Proarrhythmia in a non-failing murine model of cardiac-specific Na +/Ca2+ exchanger overexpression: Whole heart and cellular Mechanisms

Basic Research in Cardiology

Volumn 107, Issue 2, 2012, Pages

  Pott, Christian ^a   Muszynski, Adam ^a   Ruhe, Matthias ^a   Bogeholz N ^a   Schulte, Jan S ^a   Milberg, Peter ^a   Mönnig, Gerold ^a   Fabritz, Larissa ^a,b   Goldhaber, Joshua I ^c   Breithardt, Günter ^a   Schmitz, Wilhelm ^a   Philipson, Kenneth D ^d   Eckardt, Lars ^a   Kirchhof, Paulus ^a,b   Müller, Frank U ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arrhythmia; Cellular electrophysiology; Sudden cardiac death; Transgenic mice; Ventricular tachycardia

Indexed keywords

ADENOVIRUS VECTOR; GELATINASE A; GELATINASE B; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; HOMEODOMAIN PROTEIN; TLX2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME INACTIVATION; ENZYME INHIBITION; GENE OVEREXPRESSION; HEART INFARCTION; HETEROZYGOSITY; MOUSE; MOUSE MUTANT; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; SURVIVAL RATE; UPREGULATION; WILD TYPE; ACTION POTENTIAL; ANIMAL; DISEASE MODEL; ELECTROCARDIOGRAPHY; GENETICS; HEART; HEART ARRHYTHMIA; HEART MUSCLE CELL; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; ARRHYTHMIAS, CARDIAC; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ELECTROCARDIOGRAPHY; HEART; HOMEODOMAIN PROTEINS; MICE; MYOCYTES, CARDIAC; ORGAN CULTURE TECHNIQUES;

EID: 84856784190     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-012-0247-7     Document Type: Article

References (52)

