Proteins within the intracellular calcium store determine cardiac RyR channel activity and cardiac output

Clinical and Experimental Pharmacology and Physiology

Volumn 39, Issue 5, 2012, Pages 477-484

  Dulhunty, Angela F ^a   Wium, Elize ^a   Li, Linwei ^a   Hanna, Amy D ^a   Mirza, Shamaruh ^a   Talukder, Sadik ^a   Ghazali, Nuur A A ^a   Beard, Nicole A ^a  

^a Biology and Environment   (Australia)

Author keywords

Calcium signalling; Calsequestrin; Cardiac muscle; Junctin; Luminal calcium dependence of calcium release; Protein protein interactions; Ryanodine receptor calcium release channel; Sarcoplasmic reticulum; Triadin

Indexed keywords

CALCIUM ION; CALSEQUESTRIN; JUNCTIN; PROTEIN; RYANODINE RECEPTOR 2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; TRIADIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; HEART CONTRACTION; HEART MUSCLE CELL; HEART OUTPUT; HUMAN; LONGEVITY; MUSCLE STRESS; PHOTOTRANSDUCTION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SARCOPLASMIC RETICULUM; SUDDEN DEATH;

ANIMALS; CALCIUM CHANNELS; CALCIUM SIGNALING; CARDIAC OUTPUT; HUMANS; INTRACELLULAR FLUID; MUTATION; MYOCARDIUM; RABBITS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM;

EID: 84860261837     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2012.05704.x     Document Type: Article

References (59)

