Endoplasmic reticulum Ca2+ measurements reveal that the cardiac ryanodine receptor mutations linked to cardiac arrhythmia and sudden death alter the threshold for store-overload-induced Ca2+ release

Biochemical Journal

Volumn 412, Issue 1, 2008, Pages 171-178

  Jones, Peter P ^a   Jiang, Dawei ^a   Bolstad, Jeff ^a   Hunt, Donald J ^a   Zhang, Lin ^a   Demaurex, Nicolas ^a,b   Chen, S R Wayne ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Arrhythmia; Cardiac ryanodine receptor; Catecholaminergic polymorphic ventricular tachycardia (CPVT); D1ER; Sarcoplasmic reticulum; Spontaneous Ca 2+ release

Indexed keywords

AMINO ACIDS; BINDING SITES; PROTEINS; TRANSCRIPTION;

CARDIAC RYANODINE RECEPTOR; ENDOPLASMIC RETICULUM; MUTATIONS;

CELL MEMBRANES;

CALCIUM ION; RYANODINE RECEPTOR; TACROLIMUS; CALCIUM; FK 506 BINDING PROTEIN; ISOPROTEIN;

ARTICLE; CALCIUM TRANSPORT; CELL STRAIN HEK293; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE MUTATION; GENETIC LINKAGE; HEART ARRHYTHMIA; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SUDDEN DEATH; CELL CULTURE; CHEMISTRY; GENETICS; HEART MUSCLE; METABOLISM; PHYSIOLOGY; POINT MUTATION; TRANSPORT AT THE CELLULAR LEVEL;

ARRHYTHMIAS, CARDIAC; BIOLOGICAL TRANSPORT; CALCIUM; CELLS, CULTURED; DEATH, SUDDEN, CARDIAC; ENDOPLASMIC RETICULUM; HUMANS; MYOCARDIUM; POINT MUTATION; PROTEIN BINDING; PROTEIN ISOFORMS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; TACROLIMUS BINDING PROTEIN 1A;

EID: 43549109826     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071287     Document Type: Article

References (40)

