Triadin overexpression stimulates excitation-contraction coupling and increases predisposition to cellular arrhythmia in cardiac myocytes

Circulation Research

Volumn 96, Issue 6, 2005, Pages 651-658

  Terentyev, Dmitry ^a   Cala, Steven E ^b   Houle, Timothy D ^b   Viatchenko Karpinski, Serge ^a   Gyorke, Inna ^a   Terentyeva, Radmila ^a   Williams, Simon C ^c,d   Gyorke, Sandor ^a,d,e  

^a OHIO STATE UNIVERSITY   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^d UMC   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

Calcium induced calcium release; Calsequestrin; Catecholaminergic polymorphic ventricular tachycardia; Ryanodine receptor; Triadin

Indexed keywords

ADENOVIRUS VECTOR; CALSEQUESTRIN; JUNCTIN; MEMBRANE PROTEIN; PROTEIN; RYANODINE RECEPTOR; TRIADIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; C TERMINAL DOMAIN; CALCIUM SIGNALING; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DISEASE PREDISPOSITION; ELECTROSTIMULATION; EXCITATION CONTRACTION COUPLING; GENE OVEREXPRESSION; HEART DEPOLARIZATION; HEART MUSCLE CELL; LIPID BILAYER; MACROMOLECULE; MALE; MEMBRANE POTENTIAL; MICROSOME; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; RAT; SARCOPLASMIC RETICULUM; STOICHIOMETRY;

ADENOVIRIDAE; ANIMALS; ARRHYTHMIA; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; DOGS; ELECTRIC STIMULATION; GENE EXPRESSION; GENETIC VECTORS; ION CHANNEL GATING; LIPID BILAYERS; MACROMOLECULAR SUBSTANCES; MALE; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MICROSOMES; MIXED FUNCTION OXYGENASES; MODELS, CARDIOVASCULAR; MUSCLE PROTEINS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; TRANSDUCTION, GENETIC;

EID: 16444375139     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000160609.98948.25     Document Type: Article

References (35)

