Abnormal termination of Ca 2+ release is a common defect of RyR2 mutations associated with cardiomyopathies

Circulation Research

Volumn 110, Issue 7, 2012, Pages 968-977

  Tang, Yijun ^a,c   Tian, Xixi ^a   Wang, Ruiwu ^a   Fill, Michael ^b   Chen, S R Wayne ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c HUBEI UNIVERSITY OF MEDICINE   (China)

Author keywords

Ca 2+; cardiac arrhythmias; cardiomyopathies; release termination; ryanodine receptor mutations; sarcoplasmic reticulum

Indexed keywords

CALCIUM ION; RYANODINE RECEPTOR 2; CALCIUM; GREEN FLUORESCENT PROTEIN; RYANODINE RECEPTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CARDIOMYOPATHY; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; CELL STRAIN HEK293; CONGESTIVE CARDIOMYOPATHY; CYTOSOL; EXON; GENE DELETION; HEART MUSCLE CELL; HEART RIGHT VENTRICLE DYSPLASIA; HUMAN; HUMAN CELL; HYPERTROPHIC CARDIOMYOPATHY; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; ANIMAL; ANIMAL MODEL; CELL CULTURE; CELL LINE; CYTOLOGY; GENETIC TRANSFECTION; GENETICS; KIDNEY; METABOLISM; PATHOLOGY; SARCOPLASMIC RETICULUM;

ANIMALS; ARRHYTHMOGENIC RIGHT VENTRICULAR DYSPLASIA; CALCIUM; CARDIOMYOPATHIES; CARDIOMYOPATHY, HYPERTROPHIC; CELL LINE; CELLS, CULTURED; EXONS; GENE DELETION; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; KIDNEY; MICE; MODELS, ANIMAL; MUTATION; MYOCYTES, CARDIAC; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; TRANSFECTION;

EID: 84862832753     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.256560     Document Type: Article

References (57)

1. Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415: 198-205. (Pubitemid 34059525)
2. Pogwizd SM, Bers DM. Cellular basis of triggered arrhythmias in heart failure. Trends Cardiovasc Med. 2004;14:61-66. (Pubitemid 38340848)
3. Venetucci LA, Trafford AW, O'Neill SC, Eisner DA. The sarcoplasmic reticulum and arrhythmogenic calcium release. Cardiovasc Res. 2008;77: 285-292. (Pubitemid 351197634)
4. George CH, Jundi H, Thomas NL, Fry DL, Lai FA. Ryanodine receptors and ventricular arrhythmias: emerging trends in mutations, mechanisms and therapies. J Mol Cell Cardiol. 2007;42:34-50. (Pubitemid 44958614)
5. Mohamed U, Napolitano C, Priori SG. Molecular and electrophysiological bases of catecholaminergic polymorphic ventricular tachycardia. J Cardiovasc Electrophysiol. 2007;18:791-797. (Pubitemid 46934514)
6. Priori SG, Chen SR. Inherited dysfunction of sarcoplasmic reticulum Ca2+handling and arrhythmogenesis. Circ Res. 2011;108:871-883.
7. Medeiros-Domingo A, Bhuiyan ZA, Tester DJ, Hofman N, Bikker H, van Tintelen JP, Mannens MM, Wilde AA, Ackerman MJ. The RYR2-encoded ryanodine receptor/calcium release channel in patients diagnosed previously with either catecholaminergic polymorphic ventricular tachycardia or genotype negative, exercise-induced long QT syndrome: A comprehensive open reading frame mutational analysis. J Am Coll Cardiol. 2009;54:2065-2074.
8. Bhuiyan ZA, van den Berg MP, van Tintelen JP, Bink-Boelkens MT, Wiesfeld AC, Alders M, Postma AV, van Langen I, Mannens MM, Wilde AA. Expanding spectrum of human RYR2-related disease: New electrocardiographic, structural, and genetic features. Circulation. 2007;116: 1569-1576. (Pubitemid 47511420)
9. Marjamaa A, Laitinen-Forsblom P, Lahtinen AM, Viitasalo M, Toivonen L, Kontula K, Swan H. Search for cardiac calcium cycling gene mutations in familial ventricular arrhythmias resembling catecholaminergic polymorphic ventricular tachycardia. BMC Med Genet. 2009;10:12.
10. Tiso N, Stephan DA, Nava A, Bagattin A, Devaney JM, Stanchi F, Larderet G, Brahmbhatt B, Brown K, Bauce B, Muriago M, Basso C, Thiene G, Danieli GA, Rampazzo A. Identification of mutations in the cardiac ryanodine receptor gene in families affected with arrhythmogenic right ventricular cardiomyopathy type 2 (ARVD2). Hum Mol Genet. 2001;10:189-194. (Pubitemid 32123976)
11. Bauce B, Rampazzo A, Basso C, Bagattin A, Daliento L, Tiso N, Turrini P, Thiene G, Danieli GA, Nava A. 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. 2002;40:341-349. (Pubitemid 34756298)
12. Tester DJ, Spoon DB, Valdivia HH, Makielski JC, Ackerman MJ. 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. 2004;79:1380-1384. (Pubitemid 39453301)
13. d'Amati G, Bagattin A, Bauce B, Rampazzo A, Autore C, Basso C, King K, Romeo MD, Gallo P, Thiene G, Danieli GA, Nava A. Juvenile sudden death in a family with polymorphic ventricular arrhythmias caused by a novel RyR2 gene mutation: Evidence of specific morphological substrates. Hum Pathol. 2005;36:761-767. (Pubitemid 41112031)
14. Nishio H, Iwata M, Suzuki K. Postmortem molecular screening for cardiac ryanodine receptor type 2 mutations in sudden unexplained death: R420W mutated case with characteristics of status thymico-lymphatics. Circ J. 2006;70:1402-1406. (Pubitemid 44672894)
15. Noboru F, Hidekazu I, Kenshi H, Katsuharu U, Mitsuru N, Tetsuo K, Hiromasa K, Yuichiro S, Toshinari T, Kazuo O, Sumio M, Masakazu Y. A novel missense mutation in cardiac ryanodine receptor gene as a possible cause of hypertrophic cardiomyopathy: Evidence from familial analysis. Circulation. 2006;114:165.
16. Kass RS, Tsien RW. Fluctuations in membrane current driven by intracellular calcium in cardiac Purkinje fibers. Biophys J. 1982;38:259-269. (Pubitemid 12019588)
17. Stern MD, Kort AA, Bhatnagar GM, Lakatta EG. Scattered-light intensity fluctuations in diastolic rat cardiac muscle caused by spontaneous Ca2+-dependent cellular mechanical oscillations. J Gen Physiol. 1983;82: 119-153. (Pubitemid 13034088)
18. Orchard CH, Eisner DA, Allen DG. Oscillations of intracellular Ca2+in mammalian cardiac muscle. Nature. 1983;304:735-738. (Pubitemid 13037721)