1. Adachi-Akahane S, Lu L, Li Z, Frank JS, Philipson KD, Morad M (1997) Calcium signaling in transgenic mice overexpressing cardiac Na(+)-Ca2+ exchanger. J Gen Physiol 109:717-729. doi: 10.1085/jgp.109.6.717 (Pubitemid 27255937)
2. Ai X, Curran JW, Shannon TR, Bers DM, Pogwizd SM (2005) Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 97:1314-1322. doi: 10.1161/01.RES.0000194329.41863.89
3. Barandi L, Virag L, Jost N, Horvath Z, Koncz I, Papp R, Harmati G, Horvath B, Szentandrassy N, Banyasz T, Magyar J, Zaza A, Varro A, Nanasi PP (2010) Reverse rate-dependent changes are determined by baseline action potential duration in mammalian and human ventricular preparations. Basic Res Cardiol 105:315-323. doi:10.1007/s00395-009-0082-7
4. Benkusky NA, Weber CS, Scherman JA, Farrell EF, Hacker TA, John MC, Powers PA, Valdivia HH (2007) Intact beta-adrenergic response and unmodified progression toward heart failure in mice with genetic ablation of a major protein kinase A phosphorylation site in the cardiac ryanodine receptor. Circ Res 101:819-829. doi: 10.1161/CIRCRESAHA.107.153007 (Pubitemid 350287197)
5. Bers DM, Pogwizd SM, Schlotthauer K (2002) Upregulated Na/ Ca exchange is involved in both contractile dysfunction and arrhythmogenesis in heart failure. Basic Res Cardiol 97(Suppl 1):I36-I42
6. Beuckelmann DJ, Nabauer M, Erdmann E (1993) Alterations of K + currents in isolated human ventricular myocytes from patients with terminal heart failure. Circ Res 73:379-385. doi: 10.1161/01.CIR.85.3.1046 (Pubitemid 23212118)
7. Blaustein MP, Lederer WJ (1999) Sodium/calcium exchange: its physiological implications. Physiol Rev 79:763-854 (Pubitemid 29330173)
8. Bondarenko VE, Szigeti GP, Bett GC, Kim SJ, Rasmusson RL (2004) Computer model of action potential of mouse ventricular myocytes. Am J Physiol Heart Circ Physiol 287:H1378-H1403. doi:10.1152/ajpheart.00185.2003 (Pubitemid 39096689)
9. Colquhoun D, Neher E, Reuter H, Stevens CF (1981) Inward current channels activated by intracellular Ca in cultured cardiac cells. Nature 294:752-754 (Pubitemid 12174445)
10. Currie S, Quinn FR, Sayeed RA, Duncan AM, Kettlewell S, Smith GL (2005) Selective down-regulation of sub-endocardial ryanodine receptor expression in a rabbit model of left ventricular dysfunction. J Mol Cell Cardiol 39:309-317. doi:10.1016/j. yjmcc.2005.04.005 (Pubitemid 40995020)
11. De Ferrari GM, Viola MC, D'Amato E, Antolini R, Forti S (1995) Distinct patterns of calcium transients during early and delayed afterdepolarizations induced by isoproterenol in ventricular myocytes. Circulation 91:2510-2515. doi:10.1161/01. CIR.91.10.2510
12. de Groot SH, Schoenmakers M, Molenschot MM, Leunissen JD, Wellens HJ, Vos MA (2000) Contractile adaptations preserving cardiac output predispose the hypertrophied canine heart to delayed afterdepolarization-dependent ventricular arrhythmias. Circulation 102:2145-2151. doi:10.1161/01.CIR.102.17.2145
13. Fabritz L, Kirchhof P, Fortmuller L, Auchampach JA, Baba HA, Breithardt G, Neumann J, Boknik P, Schmitz W (2004) Gene dose-dependent atrial arrhythmias, heart block, and brady-cardiomyopathy in mice overexpressing A(3) adenosine receptors. Cardiovasc Res 62:500-508. doi:10.1016/j.cardiores.2004.02.004 (Pubitemid 38648964)
14. Fabritz L, Kirchhof P, Franz MR, Eckardt L, Monnig G, Milberg P, Breithardt G, Haverkamp W (2003) Prolonged action potential durations, increased dispersion of repolarization, and polymorphic ventricular tachycardia in a mouse model of proarrhythmia. Basic Res Cardiol 98:25-32. doi:10.1007/s00395- 003-0386-y (Pubitemid 36163514)
15. Guo W, Li H, London B, Nerbonne JM (2000) Functional consequences of elimination of i(to, f) and i(to, s): early afterdepolarizations, atrioventricular block, and ventricular arrhythmias in mice lacking Kv1.4 and expressing a dominant-negative Kv4 alpha subunit. Circ Res 87:73-79. doi:10.1161/01.RES.87.1.73 (Pubitemid 30456938)
16. 2+ - exchanger protein levels and diastolic function of failing human myocardium. Circulation 99:641-648. doi:10.1161/01.CIR.99.5.641 (Pubitemid 29077705)
17. Keating MT, Sanguinetti MC (2001) Molecular and cellular mechanisms of cardiac arrhythmias. Cell 104:569-580. doi: 10.1016/S0092-8674(01)00243-4 (Pubitemid 32201951)
