and causes inherited arrhythmias. Circulation 2007, 116:2260-2268.
21. Lou Q., Fedorov V.V., Glukhov A.V., Moazami N., Fast V.G., Efimov I.R. Transmural heterogeneity and remodeling of ventricular excitation-contraction coupling in human heart failure/clinical perspective. Circulation 2011, 123:1881-1890.
22. ATP channel openers diazoxide and pinacidil in coronary-perfused atria and ventricles from failing and non-failing human hearts. J Mol Cell Cardiol 2011, 51:215-225.
23. Laughner J.I., Sulkin M.S., Wu Z., Deng C.X., Efimov I.R. Three potential mechanisms for failure of high intensity focused ultrasound ablation in cardiac tissue/clinical perspective. Circ Arrhythm Electrophysiol 2012, 5:409-416.
24. Bayly P., KenKnight B., Rogers J., Hillsley R., Ideker R., Smith W. Estimation of conduction velocity vector fields from epicardial mapping data. IEEE Trans Biomed Eng 1998, 45:563-571.
25. Landmesser U., Dikalov S., Price S.R., McCann L., Fukai T., Holland S., et al. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 2003, 111:1201-1209.
26. Kellenberger E., Kuhn I., Schuber F., Muller-Steffner H. Flavonoids as inhibitors of human CD38. Bioorg Med Chem Lett 2011, 21:3939-3942.
27. López-Sendón J., Swedberg K., McMurray J., Tamargo J., Maggioni A., Dargie H., et al. Expert consensus document of b-adrenergic receptor blockers. Eur Heart J 2004, 25:1341-1362.
28. Wang D.W., Mistry A.M., Kahlig K.M., Kearney J.A., Xiang J., George A.L. Propranolol blocks cardiac and neuronal voltage-gated sodium channels. Front Pharmacol 2010, 1:144.
29. + is an agonist of the human P2Y11 purinergic receptor in human granulocytes. J Biol Chem 2006, 281:31419-31429.
30. Umapathy N.S., Zemskov E.A., Gonzales J., Gorshkov B.A., Sridhar S., Chakraborty T., et al. Extracellular β-nicotinamide adenine dinucleotide (β-NAD) promotes the endothelial cell barrier integrity via PKA- and EPAC1/Rac1-dependent actin cytoskeleton rearrangement. J Cell Physiol 2010, 223:215-223.
31. Glukhov A.V., Fedorov V.V., Kalish P.W., Ravikumar V.K., Lou Q., Janks D., et al. Conduction remodeling in human end-stage nonischemic left ventricular cardiomyopathy/clinical perspective. Circulation 2012, 125:1835-1847.
32. v1.5 and its associated proteins. Arch Mal Coeur Vaiss 2007, 100:787-793.
33. Shibata E.F., Brown T.L., Washburn Z.W., Bai J., Revak T.J., Butters C.A. Autonomic regulation of voltage-gated cardiac ion channels. J Cardiovasc Electrophysiol 2006, 17(Suppl. 1):S34-S42.
34. Akai J., Makita N., Sakurada H., Shirai N., Ueda K., Kitabatake A., et al. A novel SCN5A mutation associated with idiopathic ventricular fibrillation without typical ECG findings of Brugada syndrome. FEBS Lett 2000, 479:29-34.
35. Brugada P., Brugada R., Brugada J. The Brugada syndrome. Curr Cardiol Rep 2000, 2:507-514.
36. Makiyama T., Akao M., Tsuji K., Doi T., Ohno S., Takenaka K., et al. High risk for bradyarrhythmic complications in patients with Brugada syndrome caused by SCN5A gene mutations. J Am Coll Cardiol 2005, 46:2100-2106.
37. Beswick R.A., Zhang H., Marable D., Catravas J.D., Hill W.D., Webb R.C. Long-term antioxidant administration attenuates mineralocorticoid hypertension and renal inflammatory response. Hypertension 2001, 37:781-786.
38. Beswick R.A., Dorrance A.M., Leite R., Webb R.C. NADH/NADPH oxidase and enhanced superoxide production in the mineralocorticoid hypertensive rat. Hypertension 2001, 38:1107-1111.
