Mathematical modeling mechanisms of arrhythmias in transgenic mouse heart overexpressing TNF-α

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 4, 2012, Pages

  Petkova Kirova, Polina S ^a,b   London, Barry ^c   Salama, Guy ^c   Rasmusson, Randall L ^d   Bondarenko, Vladimir E ^e  

^a Department of Cell Biology and Physiology ^*  (United States)

^b INSTITUTE OF BIOPHYSICS AND BIOMEDICAL ENGINEERING   (Bulgaria)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

^e GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Action potential; Alternans; Cardiac myocytes; Computer modeling; Reentry

Indexed keywords

CALCIUM ION; TUMOR NECROSIS FACTOR ALPHA;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GAP JUNCTION; GENE OVEREXPRESSION; HEART ARRHYTHMIA; ION CURRENT; MATHEMATICAL MODEL; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; SODIUM TRANSPORT;

ACTION POTENTIALS; ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GAP JUNCTIONS; MICE; MICE, TRANSGENIC; MODELS, THEORETICAL; MYOCARDIUM; SARCOPLASMIC RETICULUM; SODIUM-CALCIUM EXCHANGER; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84857019766     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00493.2011     Document Type: Article

References (71)

1. /~ mouse with heart failure. J Mol Cell Cardiol 40: 350-360, 2006.
2. Antzelevitch C, Sicouri S, Litovsky SH, Lukas A, Krishnan SC, Di Diego JM, Gintant GA, Liu DW. Heterogeneity within the ventricular wall: electrophysiology and pharmacology of epicardial, endocardial, and M cells. Circ Res 69: 1427-1449, 1991.
3. Anumonwo JMB, Tallini YN, Vetter FJ, Jalife J. Action potential characteristics and arrhythmogenic properties of the cardiac conduction system of the murine heart. Circ Res 89: 329-335, 2001.
4. Baker LC, London B, Choi BR, Koren G, Salama G. Enhanced dispersion of repolarization and refractoriness in transgenic mouse hearts promotes reentrant ventricular tachycardia. Circ Res 86: 396-407, 2000.
5. Barry DM, Xu H, Schuessler RB, Nerbonne JM. Functional knockout of the transient outward current, long-QT syndrome, and cardiac remodeling in mice expressing a dominant-negative Kv4 a subunit. Circ Res 83: 560-567, 1998.
6. + currents in isolated human ventricular myocytes from patients with terminal heart failure. Circ Res 73: 379-385, 1993.
7. Bondarenko VE, Rasmusson RL. Simulations of propagated mouse ventricular action potentials: effects of molecular heterogeneity. Am J Physiol Heart Circ Physiol 293: H1816-H1832, 2007.
8. 2+ handling in a model of mouse ventricular tissue. Am J Physiol Heart Circ Physiol 299: H454-H469, 2010.
9. Bondarenko VE, Szigeti GP, Bett GCL, Kim SJ, Rasmusson RL. Computer model of action potential of mouse ventricular myocytes. Am J Physiol Heart Circ Physiol 287: H1378-H1403, 2004.
10. + current in isolated adult rat atrial myocytes. Am J Physiol Heart Circ Physiol 260: H1236-H1247, 1991.
11. Bradham WS, Moe G, Wendt KA, Scott AA, Konig A, Romanova M, Naik G, Spinale FG. TNF-α and myocardial matrix metalloproteinases in heart failure: relationship to LV remodeling. Am J Physiol Heart Circ Physiol 282: H1288-H1295, 2002.
12. + currents in adult mouse ventricles. J Physiol 559: 103-120, 2004.
13. 2+ dynamics and the stability of ventricular tachycardia. Biophys J 77: 2930-2941, 1999.
14. 2+ transient in rat ventricular myocytes. Circ Res 91: 585-593, 2002.