18. Kimura S, Cameron JS, Kozlovskis PL, Bassett AL, Myerburg RJ (1984) Delayed afterdepolarizations and triggered activity induced in feline Purkinje fibers by alpha-adrenergic timulation in the presence of elevated calcium levels. Circulation 70:1074-1082. doi:10.1161/01.CIR.70.6.1074 (Pubitemid 15219369)
19. Kirchhefer U, Klimas J, Baba HA, Buchwalow IB, Fabritz L, Huls M, Matus M, Muller FU, Schmitz W, Neumann J (2007) Triadin is a critical determinant of cellular Ca cycling and contractility in the heart. Am J Physiol Heart Circ Physiol 293:H3165-H3174. doi:10.1152/ajpheart.00799.2007 (Pubitemid 350106543)
20. Kjekshus J (1990) Arrhythmias and mortality in congestive heart failure. Am J Cardiol 65:42I-48I. doi:10.1084/jem.20051151 (Pubitemid 20166451)
21. Kuhlmann MT, Kirchhof P, Klocke R, Hasib L, Stypmann J, Fabritz L, Stelljes M, Tian W, Zwiener M, Mueller M, Kienast J, Breithardt G, Nikol S (2006) G-CSF/SCF reduces inducible arrhythmias in the infarcted heart potentially via increased connexin43 expression and arteriogenesis. J Exp Med 203:87-97. doi:10.1084/jem.20051151 (Pubitemid 43139648)
22. Meszaros J, Khananshvili D, Hart G (2001) Mechanisms underlying delayed afterdepolarizations in hypertrophied left ventricular myocytes of rats. Am J Physiol Heart Circ Physiol 281:H903-H914
23. Milberg P, Klocke R, Frommeyer G, Quang TH, Dieks K, Stypmann J, Osada N, Kuhlmann M, Fehr M, Milting H, Nikol S, Waltenberger J, Breithardt G, Eckardt L (2011) G-CSF therapy reduces myocardial repolarization reserve in the presence of increased arteriogenesis, angiogenesis and connexin 43 expression in an experimental model of pacing-induced heart failure. Basic Res Cardiol 106:995-1008. doi:10.1007/s00395- 011-0230-8
24. Mitra R, Morad M (1985) A uniform enzymatic method for dissociation of myocytes from hearts and stomachs of vertebrates. Am J Physiol 249:H1056-H1060 (Pubitemid 16197350)
25. Nerbonne JM, Kass RS (2005) Molecular physiology of cardiac repolarization. Physiol Rev 85:1205-1253. doi:10.1152/physrev. 00002.2005 (Pubitemid 41362269)
26. Noble D (2002) Influence of Na/Ca exchange stoichiometry on model cardiac action potentials. Ann N Y Acad Sci 976:133-136. doi:10.1111/j.1749-6632.2002. tb04731.x (Pubitemid 36126886)
27. Nuyens D, Stengl M, Dugarmaa S, Rossenbacker T, Compernolle V, Rudy Y, Smits JF, Flameng W, Clancy CE, Moons L, Vos MA, Dewerchin M, Benndorf K, Collen D, Carmeliet E, Carmeliet P (2001) Abrupt rate accelerations or premature beats cause life-threatening arrhythmias in mice with long-QT3 syndrome. Nat Med 7:1021-1027. doi:10.1038/nm0901-1021 (Pubitemid 32937382)
28. Pogwizd SM, Bers DM (2004) Cellular basis of triggered arrhythmias in heart failure. Trends Cardiovasc Med 14:61-66. doi:10.1016/j.tcm.2003.12.002 (Pubitemid 38340848)
29. Pogwizd SM, Qi M, Yuan W, Samarel AM, Bers DM (1999) Upregulation of Na(+)/Ca(2+) exchanger expression and function in an arrhythmogenic rabbit model of heart failure. Circ Res 85:1009-1019. doi:10.1161/01.RES.85.11.1009
30. Pogwizd SM, Schlotthauer K, Li L, Yuan W, Bers DM (2001) Arrhythmogenesis and contractile dysfunction in heart failure: roles of sodium-calcium exchange, inward rectifier potassium current, and residual beta-adrenergic responsiveness. Circ Res 88:1159-1167. doi:10.1161/hh1101.091193 (Pubitemid 34132516)
31. Pott C, Goldhaber JI, Philipson KD (2007) Homozygous overexpression of the Na+-Ca2+ exchanger in mice: evidence for increased transsarcolemmal Ca2+ fluxes. Ann N Y Acad Sci 1099:310-314. doi:10.1196/annals.1387.019 (Pubitemid 47092585)
32. Pott C, Philipson KD, Goldhaber JI (2005) Excitation-contraction coupling in Na+-Ca2+ exchanger knockout mice: reducedtranssarcolemmal Ca2+ flux. Circ Res 97:1288-1295. doi: 10.1161/01.RES.0000196563.84231.21
33. Pott C, Yip M, Goldhaber JI, Philipson KD (2007) Regulation of cardiac L-type Ca2+ current in Na+-Ca2+ exchanger knockout mice: functional coupling of the Ca2+ channel and the Na+- Ca2+ exchanger. Biophys J 92:1431-1437. doi:10.1529/biophysj. 106.091538 (Pubitemid 46203203)
34. Rae J, Cooper K, Gates P, Watsky M (1991) Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37:15-26. doi:10.1016/0165-0270(91)90017-t
