Physiological consequences of the P2328S mutation in the ryanodine receptor (RyR2) gene in genetically modified murine hearts

Acta Physiologica

Volumn 194, Issue 2, 2008, Pages 123-140

  Goddard, C A ^a   Ghais, N S ^a   Zhang, Y ^a   Williams, A J ^b   Colledge, W H ^a   Grace, A A ^a   Huang, C L H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

Cardiac action potentials; Cardiac arrhythmogenesis; Catecholaminergic polymorphic ventricular tachycardia; Genetically modified mice; P2328S RyR2; Ryanodine receptor

Indexed keywords

ISOPRENALINE; RYANODINE RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARRHYTHMOGENESIS; ARTICLE; CALCIUM CURRENT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE; GENE DOSAGE; GENE MUTATION; HEART MUSCLE CAPILLARY; HEART MUSCLE POTENTIAL; HETEROZYGOTE; HOMOZYGOTE; ISOLATED HEART; MALE; MOUSE; NONHUMAN; POLYMORPHIC VENTRICULAR TACHYCARDIA; PRIORITY JOURNAL; RYR2 GENE; TRANSGENIC MOUSE;

ACTION POTENTIALS; ANIMALS; CALCIUM; CARDIAC PACING, ARTIFICIAL; CELLS, CULTURED; HETEROZYGOTE; HOMEOSTASIS; HOMOZYGOTE; MICE; MICE, TRANSGENIC; MUTATION; MYOCYTES, CARDIAC; ORGAN CULTURE TECHNIQUES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; TACHYCARDIA, VENTRICULAR;

EID: 51449100865     PISSN: 17481708     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2008.01865.x     Document Type: Article

References (63)

