Calsequestrin 2 (CASQ2) mutations increase expression of calreticulin and ryanodine receptors, causing catecholaminergic polymorphic ventricular tachycardia

Journal of Clinical Investigation

Volumn 117, Issue 7, 2007, Pages 1814-1823

  Song, Lei ^a   Alcalai, Ronny ^b   Arad, Michael ^c   Wolf, Cordula M ^d   Toka, Okan ^b   Conner, David A ^b   Berul, Charles I ^b,d   Eldar, Michael ^c   Seidman, Christine E ^a   Seidman, J G ^b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALRETICULIN; CALSEQUESTRIN; CALSEQUESTRIN 2; RNA; RYANODINE RECEPTOR 2; UNCLASSIFIED DRUG;

ALLELE; ANIMAL MODEL; ARTICLE; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; CONTROLLED STUDY; FAMILIAL DISEASE; GENE MUTATION; HEART CONTRACTION; HEART VENTRICLE ARRHYTHMIA; HEART VENTRICLE HYPERTROPHY; MOUSE; MUSCLE CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOPLASMIC RETICULUM; STRESS; WESTERN BLOTTING;

ANIMALS; CALCIUM; CALRETICULIN; CALSEQUESTRIN; CATECHOLAMINES; ELECTROPHYSIOLOGY; EXONS; GENE DELETION; GENE EXPRESSION REGULATION; MAGNESIUM; MICE; MICE, KNOCKOUT; MUTATION; RNA; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; TACHYCARDIA, VENTRICULAR;

EID: 34447133403     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI31080     Document Type: Article

References (56)