1. Bers DM. Excitation-Contraction Coupling and Cardiac Contractile Force, 2nd edition. Dordrecht. The Netherlands: Kluwer Academic Publishers; 2001.
2. Fabiato A. Time and calcium dependence of activation and inactivation of calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985;85:247-289.
3. 2+ release in cardiac myocytes. Circ Res. 2002;91:414-420.
4. Terentyev D, Viatchenko-Karpinski S, Gyorke I, Volpe P, Williams SC, Gyorke 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.
5. Bers DM. Macromolecular complexes regulating cardiac ryanodine receptor function. J Mol Cell Cardiol. 2004;37:417-429.
6. Priori SG, Napolitano C, Tiso N, Memmi M, Vignati G, Bloise R, Sorrentino VV, Danieli GA. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation. 2001;103:196-200.
7. Laitinen PJ, Brown KM, Piippo K, Swan H, Devaney JM, Brahmbhatt B, Donarum EA, Marino M, Tiso N, Viitasalo M, Toivonen L, Stephan DA, Kontula K. Mutations of the cardiac ryanodine receptor (RyR2) gene in familial polymorphic ventricular tachycardia. Circulation. 2001;103: 485-490.
8. Lahat H, Pras E, Olender T, Avidan N, Ben-Asher E, Man O, Levy-Nissenbaum E, Khoury A, Lorber A, Goldman B, Lancet D, Eldar M. 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. 2001;69: 1378-1384.
9. Postma AV, Denjoy I, Hoorntje TM, Lupoglazoff JM, Da Costa A, Sebillon P, Mannens MM, Wilde AA, Guicheney P. Absence of calsequestrin 2 causes severe forms of catecholaminergic polymorphic ventricular tachycardia. Circ Res. 2002;91:e21-e26.
10. Schmidt AG, Kadambi VJ, Ball N, Sato Y, Walsh RA, Kranias EG, Hoit BD. Cardiac-specific overexpression of calsequestrin results in left ventricular hypertrophy, depressed force-frequency relation and pulsus alternans in vivo. J Mol Cell Cardiol. 2000;32:1735-1744.
11. Kirchhefer U, Neumann J, Baba HA, Begrow F, Kobayashi YM, Reinke U, Schmitz W, Jones LR. Cardiac hypertrophy and impaired relaxation in transgenic mice overexpressing triadin 1. J Biol Chem. 2001;276: 4142-4149.
12. Kirchhefer U, Neumann J, Bers DM, Buchwalow IB, Fabritz L, Hanske G, Justus I, Riemann B, Schmitz W, Jones LR. Impaired relaxation in transgenic mice overexpressing junclin. Cardiovasc Res. 2003;59: 369-379.
13. 2+ signaling in transgenic mouse cardiac myocyles overexpressing calsequestrin. J Clin Invest. 1998;101:1385-1393.
14. Shorofsky SR, Aggarwal R, Correlli M, Baffa JM, Strum JM, Al-Seikhan BA, Kobayashi YM, Jones LR, Wier WG, Balke CW. Cellular mechanisms of altered contractility in the hypertrophied heart: big heans, big sparks. Circ Res. 1999;84:424-434.
15. Engelhardt S, Boknik P, Keller U, Neumann J, Lohse MJ, Hein L. Early impairment of calcium handling and altered expression of junclin in hearts of mice overexpressing the beta1-adrenergic receptor. FASEB J. 2001;15:2718-2720.
16. Jones LR, Zhang L, Sanborn K, Jorgensen AO, Kelley J. Purification, primary structure, and immunological characterizalion of the 26-kDa calsequestrin binding protein (junclin) from cardiac junctional sarcoplasmic reticulum. J Biol Chem. 1995;270:30787-30796.
17. Kobayashi YM, Jones LR. Identification of triadin 1 as the predominant triadin isoform expressed in mammalian myocardium. J Biol Chem. 1999;274:28660-28668.
18. 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;275:17639-17646.
19. Guo W, Jorgensen AO, Jones LR, Campbell KP. Biochemical characterization and molecular cloning of cardiac triadin. J Biol Chem. 1996;271: 458-465.
20. Realini C, Rogers SW, Rechsteiner M. KEKE moiifs. Proposed roles in protein-protein association and presentation of peptides by MHC class I receptors. FEBS Lett. 1994;348:109-113.
21. 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;272:23389-23397.
22. Lee JM, Rho SH, Shin DW, Cho C, Park WJ, Eom SH, Ma J, Kim do H. 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.
23. Zhang L, Franzini-Armstrong C, Ramesh V, Jones LR. Structural alterations in cardiac calcium release units resulting from overexpression of junctin. J Mol Cell Cardiol. 2001;33:233-247.
24. 2+ sensing sites. Biophys J,. 1998; 75:2801-2810.
25. Houle T, Ram M, Cala, S. Calsequestrin mutant D307H exhibits depressed binding to its protein targets and a depressed response to calcium. Cardiovasc Res. 2004;64:227-233.
26. Allen DG, Eisner DA, Orchard CH. Characterization of oscillations of intracellular calcium concentration in ferret ventricular muscle. J Physiol. 1984;352:113-128.
27. Lakatta EG, Guarnieri T. Spontaneous myocardial calcium oscillations: are they linked to ventricular fibrillation? J Cardiovasc Electrophysiol. 1993;4:473-489.
28. Marban E, Robinson SW, Wier WG. Mechanisms of arrhythmogenic delayed and early afterdepolarizations in ferret ventricular muscle. J Clin Invest. 1986;78:1185-1192.
29. Cordeiro JM, Bridge JH, Spitzer KW. Early and delayed afterdepolarizations in rabbit heart Purkinje cells viewed by confocal microscopy. Cell Calcium. 2001;29:289-297.
30. Viatchenko-Karpinski S, Terentyev D, Gyorke I, Terentyeva R, Volpe P, Priori SG, Napolitano C, Non A, Williams SC, Gyorke S. Abnormal calcium signaling and sudden cardiac death associated with mutation of calsequestrin. Circ Res. 2004;94:471-477.
31. 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;86:2121-2128.
32. Wehrens XH, Lehnart SE, Huang F, Vest JA, Reiken SR, Mohler PJ, Sun J, Guatimosim S, Song LS, Rosemblit N, D'Armiento JM, Napolitano C, Memmi M, Priori SG, Lederer WJ, Marks AR. FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell. 2003;113:829-840.
33. George CH, Higgs GV, Lai FA. Ryanodine receptor mutations associated with stress-induced ventricular tachycardia mediate increased calcium release in stimulated cardiomyocytes. Circ Res. 2003;93:531-540.
34. Kubalova Z, Gyorke I, Terentyeva R, Viatchenko-Karpinski S, Terentyev D, Williams SC, Gyorke S. Modulation of cytosolic and intra-SR calcium waves by calsequestrin in cardiac myocytes. J Physiol. 2004;561: 515-524.
35. 2+ release (SOICR). Proc Natl Acad Sci U S A. 2004;101:13062-13067.