1. Allouis, M., Probst, V., Jaafar, P., Schott, J.J. Le Marec, H. 2005. Unusual clinical presentation in a family with catecholaminergic polymorphic ventricular tachycardia due to a G14876A ryanodine receptor gene mutation. Am J Cardiol 95, 700 702.
2. d'Amati, G., Bagattin, A., Bauce, B., Rampazzo, A., Autore, C., Basso, C., King, K., Romeo, M.D., Gallo, P., Thiene, G., Danieli, G.A. Nava, A. 2005. Juvenile sudden death in a family with polymorphic ventricular arrhythmias caused by a novel RyR2 gene mutation: evidence of specific morphological substrates. Hum Pathol 36, 761 767.
3. Balasubramaniam, R., Grace, A.A., Saumarez, R.C., Vandenberg, J.I. Huang, C.L. 2003. Electrogram prolongation and nifedipine-suppressible ventricular arrhythmias in mice following targeted disruption of KCNE1. J Physiol 552, 535 546.
4. 2+ homeostasis. Am J Physiol Heart Circ Physiol 289, H1584 H1593.
5. Bers, D.M. 2002. Cardiac excitation-contraction coupling. Nature, 415, 198 205.
6. Brilliantes, A.B., Ondrias, K., Scott, A., Kobrinsky, E., Ondriasova, E., Moschella, M., Jayaraman, T., Landers, M., Ehrlich, B.E. Marks, A.R. 1994. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77, 513 523.
7. Cerrone, M., Colombi, B., Santoro, M., di Barletta, M.R., Scelsi, M., Villani, L., Napolitano, C. Priori, S.G. 2005. Bidirectional ventricular tachycardia and fibrillation elicited in a knock-in mouse model carrier of a mutation in the cardiac ryanodine receptor. Circ Res, 96, e77 e82.
8. Cerrone, M., Noujaim, S.F., Tolkacheva, E.G., Talkachou, A., O'Connell, R., Berenfeld, O., Anumonwo, J., Pandit, S.V., Vikstrom, K., Napolitano, C., Priori, S.G. Jalife, J. 2007. Arrhythmogenic mechanisms in a mouse model of catecholaminergic polymorphic ventricular tachycardia. Circ Res 101, 1039 1048.
9. 2+ and trigger ventricular arrhythmias in mice. Circ Res 101, 617 626.
10. Danik, S., Cabo, C., Chiello, C., Kang, S., Wit, A.L. Coromilas, J. 2002. Correlation of repolarization of ventricular monophasic action potential with ECG in the murine heart. Am J Physiol Heart Circ Physiol 283, H372 H381.
11. 2+ release. J Physiol 501, 3 16.
12. Francis, J., Sankar, V., Nair, V.K. Priori, S.G. 2005. Catecholaminergic polymorphic ventricular tachycardia. Heart Rhythm 2, 550 554.
13. George, C.H., Higgs, G.V. Lai, F.A. 2003. Ryanodine receptor mutations associated with stress-induced ventricular tachycardia mediate increased calcium release in stimulated cardiomyocytes. Circ Res 93, 531 540.
14. George, C.H., Jundi, H., Thomas, N.L., Scoote, M., Walters, N., Williams, A.J. Lai, F.A. 2004. Ryanodine receptor regulation by intramolecular interaction between cytoplasmic and transmembrane domains. Mol Biol Cell 15, 2627 2638.
15. 2+ release channel dysfunction. Circ Res 98, 88 97.
16. George, C.H., Jundi, H., Thomas, N.L., Fry, D.L. Lai, F.A. 2007. Ryanodine receptors and ventricular arrhythmias: emerging trends in mutations, mechanisms and therapies. J Mol Cell Cardiol 42, 34 50.
17. 2+ channels and ryanodine receptors: insights into regulation by FKPP 12.6. Am J Physiol Cell Physiol 289, C1476 1484.
18. + current diversity in mouse ventricular myocytes. J Physiol 521, 587 599.
19. Harding, S.E., Jones, S.M., O'Gara, P., del Monte, F., Vescovo, G. Poole-Wilson, P.A. 1992. Isolated ventricular myocytes from failing and non-failing human heart; the relation of age and clinical status of patients to isoproterenol response. J Mol Cell Cardiol 24, 549 564.
20. Head, C.E., Balasubramaniam, R., Thomas, G., Goddard, C.A., Lei, M., Colledge, W.H., Grace, A.A. Huang, C.L-H. 2005. Paced electrogram fractionation analysis (PEFA) of arrhythmogenic tendency in ΔKPQ Scn5a (Long QT3) mice. J Cardiovasc Electrophysiol 16, 1329 1340.
21. 2+ release (SOICR). Proc Natl Acad Sci USA 101, 13062 13067.
22. 2+ activation are common defects of RyR2 mutations linked to ventricular tachycardia and sudden death. Circ Res 97, 1173 1181.