19. Wier WG, Kort AA, Stern MD, Lakatta EG, Marban E. Cellular calcium fluctuations in mammalian heart: Direct evidence from noise analysis of aequorin signals in Purkinje fibers. Proc Natl Acad Sci USA. 1983;80: 7367-7371. (Pubitemid 14208859)
20. Lakatta EG. Functional implications of spontaneous sarcoplasmic reticulum Ca2+release in the heart. Cardiovasc Res. 1992;26:193-214.
21. Diaz ME, Trafford AW, O'Neill SC, Eisner DA. Measurement of sarcoplasmic reticulum Ca2+content and sarcolemmal Ca2+fluxes in isolated rat ventricular myocytes during spontaneous Ca2+release. J Physiol. 1997;501(Pt 1):3-16. (Pubitemid 27230397)
22. Jiang D, Xiao B, Yang D, Wang R, Choi P, Zhang L, Cheng H, Chen SR. RyR2 mutations linked to ventricular tachycardia and sudden death reduce the threshold for store-overload-induced Ca2+release (SOICR). Proc Natl Acad Sci USA. 2004;101:13062-13067. (Pubitemid 39167583)
23. Jiang D, Wang R, Xiao B, Kong H, Hunt DJ, Choi P, Zhang L, Chen SR. Enhanced store overload-induced Ca2+release and channel sensitivity to luminal Ca2+activation are common defects of RyR2 mutations linked to ventricular tachycardia and sudden death. Circ Res. 2005;97: 1173-1181.
24. Shannon TR, Guo T, Bers DM. Ca2+scraps: Local depletions of free [Ca2+] in cardiac sarcoplasmic reticulum during contractions leave substantial Ca2+reserve. Circ Res. 2003;93:40-45. (Pubitemid 36859039)
25. Brochet DX, Yang D, Di Maio A, Lederer WJ, Franzini-Armstrong C, Cheng H. Ca2+blinks: Rapid nanoscopic store calcium signaling. Proc Natl Acad Sci USA. 2005;102:3099-3104. (Pubitemid 40299922)
26. Zima AV, Picht E, Bers DM, Blatter LA. Termination of cardiac Ca2+sparks role of intra-SR [Ca2+], release flux, and intra-SR Ca2+diffusion. Circ Res. 2008;103:e105-e110.
27. Stern MD, Cheng H. Putting out the fire: What terminates calciuminduced calcium release in cardiac muscle? Cell Calcium. 2004;35: 591-601. (Pubitemid 38618571)
28. Domeier TL, Blatter LA, Zima AV. Alteration of sarcoplasmic reticulum Ca2+release termination by ryanodine receptor sensitization and in heart failure. J Physiol. 2009;587:5197-5209.
29. Gyorke S, Terentyev D. Modulation of ryanodine receptor by luminal calcium and accessory proteins in health and cardiac disease. Cardiovasc Res. 2008;77:245-255. (Pubitemid 351197640)
30. Sobie EA, Lederer WJ. Dynamic local changes in sarcoplasmic reticulum calcium: Physiological and pathophysiological roles. J Mol Cell Cardiol. 2012;52:304-311.
31. Wilkins BJ, Molkentin JD. Calcineurin and cardiac hypertrophy: Where have we been? Where are we going? J Physiol. 2002;541:1-8. (Pubitemid 35203232)
32. Houser SR, Molkentin JD. Does contractile Ca2+control calcineurin-NFAT signaling and pathological hypertrophy in cardiac myocytes? Sci Signal. 2008;1:pe31.
33. Fatkin D, McConnell BK, Mudd JO, Semsarian C, Moskowitz IG, Schoen FJ, Giewat M, Seidman CE, Seidman JG. An abnormal Ca(2+) response in mutant sarcomere protein-mediated familial hypertrophic cardiomyopathy. J Clin Invest. 2000;106:1351-1359.
34. Haghighi K, Gregory KN, Kranias EG. Sarcoplasmic reticulum Ca-ATPase-phospholamban interactions and dilated cardiomyopathy. Biochem Biophys Res Commun. 2004;322:1214-1222. (Pubitemid 39164651)
35. Robinson P, Griffiths PJ, Watkins H, Redwood CS. Dilated and hypertrophic cardiomyopathy mutations in troponin and alpha-tropomyosin have opposing effects on the calcium affinity of cardiac thin filaments. Circ Res. 2007;101:1266-1273. (Pubitemid 350294643)
36. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 1989;77:51-59. (Pubitemid 19125653)
37. Palmer AE, Jin C, Reed JC, Tsien RY. Bcl-2-mediated alterations in endoplasmic reticulum Ca2+analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci USA. 2004;101: 17404-17409. (Pubitemid 39657417)
38. Jones PP, Jiang D, Bolstad J, Hunt DJ, Zhang L, Demaurex N, Chen SR. 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. Biochem J. 2008;412:171-178. (Pubitemid 351678347)
39. Poburko D, Liao CH, van Breemen C, Demaurex N. Mitochondrial regulation of sarcoplasmic reticulum Ca2+content in vascular smooth muscle cells. Circ Res. 2009;104:104-112.