1. 2+ sensing sites. Biophys. J. 1998; 75: 2801-10.
2. 2+ sites. Biophys. J. 2007; 92: 3541-55.
3. Wei L, Hanna AD, Beard NA, Dulhunty AF. Unique isoform-specific properties of calsequestrin in the heart and skeletal muscle. Cell Calcium 2009; 45: 474-84.
4. 2+ activation in the cardiac ryanodine receptor is associated with ventricular fibrillation and sudden death. Proc. Natl Acad. Sci. USA 2007; 104: 18.
5. 2+ activation of RyR1 underlies a causal mechanism of porcine malignant hyperthermia. J. Biol. Chem. 2008; 283: 20.
6. Terentyev D, Nori A, Santoro M et al. Abnormal interactions of calsequestrin with the ryanodine receptor calcium release channel complex linked to exercise-induced sudden cardiac death. Circ. Res. 2006; 98: 1151-8.
7. Viatchenko-Karpinski S, Terentyev D, Gyorke I et al. Abnormal calcium signaling and sudden cardiac death associated with mutation of calsequestrin. Circ. Res. 2004; 94: 471-7.
8. Liu N, Colombi B, Memmi M et al. Arrhythmogenesis in catecholaminergic polymorphic ventricular tachycardia: Insights from a RyR2 R4496C knock-in mouse model. Circ. Res. 2006; 99: 292-8.
9. Rizzi N, Liu N, Napolitano C et al. Unexpected structural and functional consequences of the R33Q homozygous mutation in cardiac calsequestrin: A complex arrhythmogenic cascade in a knock in mouse model. Circ. Res. 2008; 103: 298-306.
10. Liu N, Rizzi N, Boveri L, Priori SG. Ryanodine receptor and calsequestrin in arrhythmogenesis: what we have learnt from genetic diseases and transgenic mice. J. Mol. Cell. Cardiol. 2009; 46: 149-59.
11. 2+ handling and arrhythmogenesis. Circ. Res. 2011; 108: 871-83.
12. Gyorke S. Molecular basis of catecholaminergic polymorphic ventricular tachycardia. Heart Rhythm 2009; 6: 123-9.
13. 2+ signaling in striated muscle. The elusive roles of triadin, junctin, and calsequestrin. Eur. Biophys. J. 2009; 39: 27-36.
14. Dulhunty A, Wei L, Beard N. Junctin: the quiet achiever. J. Physiol. 2009; 587: 3135-7.
15. Bers DM (ed). Excitation-Contraction Coupling and Cardiac Contractile Force, 2nd edn. Kluwer Academic Publishers, 2002.
16. Stern MD, Cheng H. Putting out the fire: what terminates calcium-induced calcium release in cardiac muscle? Cell Calcium 2004; 35: 591-601.
17. Treves S, Vukcevic M, Maj M, Thurnheer R, Mosca B, Zorzato F. Minor sarcoplasmic reticulum membrane components that modulate excitation-contraction coupling in striated muscles. J. Physiol. 2009; 587: 3071-9.
18. Arvanitis DA, Vafiadaki E, Fan GC et al. Histidine-rich Ca-binding protein interacts with sarcoplasmic reticulum Ca-ATPase. Am. J. Physiol. Heart Circ. Physiol. 2007; 293: H1581-9.
19. Arvanitis DA, Vafiadaki E, Sanoudou D, Kranias EG. Histidine-rich calcium binding protein: the new regulator of sarcoplasmic reticulum calcium cycling. J. Mol. Cell. Cardiol. 2011; 50: 43-9.
20. 2+ binding protein: potential roles in heart failure and arrhythmogenesis. J. Physiol. 2009; 587: 3125-33.
21. Marty I, Faure J, Fourest-Lieuvin A, Vassilopoulos S, Oddoux S, Brocard J. Triadin: what possible function 20 years later? J. Physiol. 2009; 587: 3117-21.
22. Guo W, Jorgensen AO, Jones LR, Campbell KP. Biochemical characterization and molecular cloning of cardiac triadin. J. Biol. Chem. 1996; 271: 458-65.
23. Vassilopoulos S, Thevenon D, Rezgui SS et al. Triadins are not triad-specific proteins: two new skeletal muscle triadins possibly involved in the architecture of sarcoplasmic reticulum. J. Biol. Chem. 2005; 280: 28.
24. Kobayashi YM, Alseikhan BA, Jones LR. Localization and characterization of the calsequestrin-binding domain of triadin 1. Evidence for a charged beta-strand in mediating the protein-protein interaction. J. Biol. Chem. 2000; 275: 17.
25. 2+-binding protein) and triadin in the lumen of sarcoplasmic reticulum. J. Biol. Chem. 2001; 276: 39.
26. Lee JM, Rho SH, Shin DW et al. Negatively charged amino acids within the intraluminal loop of ryanodine receptor are involved in the interaction with triadin. J. Biol. Chem. 2004; 279: 6994-7000.
27. Wei L, Gallant EM, Dulhunty AF, Beard NA. Junctin and triadin activate skeletal ryanodine receptors; junctin alone mediates functional interactions with calsequestrin. Int. J. Biochem. Cell Biol. 2009; 41: 2214-24.
28. Fan GC, Yuan Q, Kranias EG. Regulatory roles of junctin in sarcoplasmic reticulum calcium cycling and myocardial function. Trends Cardiovasc. Med. 2008; 18: 1-5.
29. Terentyev D, Cala SE, Houle TD et al. Triadin overexpression stimulates excitation-contraction coupling and increases predisposition to cellular arrhythmia in cardiac myocytes. Circ. Res. 2005; 96: 651-8.
