The arrhythmogenic human HRC point mutation S96A leads to spontaneous Ca2+ release due to an impaired ability to buffer store Ca2+

Journal of Molecular and Cellular Cardiology

Volumn 74, Issue , 2014, Pages 22-31

  Zhang, Joe Z ^a   McLay, Janet C ^a   Jones, Peter P ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Arrhythmia; Cardiac ryanodine receptor (RyR2); Histidine rich calcium binding protein (HRC); Sarcoplasmic reticulum (SR); SERCA; Store overload induced calcium release (SOICR)

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM ION; HISTIDINE RICH CALCIUM BINDING PROTEIN; RYANODINE RECEPTOR; UNCLASSIFIED DRUG; CALCIUM; HRC PROTEIN, HUMAN;

ANIMAL CELL; ARRHYTHMOGENESIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM METABOLISM; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOSOL; EXPERIMENTAL MODEL; HEART ARRHYTHMIA; HEK293 CELL LINE; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; WILD TYPE; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART MUSCLE CELL; HEART VENTRICLE; ION TRANSPORT; METABOLISM; PRIMARY CELL CULTURE; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; TRANSGENE;

ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; GENE EXPRESSION REGULATION; HEART VENTRICLES; HEK293 CELLS; HUMANS; ION TRANSPORT; MICE; MYOCYTES, CARDIAC; POINT MUTATION; PRIMARY CELL CULTURE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; TRANSGENES;

EID: 84904764767     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.04.019     Document Type: Article

References (46)