15. Feldman AM, Combes A, Wagner D, Kadakomi T, Kubota T, Li YY, McTiernan C. The role of tumor necrosis factor in the pathophysiology of heart failure. J Am Coll Cardiol 35: 537-544, 2000.
16. Fernández-Velasco M, Ruiz-Hurtado G, Hurtado O, Moro MÁ, Del-gado C. TNF-α downregulates transient outward potassium current in rat ventricular myocytes through iNOS overexpression and oxidant species generation. Am J Physiol Heart Circ Physiol 293: H238-H245, 2007.
17. 2+ exchanger in failing human myocardium. Circulation 94: 992-1002, 1996.
18. Fox JJ, McHarg JL, Gilmour RF. Ionic mechanism of electrical alternans. Am J Physiol Heart Circ Physiol 282: H516-H530, 2002.
19. Garfinkel A. Eight (or more) kinds of alternans. J Electrocardiol 40: S70-S74, 2007.
20. Gutstein DE, Morley GE, Tamaddon H, Vaidya D, Schneider MD, Chen J, Chien KR, Stuhlmann H, Fishman GI. Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43. Circ Res 88: 333-339, 2001.
21. Hasenfuss G. Alterations of calcium-regulatory proteins in heart failure. Cardiovasc Res 37: 279-289, 1998.
22. 2+ exchange activity in canine pacing-induced heart failure. Circ Res 87: 690-698, 2000.
23. Ito K, Yan X, Tajima M, Su Z, Barry WH, Lorell BH. Contractile reserve and intracellular calcium regulation in mouse myocytes from normal and hypertrophied failing hearts. Circ Res 87: 588-595, 2000.
24. Janczewski AM, Kadokami T, Lemster B, Frye CS, McTiernan C, Feldman AM. Morphological and functional changes in cardiac myocytes isolated from mice overexpressing TNF-α. Am J Physiol Heart Circ Physiol 284: H960-H969, 2003.
25. Janczewski AM, Zahid M, Lemster BH, Frye CS, Gibson G, Higuchi Y, Kranias EG, Feldman AM, McTiernan CF. Phospholamban gene ablation improves calcium transients but not cardiac function in a heart failure model. Cardiovasc Res 62: 468-480, 2004.
26. 2+ homeostasis and cardiomyocyte function. J Biol Chem 275: 38073-38080, 2000.
27. Kääb S, Nuss HB, Chiamvimonvat N, O'Rourke B, Pak PH, Kass DA, Marban E, Tomaselli GF. Ionic mechanism of action potential prolongation in ventricular myocytes from dogs with pacing-induced heart failure. Circ Res 78: 262-273, 1996.
28. 2+ channel pathways. J Clin Invest 103: 1089-1097, 1999.
29. Knollmann BC, Katchman AN, Franz MR. Monophasic action potential recordings from intact mouse heart: validation, regional heterogeneity, and relation to refractoriness. J Cardiovasc Electrophysiol 12: 1286-1294, 2001.
30. Knollmann BC, Knollmann-Ritschel BEC, Weissman NJ, Jones LR, Morad M. Remodelling of transgenic mice overexpressing calsequestrin. J Physiol 525: 483-498, 2000.
31. Knollmann BC, Schober T, Petersen AO, Sirenko SG, Franz MR. Action potential characterization in intact mouse heart: steady-state cycle length dependence and electrical restitution. Am J Physiol Heart Circ Physiol 292: H614-H621, 2007.
32. Kubota T, Bounoutas GS, Miyagishima M, Kadokami T, Sanders VJ, Bruton C, Robbins PD, McTiernan CF, Feldman AM. Soluble tumor necrosis factor receptor abrogates myocardial inflammation but not hypertrophy in cytokine-induced cardiomyopathy. Circulation 101: 2518-2525, 2000.
33. Kubota T, McTiernan C, Frye CS, Slawson SE, Lemsster BH, Kore-tsky AP, Demetris AJ, Feldman AM. Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-α. Circ Res 81: 627-635, 1997.