1. Leenhardt, A., et al. 1995. Catecholaminergic polymorphic ventricular tachycardia in children. A 7-year follow-up of 21 patients. Circulation. 91:1512-1519.
2. Priori, S.G., et al. 2002. Clinical and molecular characterization of patients with catecholaminergic polymorphic ventricular tachycardia. Circulation. 106:69-74.
3. Lahat, H., et al. 2001. Autosomal recessive catecholamine-or exercise-induced polymorphic ventricular tachycardia: clinical features and assignment of the disease gene to chromosome 1p13-21. Circulation. 103:2822-2827.
4. Postma, A.V., et al. 2002. Absence of calsequestrin 2 causes severe forms of catecholaminergic polymorphic ventricular tachycardia. Circ. Res. 91:e21-e26.
5. 2+ in the heart: contraction versus intracellular signaling. J. Clin. Invest. 116:623-626. doi:10.1172/JCI27824.
6. Saks, V., et al. 2006. Cardiac system bioenergetics: metabolic basis of the Frank-Starling law. J. Physiol. 571:253-273.
7. Beard, N.A., Laver, D.R., and Dulhunty, A.F. 2004. Calsequestrin and the calcium release channel of skeletal and cardiac muscle. Prog. Biophys. Mol. Biol. 85:33-69.
8. Yano, K., and Zarain-Herzberg, A. 1994. Sarcoplasmic reticulum calsequestrins: structural and functional properties. Mol. Cell. Biochem. 135:61-70.
9. Treves, S., Vilsen, B., Chiozzi, P., Andersen, J.P., and Zorzato, F. 1992. Molecular cloning, functional expression and tissue distribution of the cDNA encoding frog skeletal muscle calsequestrin. Biochem. J. 283:767-772.
10. Slupsky, J.R., Ohnishi, M., Carpenter, M.R., and Reithmeier, R.A. 1987. Characterization of cardiac calsequestrin. Biochemistry. 26:6539-6544.
11. Cozens, B., and Reithmeier, R.A. 1984. Size and shape of rabbit skeletal muscle calsequestrin. J. Biol. Chem. 259:6248-6252.
12. Scott, B.T., Simmerman, H.K., Collins, J.H., Nadal-Ginard, B., and Jones, L.R. 1988. Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J. Biol. Chem. 263:8958-8964.
13. Campbell, K.P., MacLennan, D.H., Jorgensen, A.O., and Mintzer, M.C. 1983. Purification and characterization of calsequestrin from canine cardiac sarcoplasmic reticulum and identification of the 53,000 dalton glycoprotein. J. Biol. Chem. 258:1197-1204.
14. Szegedi, C., Sarkozi, S., Herzog, A., Jona, I., and Varsanyi, M. 1999. Calsequestrin: more than 'only' a luminal Ca2+ buffer inside the sarcoplasmic reticulum. Biochem. J. 337:19-22.
15. Gyorke, I., Hester, N., Jones, L.R., and Gyorke, S. 2004. The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys. J. 86:2121-2128.
16. Zhang, L., Kelley, J., Schmeisser, G., Kobayashi, Y.M., and Jones, L.R. 1997. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J. Biol. Chem. 272:23389-23397.
17. Lahat, H., et al. 2001. A missense mutation in a highly conserved region of CASQ2 is associated with autosomal recessive catecholamine-induced polymorphic ventricular tachycardia in Bedouin families from Israel. Am. J. Hum. Genet. 69:1378-1384.
18. di Barletta, M.R., et al. 2006. Clinical phenotype and functional characterization of CASQ2 mutations associated with catecholaminergic polymorphic ventricular tachycardia. Circulation. 114:1012-1019.
19. Terentyev, D., et al. 2006. Abnormal interactions of calsequestrin with the ryanodine receptor calcium release channel complex linked to exercise-induced sudden cardiac death. Circ. Res. 98:1151-1158.
20. Knollmann, B.C., et al. 2006. Casq2 deletion causes sarcoplasmic reticulum volume increase, premature Ca2+ release, and catecholaminergic polymorphic ventricular tachycardia. J. Clin. Invest. 116:2510-2520. doi:10.1172/JCI29128.
21. Viatchenko-Karpinski, S., et al. 2004. Abnormal calcium signaling and sudden cardiac death associated with mutation of calsequestrin. Circ. Res. 94:471-477.
22. Houle, T.D., Ram, M.L., and Cala, S.E. 2004. Calsequestrin mutant D307h exhibits depressed binding to its protein targets and a depressed response to calcium. Cardiovasc. Res. 64:227-233.
23. Cerrone, M., et al. 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.
24. Laver, D.R., Baynes, T.M., and Dulhunty, A.F. 1997. Magnesium inhibition of ryanodine-receptor calcium channels: evidence for two independent mechanisms. J. Membr. Biol. 156:213-229.
25. Tzivoni, D., et al. 1988. Treatment of torsade de pointes with magnesium sulfate. Circulation. 77:392-397.
26. Michalak, M., Guo, L., Robertson, M., Lozak, M., and Opas, M. 2004. Calreticulin in the heart. Mol. Cell. Biochem. 263:137-142.