39. Dikalova A.E., Bikineyeva A.T., Budzyn K., Nazarewicz R.R., McCann L., Lewis W., et al. Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 2010, 107:106-116.
40. Lin S.J., Guarente L. Nicotinamide adenine dinucleotide, a metabolic regulator of transcription, longevity and disease. Curr Opin Cell Biol 2003, 15:241-246.
41. Franco L., Guida L., Bruzzone S., Zocchi E., Usai C., Flora A.D. The transmembrane glycoprotein CD38 is a catalytically active transporter responsible for generation and influx of the second messenger cyclic ADP-ribose across membranes. FASEB J 1998, 12:1507-1520.
42. Guida L., Bruzzone S., Sturla L., Franco L., Zocchi E., De Flora A. Equilibrative and concentrative nucleoside transporters mediate influx of extracellular cyclic ADP-ribose into 3T3 murine fibroblasts. J Biol Chem 2002, 277:47097-47105.
43. Schreibmayer W., Dascal N., Lotan I., Wallner M., Weigl L. Molecular mechanism of protein kinase C modulation of sodium channel α-subunits expressed in Xenopus oocytes. FEBS Lett 1991, 291:341-344.
44. Murphy E., Steenbergen C. Preconditioning: the mitochondrial connection. Annu Rev Physiol 2007, 69:51-67.
45. Barth E., Stämmler G., Speiser B., Schaper J. Ultrastructural quantitation of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man. J Mol Cell Cardiol 1992, 24:669-681.
46. Das D.K., Maulik N. Mitochondrial function in cardiomyocytes: target for cardioprotection. Curr Opin Anaesthesiol 2005, 18:77-82.
47. Duchen M.R. Contributions of mitochondria to animal physiology: from homeostatic sensor to calcium signalling and cell death. J Physiol 1999, 516:1-17.
48. Ide T., Tsutsui H., Kinugawa S., Utsumi H., Kang D., Hattori N., et al. Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ Res 1999, 85:357-363.
49. ATP increases superoxide generation from complex I of the electron transport chain. Am J Physiol Heart Circ Physiol 2006, 291:H2067-H2074.
50. Eaton P. Protein thiol oxidation in health and disease: techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radic Biol Med 2006, 40:1889-1899.
51. Winterbourn C.C. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 2008, 4:278-286.
52. Santos C.X.C., Anilkumar N., Zhang M., Brewer A.C., Shah A.M. Redox signaling in cardiac myocytes. Free Radic Biol Med 2011, 50:777-793.
53. Lovelock J.D., Monasky M.M., Jeong E.M., Lardin H.A., Liu H., Patel B.G., et al. Ranolazine improves cardiac diastolic dysfunction through modulation of myofilament calcium sensitivity. Circ Res 2012, 110:841-850.
54. Zhou J., Shin H.G., Yi J., Shen W., Williams C.P., Murray K.T. Phosphorylation and putative ER retention signals are required for protein kinase A-mediated potentiation of cardiac sodium current. Circ Res 2002, 91:540-546.
55. Tateyama M., Kurokawa J., Terrenoire C., Rivolta I., Kass R.S. Stimulation of protein kinase C inhibits bursting in disease-linked mutant human cardiac sodium channels. Circulation 2003, 107:3216-3222.
56. Epstein A.E., DiMarco J.P., Ellenbogen K.A., Estes N.A.M., Freedman R.A., Gettes L.S., et al. ACC/AHA/HRS 2008 guidelines for device-based therapy of cardiac rhythm abnormalities: a report of the American College of Cardiology/American Heart Association Task Force on practice guidelines (writing committee to revise the ACC/AHA/NASPE 2002 guideline update for implantation of cardiac pacemakers and antiarrhythmia devices) developed in collaboration with the American Association for Thoracic Surgery and Society of Thoracic Surgeons. J Am Coll Cardiol 2008, 117:e350-e408.
57. Ruan Y., Liu N., Priori S.G. Sodium channel mutations and arrhythmias. Nat Rev Cardiol 2009, 6:337-348.