1. Arvanitis D.A., Sanoudou D., Kolokathis F., Vafiadaki E., Papalouka V., Kontrogianni-Konstantopoulos A. The Ser96Ala variant in histidine-rich calcium-binding protein is associated with life-threatening ventricular arrhythmias in idiopathic dilated cardiomyopathy. Eur Heart J 2008, 29:2514-2525.
2. Han P., Cai W., Wang Y., Lam C.K., Arvanitis D.A., Singh V.P., et al. Catecholaminergic-induced arrhythmias in failing cardiomyocytes associated with human HRCS96A variant overexpression. Am J Physiol Heart Circ Physiol 2011, 301:H1588-H1595.
3. Fabiato A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol Cell Physiol 1983, 245:C1-C14.
4. 2+ release. J Physiol (Lond) 1997, 501:3-16.
5. 2+ release from the cardiac sarcoplasmic reticulum: regulation versus autoregulation. Cardiovasc Res 1998, 38:589-604.
6. 2+ release (SOICR). Proc Natl Acad Sci U S A 2004, 101:13062-13070.
7. Kass R.S., Tsien R.W. Fluctuations in membrane current driven by intracellular calcium in cardiac Purkinje fibers. Biophys J 1982, 38:259-269.
8. Wier W.G., Kort A.A., Stern M.D., Lakatta E.G., Marban E. Cellular calcium fluctuations in mammalian heart: direct evidence from noise analysis of aequorin signals in Purkinje fibers. Proc Natl Acad Sci U S A 1983, 80:7367-7371.
9. 2+ activation are common defects of RyR2 mutations linked to ventricular tachycardia and sudden death. Circ Res 2005, 97:1173-1181.
10. 2+ release. Biochem J 2008, 412:171-178.
11. 2+ activation of the ryanodine receptor. Biochem J 2008, 414:441.
12. 2+ waves. Circ Res 2010, 107:1483-1489.
13. Song D.W., Lee J.G., Youn H.S., Eom S.H., Kim D.H. Ryanodine receptor assembly: a novel systems biology approach to 3D mapping. Prog Biophys Mol Biol 2011, 105:145-161.
14. Faggioni M., Knollmann B.C. Calsequestrin 2 and arrhythmias. Am J Physiol Heart Circ Physiol 2012, 302:H1250-H1260.
15. Arvanitis D.A., Vafiadaki E., Sanoudou D., Kranias E.G. Histidine-rich calcium binding protein: the new regulator of sarcoplasmic reticulum calcium cycling. J Mol Cell Cardiol 2011, 50:43-49.
16. 2+ binding protein). Biochem Biophys Res Commun 2003, 300:192-196.
17. Fan G.C., Gregory K.N., Zhao W., Park W.J., Kranias E.G. Regulation of myocardial function by histidine-rich, calcium-binding protein. Am J Physiol Heart Circ Physiol 2004, 287:H1705-H1711.
18. Shoshan-Barmatz V., Orr I., Weil S., Meyer H., Varsanyi M., Heilmeyer L.M.G. The identification of the phosphorylated 150/160-kDa proteins of sarcoplasmic reticulum, their kinase and their association with the ryanodine receptor. Biochim Biophys Acta Biomembr 1996, 1283:89-100.
19. 2+-binding protein at the triadic junction in skeletal muscle fibers. J Muscle Res Cell Motil 1999, 20:403-415.
20. 2+-binding protein) and triadin in the lumen of sarcoplasmic reticulum. J Biol Chem 2001, 276:39533.
21. 2+-binding protein carboxyl-terminal region. Biochem Biophys Res Commun 2001, 289:1125-1134.
22. 2+ binding protein: a regulator of sarcoplasmic reticulum calcium sequestration and cardiac function. J Mol Cell Cardiol 2006, 40:653-665.
23. Jaehnig E.J., Heidt A.B., Greene S.B., Cornelissen I., Black B.L. Increased susceptibility to isoproterenol-induced cardiac hypertrophy and impaired weight gain in mice lacking the histidine-rich calcium-binding protein. Mol Cell Biol 2006, 26:9315-9326.
24. Park C.S., Cha H., Kwon E.J., Jeong D., Hajjar R.J., Kranias E.G., et al. AAV-mediated knock-down of HRC exacerbates transverse aorta constriction-induced heart failure. PLoS One 2012, 7:e43282.
25. 2+-cycling and severe pathology under pressure-overload stress. Basic Res Cardiol 2013, 108:1-18.
26. Zhou X., Fan G.C., Ren X., Waggoner J.R., Gregory K.N., Chen G., et al. Overexpression of histidine-rich Ca-binding protein protects against ischemia/reperfusion-induced cardiac injury. Cardiovasc Res 2007, 75:487-497.
27. 2+ release. Nat Med 2011, 17:1003-1009.
28. 2+ release is a common defect of RyR2 mutations associated with cardiomyopathies novelty and significance. Circ Res 2012, 110:968-977.
29. 2+ triggered arrhythmias. Nat Med 2014, 20:184-192.
30. 2+ diffusion. Circ Res 2008, 103:e105.
31. 2+ blinks: rapid nanoscopic store calcium signaling. Proc Natl Acad Sci U S A 2005, 102:3099-3104.
32. 2+ sparks in rat ventricular myocytes. J Physiol 1998, 507:667-677.
33. 2+-binding protein of skeletal muscle sarcoplasmic reticulum. Biochem Biophys Res Commun 1992, 186:659-667.
34. Arvanitis D.A., Vafiadaki E., Fan G.C., Mitton B.A., Gregory K.N., Del Monte F., et al. Histidine-rich Ca-binding protein interacts with sarcoplasmic reticulum Ca-ATPase. Am J Physiol Heart Circ Physiol 2007, 293:H1581-H1590.
35. Gullberg M., Andersson A.-C. Visualization and quantification of protein-protein interactions in cells and tissues. Nat Methods 2010, 7.
36. 2+ release and [3H]ryanodine binding to RyR2 irrespective of FKBP12.6 association. Biochem J 2007, 404:431-438.
37. 2+ release in cardiac myocytes. Circ Res 2002, 91:414.
38. Terentyev D., Viatchenko-Karpinski S., Györke I., Volpe P., Williams S.C., Györke S. Calsequestrin determines the functional size and stability of cardiac intracellular calcium stores: mechanism for hereditary arrhythmia. Proc Natl Acad Sci U S A 2003, 100:11759-11764.
39. Viatchenko-Karpinski S., Terentyev D., Györke I., Terentyeva R., Volpe P., Priori S.G., et al. Abnormal calcium signaling and sudden cardiac death associated with mutation of calsequestrin. Circ Res 2004, 94:471-477.
40. 2+ binding protein) resides in the lumen of sarcoplasmic reticulum as a multimer. Biochem Biophys Res Commun 1999, 263:667-671.
41. Marks A., Priori S., Memmi M., Kontula K., Laitinen P. Involvement of the cardiac ryanodine receptor/calcium release channel in catecholaminergic polymorphic ventricular tachycardia. J Cell Physiol 2002, 190:1-6.
42. Singh V.P., Rubinstein J., Arvanitis D.A., Ren X., Gao X., Haghighi K., et al. Abnormal calcium cycling and cardiac arrhythmias associated with the human Ser96Ala genetic variant of histidine-rich calcium-binding protein. J Am Heart Assoc 2013, 2:e000460.
43. Ramay H.R., Liu O.Z., Sobie E.A. Recovery of cardiac calcium release is controlled by sarcoplasmic reticulum refilling and ryanodine receptor sensitivity. Cardiovasc Res 2011, 91:598-605.
44. Stern M. Buffering of calcium in the vicinity of a channel pore. Cell Calcium 1992, 13:183-192.
45. 2+ release channels and their regulation by endogenous effectors. Annu Rev Physiol 1994, 56:485-508.
46. Fill M., Copello J.A. Ryanodine receptor calcium release channels. Physiol Rev 2002, 82:893-922.