CaMKII inhibition rectifies arrhythmic phenotype in a patient-specific model of catecholaminergic polymorphic ventricular tachycardia

Cell Death and Disease

Volumn 4, Issue 10, 2013, Pages

  Di Pasquale, E ^a   Lodola, F ^b   Miragoli, M ^c,d   Denegri, M ^b   Avelino Cruz, J E ^b   Buonocore, M ^b   Nakahama, H ^c   Portararo, P ^e   Bloise, R ^b   Napolitano, C ^b,f   Condorelli, G ^d   Priori, S G ^b,c,f,g  

^a Milan Unit   (Italy)

^b IRCCS   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF PARMA   (Italy)

^e IRCCS MULTIMEDICA   (Italy)

^f UNIVERSITY OF PAVIA   (Italy)

^g NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium calmodulin pathway; Cardiomyocytes; CPVT; Diseases modeling; Induced pluripotent stem cells

Indexed keywords

ANTIARRHYTHMIC AGENT; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; ISOPRENALINE; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; RYANODINE RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIARRHYTHMIC ACTIVITY; ARTICLE; BETA ADRENERGIC STIMULATION; CALCIUM CELL LEVEL; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; CONTROLLED STUDY; DEPOLARIZATION; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAM; ENZYME INHIBITION; HEART MUSCLE CELL; HEART VENTRICLE EXTRASYSTOLE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OPTICAL RESOLUTION; PATCH CLAMP; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SUDDEN CARDIAC DEATH; WHOLE CELL;

ADOLESCENT; ADULT; ANIMALS; ARRHYTHMIAS, CARDIAC; BASE SEQUENCE; BENZYLAMINES; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL DIFFERENTIATION; CHILD; CHILD, PRESCHOOL; FEMALE; HEK293 CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MICE; MOLECULAR SEQUENCE DATA; MYOCYTES, CARDIAC; PEDIGREE; PHENOTYPE; PROTEIN KINASE INHIBITORS; RECEPTORS, ADRENERGIC, BETA; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SULFONAMIDES; TACHYCARDIA, VENTRICULAR;

EID: 84887454024     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.369     Document Type: Article

References (43)