23. Kannankeril, P.J., Mitchell, B.M., Goonasekera, S.A., Chelu, M.G., Zhang, W., Sood, S., Kearney, D.L., Danila, C.I., De Biasi, M., Wehrens, X.H. et al. 2006. Mice with the R176Q cardiac ryanodine receptor mutation exhibit catecholamine-induced ventricular tachycardia and cardiomyopathy. Proc Natl Acad Sci USA 103, 12179 12184.
24. Keating, M.T. Sanguinetti, M.C. 2001. Molecular and cellular mechanisms of caridiac arrhythmias. Cell 104, 569 580.
25. Kontula, K., Laitinen, P.J., Lehtonen, A., Toivonen, L., Viitasalo, M. Swan, H. 2005. Catecholaminergic polymorphic ventricular tachycardia: recent mechanistic insights. Cardiovasc Res 67, 379 387.
26. Kummer, J.L., Nair, R. Krishnan, S.C. 2006. Images in cardiovascular medicine. Bidirectional ventricular tachycardia caused by digitalis toxicity. Circulation, 113, e156 e157.
27. Laitinen, P.J., Brown, K.M., Piippo, K., Swan, H., Devaney, J.M., Brahmbhatt, B., Donarum, E.A., Marino, M., Tiso, N., Viitasalo, M., Toivonen, L., Stephan, D.A. Kontula, K. 2001. Mutations of the cardiac ryanodine receptor (RyR2) gene in familial polymorphic ventricular tachycardia. Circulation 103, 485 490.
28. Laurita, K.R. Katra, R.P. 2005. Delayed after depolarization-mediated triggered activity associated with slow calcium sequestration near the endocardium. J Cardiovasc Electrophysiol 16, 418 424.
29. Leenhardt, A., Lucet, V., Denjoy, I., Grau, F., Ngoc, D.D. Coumel, P. 1995. Catecholaminergic polymorphic ventricular tachycardia in children. A 7-year follow-up of 21 patients. Circulation 91, 1512 1519.
30. Lehnart, S.E., Wehrens, X.H., Laitinen, P.J., Reiken, S.R., Deng, S.X., Cheng, Z., Landry, D.W., Kontula, K., Swan, H. Marks, A.R. 2004. Sudden death in familial polymorphic ventricular tachycardia associated with calcium release channel (ryanodine receptor) leak. Circulation 109, 3208 3214.
31. Liu, N., Colombi, B., Memmi, M., Zissimopoulos, S., Rizzi, N., Negri, S., Imbriani, M., Napolitano, C., Lai, F.A. Priori, S.G. 2006. Arrhythmogenesis in catecholaminergic polymorphic ventricular tachycardia: insights from a RyR2 R4496C knock-in mouse model. Circ Res 99, 292 298.
32. London, B. 2001. Cardiac arrhythmias: from (transgenic) mice to men. J Cardiovasc Electrophysiol 12, 1089 1091.
33. Maguire, C.T., Wakimoto, H., Patel, V.V., Hammer, P.E., Gauvreau, K. Berul, C.I. 2003. Implications of ventricular arrhythmia vulnerability during murine electrophysiology studies. Physiol Genomics 15, 84 91.
34. 2+ release channel (ryanodine receptor). J Biol Chem 278, 3786 3792.
35. 2+ waves. Eur Heart J 28, 1135 1142.
36. Papadatos, G.A., Wallerstein, P.M., Head, C.E., Ratcliff, R., Brady, P.A., Benndorf, K., Saumarez, R.C., Trezise, A.E., Huang, C.L., Vandenberg, J.I., Colledge, W.H. Grace, A.A. 2002. Slowed conduction and ventricular tachycardia after targeted disruption of the cardiac sodium channel gene Scn5a. Proc Natl Acad Sci USA, 99 6210 6215.
37. Phrommintikul, A. Chattipakorn, N. 2006. Roles of cardiac ryanodine receptor in heart failure and sudden cardiac death. Int J Cardiol 112, 142 152.
38. Postma, A.V., Denjoy, I., Kamblock, J., Alders, M., Lupoglazoff, J.M., Vaksmann, G., Dubosq-Bidot, L., Sebillon, P., Mannens, M.M., Guicheney, P. Wilde, A.A. 2005. Catecholaminergic polymorphic ventricular tachycardia: RYR2 mutations, bradycardia, and follow up of the patients. J Med Genet 42, 863 870.
39. Priori, S.G. Napolitano, C. 2005. Intracellular calcium handling dysfunction and arrhythmogenesis: a new challenge for the electrophysiologist. Circ Res 97, 1077 1079.
40. Priori, S.G., Napolitano, C., Tiso, N., Memmi, M., Vignati, G., Bloise, R., Sorrentino, V. Danieli, G.A. 2001. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation 103, 196 200.
41. Priori, S.G., Napolitano, C., Memmi, M., Colombi, B., Drago, F., Gasparini, M., DeSimone, L., Coltorti, F., Bloise, R., Keegan, R., Cruz Filho, F.E., Vignati, G., Benatar, A. DeLogu, A. 2002. Clinical and molecular characterization of patients with catecholaminergic polymorphic ventricular tachycardia. Circulation 106, 69 74.