30. Wang Y, Li X, Duan H, Fulton TR, Eu JP, Meissner G. Altered stored calcium release in skeletal myotubes deficient of triadin and junctin. Cell Calcium 2009; 45: 29-37.
31. Goonasekera SA, Beard NA, Groom L et al. Triadin binding to the C-terminal luminal loop of the ryanodine receptor is important for skeletal muscle excitation contraction coupling. J. Gen. Physiol. 2007; 130: 365-78.
32. Gyorke I, Hester N, Jones LR, Gyorke S. The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys. J. 2004; 86: 2121-8.
33. 2+. J. Biol. Chem. 2011; 285: 38.
34. Dulhunty AF, Beard NA, Pouliquin P, Casarotto MG. Agonists and antagonists of the cardiac ryanodine receptor: potential therapeutic agents? Pharmacol. Ther. 2007; 113: 247-63.
35. Groh S, Marty I, Ottolia M et al. Functional interaction of the cytoplasmic domain of triadin with the skeletal ryanodine receptor. J. Biol. Chem. 1999; 274: 12.
36. 2+ release from sarcoplasmic reticulum. FEBS Lett. 1992; 299: 57-9.
37. Caswell AH, Brandt NR. Membrane topography of cardiac triadin. Arch. Biochem. Biophys. 2002; 398: 61-72.
38. Marty I, Robert M, Ronjat M, Bally I, Arlaud G, Villaz M. Localization of the N-terminal and C-terminal ends of triadin with respect to the sarcoplasmic reticulum membrane of rabbit skeletal muscle. Biochem. J. 1995; 307: 769-74.
39. Altschafl BA, Arvanitis DA, Fuentes O, Yuan Q, Kranias EG, Valdivia HH. Dual role of junctin in the regulation of ryanodine receptors and calcium release in cardiac ventricular myocytes. J. Physiol. 2011; 589: 6063-80.
40. Zhang L, Kelley J, Schmeisser G, Kobayashi YM, Jones LR. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J. Biol. Chem. 1997; 272: 23.
41. Protasi F, Paolini C, Dainese M. Calsequestrin-1: a new candidate gene for malignant hyperthermia and exertional/environmental heat stroke. J. Physiol. 2009; 587: 3095-100.
42. Wei L, Varsanyi M, Dulhunty AF, Beard NA. The conformation of calsequestrin determines its ability to regulate skeletal ryanodine receptors. Biophys. J. 2006; 91: 1288-301.
43. Wang S, Trumble WR, Liao H, Wesson CR, Dunker AK, Kang CH. Crystal structure of calsequestrin from rabbit skeletal muscle sarcoplasmic reticulum. Nat. Struct. Biol. 1998; 5: 476-83.
44. Park H, Park IY, Kim E et al. Comparing skeletal and cardiac calsequestrin structures and their calcium binding: a proposed mechanism for coupled calcium binding and protein polymerization. J. Biol. Chem. 2004; 279: 18.
45. Park H, Wu S, Dunker AK, Kang C. Polymerization of calsequestrin. Implications for Ca2+ regulation. J. Biol. Chem. 2003; 278: 16.
46. 2+ regulation of single cardiac ryanodine receptors: insights provided by calsequestrin and its mutants. J. Gen. Physiol. 2008; 131: 325-34.
47. Valle G, Galla D, Nori A et al. Catecholaminergic polymorphic ventricular tachycardia-related mutations R33Q and L167H alter calcium sensitivity of human cardiac calsequestrin. Biochem. J. 2008; 413: 291-303.
48. 2+-binding protein changes in CSQ2 knockout mice. Am. J. Physiol. Heart Circ. Physiol. 2011; 300: H595-604.
49. 2+ storage levels in sarcoplasmic reticulum of fast- and slow-twitch fibres of rat. J. Physiol. 2009; 587: 443-60.
50. 2+. J. Membr. Biol. 1997; 159: 179-85.
51. 2+ release channel of skeletal muscle sarcoplasmic reticulum (ryanodine receptor isoform 1). J. Biol. Chem. 2004; 279: 37.
52. Zissimopoulos S, Lai FA. Ryanodine receptor structure, function and pathophysiology. In: Krebs J, Michalak M (eds). Calcium: A Matter of Life or Death. Elsevier, Oxford. 2007; 227-342.
53. + channel. J. Gen. Physiol. 2001; 117: 469-90.
54. Beard NA, Sakowska MM, Dulhunty AF, Laver DR. Calsequestrin is an inhibitor of skeletal muscle ryanodine receptor calcium release channels. Biophys. J. 2002; 82: 310-20.
55. Bers DM. Cardiac excitation-contraction coupling. Nature 2002; 415: 198-205.
56. Ginsburg KS, Weber CR, Bers DM. Control of maximum sarcoplasmic reticulum Ca load in intact ferret ventricular myocytes. Effects of thapsigargin and isoproterenol. J. Gen. Physiol. 1998; 111: 491-504.
57. 2+ release: cytoplasmic and luminal regulation modeled in a tetrameric channel. J. Gen. Physiol. 2008; 132: 429-46.
58. Xu L, Wang Y, Gillespie D, Meissner G. Two rings of negative charges in the cytosolic vestibule of type-1 ryanodine receptor modulate ion fluxes. Biophys. J. 2006; 90: 443-53.
59. Samso M, Wagenknecht T, Allen PD. Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM. Nat. Struct. Mol. Biol. 2005; 12: 539-44.