35. Ramirez RJ, Sah R, Liu J, Rose RA, Backx PH (2011) Intracellular [Na(+)] modulates synergy between Na(+)/Ca (2+) exchanger and L-type Ca (2+) current in cardiac excitation- contraction coupling during action potentials. Basic Res Cardiol106:967-977. doi:10.1007/s00395-011-0202-z
36. Reinecke H, Studer R, Vetter R, Holtz J, Drexler H (1996) Cardiac Na+/Ca2+ exchange activity in patients with end-stage heart failure. Cardiovasc Res 31:48-54. doi:10.1016/S0008- 6363(95)00176-x
37. Reuter H, Han T, Motter C, Philipson KD, Goldhaber JI (2004) Mice overexpressing the cardiac sodium-calcium exchanger: defects in excitation-contraction coupling. J Physiol 554:779-789. doi:10.1113/jphysiol. 2003.055046 (Pubitemid 38219891)
38. Roos KP, Jordan MC, Fishbein MC, Ritter MR, Friedlander M, Chang HC, Rahgozar P, Han T, Garcia AJ, Maclellan WR, Ross RS, Philipson KD (2007) Hypertrophy and heart failure in mice overexpressing the cardiac sodium-calcium exchanger. J Card Fail 13:318-329 (Pubitemid 46756340)
39. Salama G, London B (2007) Mouse models of long QT syndrome. J Physiol 578:43-53. doi:10.1113/jphysiol.2006.118745 (Pubitemid 44971109)
40. Shah M, Akar FG, Tomaselli GF (2005) Molecular basis of arrhythmias. Circulation 112:2517-2529 (Pubitemid 41504503)
41. Sicouri S, Antzelevitch C (1991) Afterdepolarizations and triggered activity develop in a select population of cells (M cells) in canine ventricular myocardium: the effects of acetylstrophanthidin and Bay K 8644. Pacing Clin Electrophysiol 14:1714-1720
42. Sipido KR, Varro A, Eisner D (2006) Sodium calcium exchange as a target for antiarrhythmic therapy. Handb Exp Pharmacol 171:159-199
43. Sipido KR, Volders PG, de Groot SH, Verdonck F, Van de Werf F, Wellens HJ, Vos MA (2000) Enhanced Ca(2+) release and Na/ Ca exchange activity in hypertrophied canine ventricular myocytes: potential link between contractile adaptation and arrhythmogenesis. Circulation 102:2137-2144. doi: 10.1161/01.CIR.102.17.2137
44. Sossalla S, Maurer U, Schotola H, Hartmann N, Didie M, Zimmermann WH, Jacobshagen C, Wagner S, Maier LS (2011) Diastolic dysfunction and arrhythmias caused by overexpression of CaMKIIdelta(C) can be reversed by inhibition of late Na(+) current. Basic Res Cardiol 106:263-272. doi:10.1007/s00395- 010-0136-x
45. Spencer CI, Sham JS (2003) Effects of Na+/Ca2+ Exchange induced by SR Ca2+ release on action potentials and afterdepolarizations in guinea pig ventricular myocytes. Am J Physiol Heart Circ Physiol 285:H2552-H2562. doi:10.1152/ajpheart. 00274.2003 (Pubitemid 37443073)
46. Studer R, Reinecke H, Bilger J, Eschenhagen T, Bohm M, Hasenfuss G, Just H, Holtz J, Drexler H (1994) Gene expression of the cardiac Na(+)-Ca2+ exchanger in end-stage human heart failure. Circ Res 75:443-453
47. Terracciano CM, Souza AI, Philipson KD, MacLeod KT (1998) Na+ -Ca2+ exchange and sarcoplasmic reticular Ca2+ Regulation in ventricular myocytes from transgenic mice overexpressing the Na+ -Ca2+ exchanger. J Physiol 512(Pt 3):651-667. doi: 10.1111/j.1469-7793.1998.651bd.x (Pubitemid 28505298)
48. Tseng GN, Wit AL (1987) Effects of reducing [Na+]o on catecholamine- induced delayed afterdepolarizations in atrial cells. Am J Physiol 253:H115-H125
49. Volders PG, Kulcsar A, Vos MA, Sipido KR, Wellens HJ, Lazzara R, Szabo B (1997) Similarities between early and delayed afterdepolarizations induced by isoproterenol in canine ventricular myocytes. Cardiovasc Res 34:348-359. doi: 10.1016/S0008-6363(96)00270-2 (Pubitemid 27241580)
50. Waldeyer C, Fabritz L, Fortmueller L, Gerss J, Damke D, Blana A, Laakmann S, Kreienkamp N, Volkery D, Breithardt G, Kirchhof P (2009) Regional, age-dependent, and genotype-dependent differences in ventricular action potential duration and activation time in 410 Langendorff-perfused mouse hearts. Basic Res Cardiol 104:523-533. doi:10.1007/s00395-009-0019-1
51. Wang Y, Hill JA (2010) Electrophysiological remodeling in heart failure. J Mol Cell Cardiol 48:619-632
52. Zygmunt AC, Goodrow RJ, Weigel CM (1998) INaCa and ICl(Ca) contribute to isoproterenol-induced delayed after depolarizations in midmyocardial cells. Am J Physiol 275:H1979-H1992