34. Kwak BR, Hermans MMP, De Jonge HR, Lohmann SM, Jongsma HJ, Chanson M. Differential regulation of distinct types of gap junction channels by similar phosphorylating conditions. Mol Biol Cell 6: 1707-1719, 1995.
35. Lee SH, Chen YC, Chen YJ, Chang SL, Tai CT, Wongcharoen W, Yeh HI, Lin CI, Chen SA. Tumor necrosis factor-α alters calcium handling and increases arrhythmogenesis of pulmonary vein cardiomyo-cytes. Life Sci 80: 1806-1815, 2007.
36. Levine B, Kalman J, Mayer L, Fillit HM, Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. N Engl J Med 323: 236-241, 1990.
37. Li L, Chu G, Kranias EG, Bers DM. Cardiac myocyte calcium transport in phospholamban knockout mouse: relaxation and endogenous CaMKII effects. Am J Physiol Heart Circ Physiol 274: H1335-H1347, 1998.
38. London B, Baker LC, Lee JS, Shusterman V, Choi BR, Kubota T, McTiernan CF, Feldman AM, Salama G. Calcium-dependent arrhythmias in transgenic mice with heart failure. Am J Physiol Heart Circ Physiol 284: H431-H441, 2003.
39. London B, Baker LC, Petkova-Kirova P, Nerbonne JM, Choi BR, Salama G. Dispersion of repolarization and refractoriness are determinants of arrhythmia phenotype in transgenic mice with long QT. J Physiol 578: 115-129, 2007.
40. LouchWE, Hougen K, Mørk HK, Swift F, Aronsen JM, Sjaastad I, Reims HM, Roald B, Andersson KB, Christensen G, Sejersted OM. Sodium accumulation promotes diastolic dysfunction in end-stage heart failure following Serca2 knockout. J Physiol 588: 465-478, 2010.
41. Luo CH, Rudy Y. A dynamic model of the cardiac ventricular action potential. I. Simulations of ionic currents and concentration changes. Circ Res 74: 1071-1096, 1994.
42. 2+ release. Circ Res 92: 904-911, 2003.
43. Moe GW, Armstrong P. Pacing-induced heart failure: a model to study the mechanism of disease progression and novel therapy in heart failure. Cardiovasc Res 42: 591-599, 1999.
44. Muñoz V, Noujaim SF, Jalife J. Dynamics and molecular mechanisms of ventricular tachycardia and fibrillation in normal hearts. In: Cardiac Electrophysiology: From Cell to Bedside (5th ed.), edited by Zipes DP and Jalife J. Philadelphia, PA: Saunders, 2009.
45. Nattel S, Maguy A, Le Bouter S, Yeh YH. Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev 87: 425-456, 2007.
46. + current (Ik1) in the mouse heart accelerates and stabilizes rotors. J Physiol 578: 315-326, 2007.
47. Panfilov AV. Theory of reentry. In: Cardiac Electrophysiology: From Cell to Bedside (5th ed.), edited by Zipes DP and Jalife J. Philadelphia, PA: Saunders, 2009.
48. Peters NS, Coromilas J, Severs NJ, Wit AL. Disturbed connexin43 gap junction distribution correlates with the location of reentrant circuits in the epicardial border zone of healing canine infarcts that cause ventricular tachycardia. Circulation 95: 988-996, 1997.
49. Peters NS, Green CR, Poole-Wilson PA, Severs NJ. Reduced content of connexin43 gap junctions in ventricular myocardium from hypertrophied and ischemic human hearts. Circulation 88: 864-875, 1993.
50. Petkova-Kirova PS, Gursoy E, Mehdi H, McTiernan CF, London B, Salama G. Electrical remodeling of cardiac myocytes from mice with heart failure due to the overexpression of tumor necrosis factor-α. Am J Physiol Heart Circ Physiol 290: H2098-H2107, 2006.
51. Piacentino V, III, Weber CR, Chen X, Weisser-Thomas J, Margu-lies KB, Bers DM, Houser SR. Cellular basis of abnormal calcium transients of failing human ventricular myocytes. Circ Res 92: 651-658, 2003.