1. Marban, E. (2002) Cardiac channelopathies. Nature 415, 213-218
2. Pogwizd, S. and Bers, D. (2002) Calcium cycling in heart failure: the arrhythmia connection. J. Cardiovasc. Electrophysiol. 13, 88-91
3. Kass, R. S. and Tsien, R. W. (1982) Fluctuations in membrane current driven by intracellular calcium in cardiac Purkinje fibers. Biophys. J. 38, 259-269
4. 2+ in mammalian cardiac muscle. Nature 304, 735-738
5. ++-dependent cellular mechanical oscillations. J. Gen. Physiol. 82, 119-153
6. Wier, W., Kort, A., Stern, M., Lakatta, E. and Marban, E. (1983) Cellular calcium fluctuations in mammalian heart: direct evidence from noise analysis of aequorin signals in Purkinje fibers. Proc. Natl. Acad. Sci. U.S.A. 80, 7367-7371
7. Marban, E., Robinson, S. W. and Wier, W. G. (1986) Mechanisms of arrhythmogenic delayed and early after depolarizations in ferret ventricular muscle. J. Clin. Invest. 78, 1185-1192
8. 2+ release (SOICR). Proc. Natl. Acad. Sci. U.S.A. 101, 13062-13067
9. 2+ activation are common defects of RyR2 mutations linked to ventricular tachycardia and sudden death. Circ. Res. 97, 1173-1181
10. Ter Keurs, H. E. and Boyden, P. A. (2007) Calcium and arrhythmogenesis. Physiol. Rev. 87, 457-506
11. George, C. H., Jundi, H., Thomas, N. L., Fry, D. L. and Lai, F. A. (2007) Ryanodine receptors and ventricular arrhythmias: emerging trends in mutations, mechanisms and therapies. J. Mol. Cell. Cardiol. 42, 34-50
12. Mohamed, U., Napolitano, C. and Priori, S. G. (2007) Molecular and electrophysiological bases of catecholaminergic polymorphic ventricular tachycardia. J. Cardiovasc. Electrophysiol. 18, 791-797
13. Priori, S. G., Napolitano, C., Tiso, N., Memmi, M., Vignati, G., Bloise, R., Sorrentino, V. V. and Danieli, G. A. (2001) Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation 103, 196-200
14. Laitinen, P. J., Brown, K. M., Piippo, K., Swan, H., Devaney, J. M., Brahmbhatt, B., Donarum, E. A., Marino, M., Tiso, N., Viitasalo, M. et al. (2001) Mutations of the cardiac ryanodine receptor (RyR2) gene in familial polymorphic ventricular tachycardia. Circulation 103, 485-490
15. Tiso, N., Stephan, D. A., Nava, A., Bagattin, A., Devaney, J. M., Stanchi, F., Larderet, G., Brahmbhatt, B., Brown, K., Bauce, B. et al. (2001) Identification of mutations in the cardiac ryanodine receptor gene in families affected with arrhythmogenic right ventricular cardiomyopathy type 2 (ARVD2). Hum. Mol. Genet. 10, 189-194
16. Bauce, B., Rampazzo, A., Basso, C., Bagattin, A., Daliento, L., Tiso, N., Turrini, P., Thiene, G., Danieli, G. A. and Nava, A. (2002) Screening for ryanodine receptor type 2 mutations in families with effort-induced polymorphic ventricular arrhythmias and sudden death: early diagnosis of asymptomatic carriers. J. Am. Coll. Cardiol. 40, 341-349
17. Priori, S. G., Napolitano, C., Memmi, M., Colombi, B., Drago, F., Gasparini, M., DeSimone, L., Coltorti, F., Bloise, R., Keegan, R. et al. (2002) Clinical and molecular characterization of patients with catecholaminergic polymorphic ventricular tachycardia. Circulation 106, 69-74
18. Laitinen, P., Swan, H., Piippo, K., Viitasalo, M., Toivonen, L. and Kontula, K. (2004) Genes, exercise and sudden death: molecular basis of familial catecholaminergic polymorphic ventricular tachycardia. Ann. Med. 36, (Suppl. 1), 81-86
19. Bagattin, A., Veronese, C., Bauce, B., Wuyts, W., Settimo, L., Nava, A., Rampazzo, A. and Danieli, G. A. (2004) Denaturing HPLC-based approach for detecting RYR2 mutations involved in malignant arrhythmias. Clin. Chem. 50, 1148-1155
20. Choi, G., Kopplin, L. J., Tester, D. J., Will, M. L., Haglund, C. M. and Ackerman, M. J. (2004) Spectrum and frequency of cardiac channel defects in swimming-triggered arrhythmia syndromes. Circulation 110, 2119-2124
21. Tester, D. J., Spoon, D. B., Valdivia, H. H., Makielski, J. C. and Ackerman, M. J. (2004) Targeted mutational analysis of the RyR2-encoded cardiac ryanodine receptor in sudden unexplained death: a molecular autopsy of 49 medical examiner/coroner's cases. Mayo Clin. Proc. 79, 1380-1384
22. 2+ release channels. J. Clin. Invest. 115, 2033-2038
23. Wagenknecht, T., Radermacher, M., Grassucci, R., Berkowitz, J., Xin, H. B. and Fleischer, S. (1997) Locations of calmodulin and FK506-binding protein on the three-dimensional architecture of the skeletal muscle ryanodine receptor. J. Biol. Chem. 272, 32463-32471
24. Sharma, M. R., Jeyakumar, L. H., Fleischer, S. and Wagenknecht, T. (2002) Three-dimensional visualization of FKBP12.6 binding to cardiac ryanodine receptor (RyR2) in open buffer condition. Biophys. J. 82, 644a
25. 2+ activation in the cardiac ryanodine receptor is associated with ventricular fibrillation and sudden death. Proc. Natl. Acad. Sci. U.S.A. 104, 18309-18314
26. Welch, W., Rheault, S., West, D. J. and Williams, A. J. (2004) A model of the putative pore region of the cardiac ryanodine receptor channel. Biophys. J. 87, 2335-2351
27. 2+ release channel of skeletal muscle sarcoplasmic reticulum (RyR1). Proc. Natl. Acad. Sci. U.S.A. 99, 16725-16730
28. Lehnart, S. E., Wehrens, X. H. T., Laitinen, P. J., Reiken, S. R., Deng, S., Cheng, Z., Landry, D. W., Kontula, K., Swan, H. and Marks, A. R. (2004) Sudden death in familial polymorphic ventricular tachycardia associated with calcium release channel (ryanodine receptor) leak. Circulation 109, 3208-3214
29. 2+ release channel (ryanodine receptor). J. Biol. Chem. 278, 3786-3792
30. Ikemoto, N. and Yamamoto, T. (2002) Regulation of calcium release by interdomain interaction within ryanodine receptors. Front. Biosci. 7, 671-683
31. George, C. H., Jundi, H., Thomas, N. L., Scoote, M., Walters, N., Williams, A. J. and Lai, F. A. (2004) Ryanodine receptor regulation by intramolecular interaction between cytoplasmic and transmembrane domains. Mol. Biol. Cell 15, 2627-2638
32. 2+ analyzed with an improved genetically encoded fluorescent sensor. Proc. Natl. Acad. Sci. U.S.A. 101, 17404-17409
33. Fabiato, A. (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 157, 378-417
34. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
35. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76, 4350-4354
36. 2+ release channel (ryanodine receptor) mutant associated with ventricular tachycardia and sudden death. Circ. Res. 91, 218-225
37. 2+ leak in intact ventricular myocytes from rabbits in heart failure. Circ. Res. 93, 592-594
38. Kubalova, Z., Gyorke, I., Terentyeva, R., Viatchenko-Karpinski, S., Terentyev, D., Williams, S. C. and Gyorke, S. (2004) Modulation of cytosolic and intra-sarcoplasmic reticulum calcium waves by calsequestrin in rat cardiac myocytes. J. Physiol. 561, 515-524
39. Wehrens, X., Lehnart, S., Huang, F., Vest, J., Reiken, S., Mohler, P., Sun, J., Guatimosim, S., Song, L., 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
40. George, C. H., Higgs, G. V. and 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