42. Rosen, M.R. Danilo, P., Jr. 1980. Effects of tetrodotoxin, lidocaine, verapamil, and AHR-2666 on ouabain-induced delayed afterdepolarizations in canine Purkinje fibers. Circ Res 46, 117 124.
43. Saumarez, R.C. Grace, A.A. 2000. Paced ventricular electrogram fractionation and sudden death in hypertrophic cardiomyopathy and other non-coronary heart diseases. Cardiovasc Res 47, 11 22.
44. Saumarez, R.C., Chojnowska, L., Derksen, R., Pytkowski, M., Sterlinski, M., Huang, C.L., Sadoul, N., Hauer, R.N., Ruzyłło, W. Grace, A.A. 2003. Sudden death in noncoronary heart disease is associated with delayed paced ventricular activation. Circulation 107, 2595 2600.
45. Scoote, M. Williams, A.J. 2002. The cardiac ryanodine receptor (calcium release channel): emerging role in heart failure and arrhythmia pathogenesis. Cardiovasc Res 56, 359 372.
46. +/- murine hearts. J Physiol 581, 255 275.
47. +/Δ murine hearts modelling long QT(3) syndrome. J Physiol 578, 69 84.
48. Swan, H., Piippo, K., Viitasalo, M., Heikkila, P., Paavonen, T., Kainulainen, K., Kere, J., Keto, P., Kontula, K. Toivonen, L. 1999. Arrhythmic disorder mapped to chromosome 1q42-q43 causes malignant polymorphic ventricular tachycardia in structurally normal hearts. J Am Coll Cardiol 34, 2035 2042.
49. Thomas, N.L., George, C.H. Lai, F.A. 2004. Functional heterogeneity of ryanodine receptor mutations associated with sudden cardiac death. Cardiovasc Res 64, 52 60.
50. Thomas, N.L., George, C.H. Lai, F.A. 2006. Role of ryanodine receptor mutations in cardiac pathology: more questions than answers? Biochem Soc Trans 34, 913 918.
51. 2+ channel antagonism on ventricular arrhythmogenesis in ΔKPQ-Scn5a (long QT3) murine hearts. J Physiol 578, 85 97.
52. Thomas, G., Killeen, M.J., Gurung, I.S., Hakim, P., Balasubramaniam, R., Goddard, C.A., Grace, A.A. Huang, C.L-H. 2007b. Mechanisms of ventricular arrhythmogenesis in mice following targeted disruption of KCNE1 modelling long QT syndrome 5. J Physiol 578, 99 114.
53. Tiso, N., Salamon, M., Bagattin, A., Danieli, G.A., Argenton, F. Bortolussi, M. 2002. The binding of the RyR2 calcium channel to its gating protein FKBP12.6 is oppositely affected by ARVD2 and VTSIP mutations. Biochem Biophys Res Commun 299, 594 598.
54. Tunwell, R.E., Wickenden, C., Bertrand, B.M., Shevchenko, V.I., Walsh, M.B., Allen, P.D. Lai, F.A. 1996. The human cardiac muscle ryanodine receptor-calcium release channel: identification, primary structure and topological analysis. Biochem J 318, 477 487.
55. Vaidya, D., Morley, G.E., Samie, F.H. Jalife, S.J. 1999. Reentry and fibrillation in the mouse heart. Circ Res 85, 174 181.
56. Venetucci, L.A., Trafford, A.W. Eisner, D.A. 2007. Increasing ryanodine receptor open probability alone does not produce arrhythmogenic calcium waves: threshold sarcoplasmic reticulum calcium content is required. Circ Res 100, 105 111.
57. Wehrens, X.H. Marks, A.R. 2003. Altered function and regulation of cardiac ryanodine receptors in cardiac disease. Trends Biochem Sci 28, 671 678.
58. Wehrens, X.H., Lehnart, S.E., Huang, F., Vest, J.A., Reiken, S.R., Mohler, P.J., Sun, J., Guatimosim, S., Song, L.S., Rosemblit, N. et al. 2003. FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 113, 829 840.
59. Wehrens, X.H., Lehnart, S.E., Reiken, S.R., Deng, S.X., Vest, J.A., Cervantes, D., Coromilas, J., Landry, D.W. Marks, A.R. 2004. Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin2. Science 304, 292 296.
60. 2+ leak through ryanodine receptor in heart failure. Circulation 102, 2131 2136.
61. 2+ handling in heart failure. J Clin Invest 115, 556 564.
62. Yano, M., Yamamoto, T., Ikemoto, N. Matsuzaki, M. 2005b. Abnormal ryanodine receptor function in heart failure. Pharmacol Ther 107, 377 391.
63. Zissimopoulos, S. Lai, F.A. 2005. Interaction of FKBP12.6 with the cardiac ryanodine receptor C-terminal domain. J Biol Chem 280, 5475 5485.