52. Pruvot EJ, Katra RP, Rosenbaum DS, Laurita KR. Role of calcium cycling versus restitution in the mechanism of repolarization alternans. Circ Res 94: 1083-1090, 2004.
53. Roden DM. Early after-depolarizations and torsade de pointes: implications for the control of cardiac arrhythmias by prolonging repolarization. Eur Heart J 14, Suppl H: 56-61, 1993.
54. Sampson KJ, Henriquez CS. Electrotonic influences on action potential duration dispersion in small hearts: a simulation study. Am J Physiol Heart Circ Physiol 289: H350-H360, 2005.
55. Sawaya SE, Rajawat YS, Rami TG, Szalai G, Price RL, Sivasubra-manian N, Mann DL, Khoury DS. Downregulation of connexin40 and increased prevalence of atrial arrhythmias in transgenic mice with cardiac-restricted overexpression of tumor necrosis factor. Am J Physiol Heart Circ Physiol 292: H1561-H1567, 2007.
56. + current in H9c2 rat ventricular cell line: biophys-ical property and molecular identity. Cell Physiol Biochem 12: 215- 226, 2002.
57. Shiferaw Y, Watanabe MA, Garfinkel A, Weiss JN, Karma A. Model of intracellular calcium cycling in ventricular myocytes. Biophys J 85: 3666-3686, 2003.
58. Shimizu W, Antzelevitch C. Cellular basis for the ECG features of the LQT1 form of the long-QT syndrome: effects of (3-adrenergic agonists and antagonists and sodium channel blockers on transmural dispersion of repolarization and Torsade de Pointes. Circulation 98: 2314-2322, 1998.
59. Sipido KR, Volders PGA, Vos MA, Verdonck F. Altered Na/Ca exchange activity in cardiac hypertrophy and heart failure: a new target for therapy? Cardiovasc Res 53: 782-805, 2002.
60. 2+ exchanger in end-stage human heart failure. Circ Res 75: 443-453, 1994.
61. Torre-Amione G, Kapadia S, Lee J, Durand JB, Bies MD, Young JB, Mann DL. Tumor necrosis factor-α and tumor necrosis receptors in the failing human heart. Circulation 96: 704-711, 1996.
62. Vaidya D, Morley GE, Samie FH, Jalife J. Reentry and fibrillation in the mouse heart. A challenge to the critical mass hypothesis. Circ Res 85: 174-181, 1999.
63. van Rijen HVM, van Kempen MJA, Postma S, Jingsma HJ. Tumor necrosis factor a alters the expression of connexin43, connexin40, and connexin37 in human umbilical vein endothelial cells. Cytokine 10: 258-264, 1998.
64. Walker ML, Rosenbaum DS. Repolarization alternans: implications for the mechanism and prevention of sudden cardiac death. Cardiovasc Res 57: 599-614, 2003.
65. 2+]i transients in cardiac myocytes at physiological stimulation frequencies. Am J Physiol Heart Circ Physiol 294: H2352-H2362, 2008.
66. ++. J Gen Physiol 95: 1061-1075, 1990.
67. + currents in adult mouse ventricular myocytes. J Gen Physiol 113: 661-677, 1999.
68. Yatani A, Frank K, Sako H, Kranias EG, Dorn GW. Cardiac-specific overexpression of Gaq alters excitation-contraction coupling in isolated cardiac myocytes. J Mol Cell Cardiol 31: 1327-1336, 1999.
69. Yokoyama T, Vaca L, Rossen RD, Durante W, Hazarika P, Mann DL. Cellular basis for the negative inotropic effects of tumor necrosis factor-α in the adult mammalian heart. J Clin Invest 92: 2303-2012, 1993.
70. 2+ exchanger: role of phosphorylation. J Biol Chem 281: 7784-7792, 2006.
71. Zhou J, Jeron A, London B, Han X, Koren G. Characterization of a slowly inactivating outward current in adult mouse ventricular myocytes. Circ Res 83: 806-814, 1998.