27. Michalak, M., Corbett, E.F., Mesaeli, N., Nakamura, K., and Opas, M. 1999. Calreticulin: one protein, one gene, many functions. Biochem. J. 344:281-292.
28. Mesaeli, N., et al. 1999. Calreticulin is essential for cardiac development. J. Cell Biol. 144:857-868.
29. Lynch, J.M., Chilibeck, K., Qui, Y., and Michalak, M. 2006. Assembling pieces of the cardiac puzzle; calreticulin and calcium-dependent pathways in cardiac development, health, and disease. Trends Cardiovasc. Med. 16:65-69.
30. Meldolesi, J., and Pozzan, T. 1998. The endoplasmic reticulum Ca2+ store: a view from the lumen. Trends Biochem. Sci. 23:10-14.
31. Krause, K.H., and Michalak, M. 1997. Calreticulin. Cell. 88:439-443.
32. Nakamura, K., et al. 2001. Complete heart block and sudden death in mice overexpressing calreticulin. J. Clin. Invest. 107:1245-1253.
33. Beard, N.A., et al. 2005. Regulation of ryanodine receptors by calsequestrin: effect of high luminal Ca2+ and phosphorylation. Biophys. J. 88:3444-3454.
34. Lehnart, S.E., et al. 2006. Stabilization of cardiac ryanodine receptor prevents intracellular calcium leak and arrhythmias. Proc. Natl. Acad. Sci. U. S. A. 103:7906-7910.
35. Lamb, G.D., and Stephenson, D.G. 1991. Effect of Mg2+ on the control of Ca2+ release in skeletal muscle fibres of the toad. J. Physiol. 434:507-528.
36. Meissner, G. 1994. Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol. 56:485-508.
37. Laver, D.R. 2005. Coupled calcium release channels and their regulation by luminal and cytosolic ions. Eur. Biophys. J. 34:359-368.
38. Iyer, V., Hajjar, R.J., and Armoundas, A.A. 2007. Mechanisms of abnormal calcium homeostasis in mutations responsible for catecholaminergic polymorphic ventricular tachycardia. Circ. Res. 100:e22-e31.
39. Shinbane, J.S., et al. 1997. Tachycardia-induced cardiomyopathy: a review of animal models and clinical studies. J. Am. Coll. Cardiol. 29:709-715.
40. Wilkins, B.J., and Molkentin, J.D. 2004. Calcium-calcineurin signaling in the regulation of cardiac hypertrophy. Biochem. Biophys. Res. Commun. 322:1178-1191.
41. Liu, P., Jenkins, N.A., and Copeland, N.G. 2003. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 13:476-484.
42. Bruneau, B.G., et al. 2001. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell. 106:709-721.
43. Truett, G.E., et al. 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and Tris (HotSHOT). Biotechniques. 29:52, 54.
44. Ausubel, F., et al. 2006. Current protocols in molecular biology. John Wiley and Sons, Inc. New York, New York, USA. 4900 pp.
45. Semsarian, C., et al. 2002. The L-type calcium channel inhibitor diltiazem prevents cardiomyopathy in a mouse model. J. Clin. Invest. 109:1013-1020. doi:10.1172/JCI200214677.
46. Eletr, S., and Inesi, G. 1972. Phospholipid orientation in sarcoplasmic membranes: spin-label ESR and proton MNR studies. Biochim. Biophys. Acta. 282:174-179.
47. Heilmann, C., Brdiczka, D., Nickel, E., and Pette, D. 1977. ATPase activities, Ca2+ transport and phosphoprotein formation in sarcoplasmic reticulum subfractions of fast and slow rabbit muscles. Eur. J. Biochem. 81:211-222.
48. McConnell, B.K., et al. 2001. Comparison of two murine models of familial hypertrophic cardiomyopathy. Circ. Res. 88:383-389.
49. 2+ response in mutant sarcomere protein-mediated familial hypertrophic cardiomyopathy. J. Clin. Invest. 106:1351-1359.
50. Arad, M., et al. 2003. Transgenic mice overexpressing mutant PRKAG2 define the cause of Wolff-Parkinson-White syndrome in glycogen storage cardiomyopathy. Circulation. 107:2850-2856.
51. Berul, C.I., Aronovitz, M.J., Wang, P.J., and Mendelsohn, M.E. 1996. In vivo cardiac electrophysiology studies in the mouse. Circulation. 94:2641-2648.
52. Gehrmann, J., and Berul, C.I. 2000. Cardiac electrophysiology in genetically engineered mice. J. Cardiovasc. Electrophysiol. 11:354-368.
53. Mitchell, G.F., Jeron, A., and Koren, G. 1998. Measurement of heart rate and Q-T interval in the conscious mouse. Am. J. Physiol. 274:H747-H751.
54. Maguire, C.T., et al. 2003. Implications of ventricular arrhythmia vulnerability during murine electrophysiology studies. Physiol. Genomics. 15:84-91.
55. Lim, C.C., Apstein, C.S., Colucci, W.S., and Liao, R. 2000. Impaired cell shortening and relengthening with increased pacing frequency are intrinsic to the senescent mouse cardiomyocyte. J. Mol. Cell. Cardiol. 32:2075-2082.
56. Nagata, K., et al. 1998. Early changes in excitation-contraction coupling: transition from compensated hypertrophy to failure in Dahl salt-sensitive rat myocytes. Cardiovasc. Res. 37:467-477.