40. Jiang D, Jones PP, Davis DR, Gow R, Green MS, Birnie DH, Chen SR, Gollob MH. Characterization of a novel mutation in the cardiac ryanodine receptor that results in catecholaminergic polymorphic ventricular tachycardia. Channels (Austin). 2010;4:302-310.
41. Priori SG, Napolitano C, Tiso N, Memmi M, Vignati G, Bloise R, Sorrentino V, Danieli GA. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation. 2001;103:196-200. (Pubitemid 32095402)
42. Kannankeril PJ, Mitchell BM, Goonasekera SA, et al. Mice with the R176Q cardiac ryanodine receptor mutation exhibit catecholamineinduced ventricular tachycardia and cardiomyopathy. Proc Natl Acad Sci USA. 2006;103:12179-12184. (Pubitemid 44215831)
43. Fernandez-Velasco M, Rueda A, Rizzi N, Benitah JP, Colombi B, Napolitano C, Priori SG, Richard S, Gomez AM. Increased Ca2+sensitivity of the ryanodine receptor mutant RyR2R4496C underlies catecholaminergic polymorphic ventricular tachycardia. Circ Res. 2009;104: 201-209.
44. Sedej S, Heinzel FR, Walther S, Dybkova N, Wakula P, Groborz J, Gronau P, Maier LS, Vos MA, Anthony Lai F, Napolitano C, Priori SG, Kockskamper J, Pieske B. Na+-dependent SR Ca2+overload induces arrhythmogenic events in mouse cardiomyocytes with a human CPVT mutation. Cardiovasc Res. 2010;87:50-59.
45. Uchinoumi H, Yano M, Suetomi T, Ono M, Xu X, Tateishi H, Oda T, Okuda S, Doi M, Kobayashi S, Yamamoto T, Ikeda Y, Ohkusa T, Ikemoto N, Matsuzaki M. Catecholaminergic polymorphic ventricular tachycardia is caused by mutation-linked defective conformational regulation of the ryanodine receptor. Circ Res. 2010;106:1413-1424.
46. Sham JS, Song LS, Chen Y, Deng LH, Stern MD, Lakatta EG, Cheng H. Termination of Ca2+release by a local inactivation of ryanodine receptors in cardiac myocytes. Proc Natl Acad Sci USA. 1998;95: 15096-15101. (Pubitemid 29003762)
47. Terentyev D, Viatchenko-Karpinski S, Valdivia HH, Escobar AL, Gyorke S. Luminal Ca2+controls termination and refractory behavior of Ca2+-induced Ca2+release in cardiac myocytes. Circ Res. 2002;91:414-420. (Pubitemid 35034209)
48. Baudenbacher F, Schober T, Pinto JR, Sidorov VY, Hilliard F, Solaro RJ, Potter JD, Knollmann BC. Myofilament Ca2+sensitization causes susceptibility to cardiac arrhythmia in mice. J Clin Invest. 2008;118: 3893-3903.
49. Huke S, Knollmann BC. Increased myofilament Ca2+-sensitivity and arrhythmia susceptibility. J Mol Cell Cardiol. 2010;48:824-833.
50. Toko H, Takahashi H, Kayama Y, et al. Ca2 +calmodulin-dependent kinase IIdelta causes heart failure by accumulation of p53 in dilated cardiomyopathy. Circulation. 2010;122:891-899.
51. Schlotthauer K, Bers DM. Sarcoplasmic reticulum Ca(2+) release causes myocyte depolarization. underlying mechanism and threshold for triggered action potentials. Circ Res. 2000;87:774-780.
52. Amador FJ, Liu S, Ishiyama N, Plevin MJ, Wilson A, MacLennan DH, Ikura M. Crystal structure of type I ryanodine receptor amino-terminal beta-trefoil domain reveals a disease-associated mutation "hot spot" loop. Proc Natl Acad Sci USA. 2009;106:11040-11044.
53. Lobo PA, Van Petegem F. Crystal structures of the N-terminal domains of cardiac and skeletal muscle ryanodine receptors: Insights into disease mutations. Structure. 2009;17:1505-1514.
54. Tung CC, Lobo PA, Kimlicka L, Van Petegem F. The amino-terminal disease hotspot of ryanodine receptors forms a cytoplasmic vestibule. Nature. 2010;468:585-588.
55. Lobo PA, Kimlicka L, Tung CC, Van Petegem F. The deletion of exon 3 in the cardiac ryanodine receptor is rescued by beta strand switching. Structure. 2011;19:790-798.
56. Samso M, Feng W, Pessah IN, Allen PD. Coordinated movement of cytoplasmic and transmembrane domains of RyR1 upon gating. PLoS Biol. 2009;7:e85.
57. Kubalova Z, Terentyev D, Viatchenko-Karpinski S, Nishijima Y, Gyorke I, Terentyeva R, da Cunha DN, Sridhar A, Feldman DS, Hamlin RL, Carnes CA, Gyorke S. Abnormal intrastore calcium signaling in chronic heart failure. Proc Natl Acad Sci USA. 2005;102:14104-14109. (Pubitemid 41377710)