1. Josowitz R, Carvajal-Vergara X, Lemischka IR, Gelb BD. Induced pluripotent stem cell-derived cardiomyocytes as models for genetic cardiovascular disorders. Curr Opin Cardiol 2011; 26: 223-229
2. Park IH, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A et al. Disease-specific induced pluripotent stem cells. Cell 2008; 134: 877-886
3. Priori SG, Napolitano C, Di Pasquale E, Condorelli G. Induced pluripotent stem cell-derived cardiomyocytes in studies of inherited arrhythmias. J Clin Invest 2013; 123: 84-91
4. Carvajal-Vergara X, Sevilla A, DSouza SL, Ang YS, Schaniel C, Lee DF et al. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 2011; 465: 808-812
5. Itzhaki I, Maizels L, Huber I, Zwi-Dantsis L, Caspi O, Winterstern A et al. Modelling the long QT syndrome with induced pluripotent stem cells. Nature 2011; 471: 225-229
6. Jung CB, Moretti A, Mederos y Schnitzler M, Iop L, Storch U, Bellin M et al. Dantrolene rescues arrhythmogenic RYR2 defect in a patient-specific stem cell model of catecholaminergic polymorphic ventricular tachycardia. EMBO Mol Med 2012; 4: 180-191
7. Sun N, Yazawa M, Liu J, Han L, Sanchez-Freire V, Abilez OJ et al. Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy. Sci Transl Med 2012; 4: 130ra147
8. Yazawa M, Hsueh B, Jia X, Pasca AM, Bernstein JA, Hallmayer J et al. Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome. Nature 2011; 471: 230-234
9. Moretti A, Bellin M, Welling A, Jung CB, Lam JT, Bott-Flugel L et al. Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med 2010; 363: 1397-1409
10. Itzhaki I, Maizels L, Huber I, Gepstein A, Arbel G, Caspi O et al. Modeling of catecholaminergic polymorphic ventricular tachycardia with patient-specific human-induced pluripotent stem cells. J Am Coll Cardiol 2012; 60: 990-1000
11. Fatima A, Xu G, Shao K, Papadopoulos S, Lehmann M, Arnaiz-Cot JJ et al. In vitro modeling of ryanodine receptor 2 dysfunction using human induced pluripotent stem cells. Cell Physiol Biochem 2011; 28: 579-592
12. Kujala K, Paavola J, Lahti A, Larsson K, Pekkanen-Mattila M, Viitasalo M et al. Cell model of catecholaminergic polymorphic ventricular tachycardia reveals early and delayed afterdepolarizations. PLoS One 2012; 7: E44660
13. Novak A, Barad L, Zeevi-Levin N, Shick R, Shtrichman R, Lorber A et al. Cardiomyocytes generated from CPVTD307H patients are arrhythmogenic in response to beta-adrenergic stimulation. J Cell Mol Med 2012; 16: 468-482
14. Lahat H, Pras E, Eldar M. A missense mutation in CASQ2 is associated with autosomal recessive catecholamine-induced polymorphic ventricular tachycardia in Bedouin families from Israel. Ann Med 2004; 36(Suppl 1): 87-91
15. Priori SG, Napolitano C, Tiso N, Memmi M, Vignati G, Bloise R et al. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation 2001; 103: 196-200
16. Marx SO, Marks AR. Dysfunctional ryanodine receptors in the heart: New insights into complex cardiovascular diseases. J Mol Cell Cardiol 2013; 58: 225-231
17. Venetucci L, Denegri M, Napolitano C, Priori SG. Inherited calcium channelopathies in the pathophysiology of arrhythmias. Nat Rev Cardiol 2012; 9: 561-575
18. Priori SG, Napolitano C, Memmi M, Colombi B, Drago F, Gasparini M et al. Clinical and molecular characterization of patients with catecholaminergic polymorphic ventricular tachycardia. Circulation 2002; 106: 69-74
19. Cerrone M, Cummings S, Alansari T, Priori SG. A clinical approach to inherited arrhythmias. Circ Cardiovasc Genet 2012; 5: 581-590
20. Ai X, Curran JW, Shannon TR, Bers DM, Pogwizd SM. Ca2+/calmodulin- dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 2005; 97: 1314-1322
21. Liu N, Ruan Y, Denegri M, Bachetti T, Li Y, Colombi B et al. Calmodulin kinase II inhibition prevents arrhythmias in RyR2(R4496C+/-) mice with catecholaminergic polymorphic ventricular tachycardia. J Mol Cell Cardiol 2011; 50: 214-222
22. Terentyev D, Belevych AE, Terentyeva R, Martin MM, Malana GE, Kuhn DE et al. miR-1 overexpression enhances Ca(2+) release and promotes cardiac arrhythmogenesis by targeting PP2A regulatory subunit B56alpha and causing CaMKII-dependent hyperphosphorylation of RyR2. Circ Res 2009; 104: 514-521
23. Di Pasquale E, Belle S, Condorelli G. Generation of human cardiomyocytes: A differentiation protocol from feeder-free human induced pluripotent stem cells. J Vis Exp 2013; 76; doi:10.3791/50429
24. Zhu WZ, Xie Y, Moyes KW, Gold JD, Askari B, Laflamme MA. Neuregulin/ErbB signaling regulates cardiac subtype specification in differentiating human embryonic stem cells. Circ Res 2010; 107: 776-786
25. Myles RC, Wang L, Kang C, Bers DM, Ripplinger CM. Local beta-adrenergic stimulation overcomes source-sink mismatch to generate focal arrhythmia. Circ Res 2012; 110: 1454-1464
26. Abriel H, Zaklyazminskaya EV. Cardiac channelopathies: Genetic and molecular mechanisms. Gene 2012; 517: 1-11
27. Priori SG, Chen SR. Inherited dysfunction of sarcoplasmic reticulum Ca2+ handling and arrhythmogenesis. Circ Res 2011; 108: 871-883
28. Mercola M, Colas A, Willems E. Induced pluripotent stem cells in cardiovascular drug discovery. Circ Res 2013; 112: 534-548
29. Herron TJ, Lee P, Jalife J. Optical imaging of voltage and calcium in cardiac cells&tissues. Circ Res 2012; 110: 609-623
30. Liu N, Napolitano C, Venetucci LA, Priori SG. Flecainide and antiarrhythmic effects in a mouse model of catecholaminergic polymorphic ventricular tachycardia. Trends Cardiovasc Med 2012; 22: 35-39
31. Watanabe H, Chopra N, Laver D, Hwang HS, Davies SS, Roach DE et al. Flecainide prevents catecholaminergic polymorphic ventricular tachycardia in mice and humans. Nat Med 2009; 15: 380-383
32. Liu N, Denegri M, Ruan Y, Avelino-Cruz JE, Perissi A, Negri S et al. Short communication: Flecainide exerts an antiarrhythmic effect in a mouse model of catecholaminergic polymorphic ventricular tachycardia by increasing the threshold for triggered activity. Circ Res 2011; 109: 291-295
33. Sikkel MB, Collins TP, Rowlands C, Shah M, OGara P, Williams AJ et al. Flecainide reduces Ca2+ spark and wave frequency via inhibition of the sarcolemmal sodium current. Cardiovasc Res 2013; 98: 286-296
34. Kobayashi S, Yano M, Suetomi T, Ono M, Tateishi H, Mochizuki M et al. Dantrolene, a therapeutic agent for malignant hyperthermia, markedly improves the function of failing cardiomyocytes by stabilizing interdomain interactions within the ryanodine receptor. J Am Coll Cardiol 2009; 53: 1993-2005
35. Maxwell JT, Domeier TL, Blatter LA. Dantrolene prevents arrhythmogenic Ca2+ release in heart failure. Am J Physiol Heart Circ Physiol 2011; 302: H953-H963
36. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T et al. Fiji: An open-source platform for biological-image analysis. Nat Methods 2012; 9: 676-682
37. Sullivan S, Egli D, Akutsu H, Melton DA, Eggan K, Cowan C. Derivation of human embryonic stem cells. Hum Embryonic Stem Cells (The Practical Handbook) 2007, chapter 4: Pp 35-51
38. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872
39. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318: 1917-1920
40. Gallo P, Grimaldi S, Latronico MV, Bonci D, Pagliuca A, Gallo P et al. A lentiviral vector with a short troponin-I promoter for tracking cardiomyocyte differentiation of human embryonic stem cells. Gene Ther 2008; 15: 161-170
41. Huangfu D, Maehr R, Guo W, Eijkelenboom A, Snitow M, Chen AE et al. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 2008; 26: 795-797
42. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002; 30: E36
43. Miragoli M, Novak P, Ruenraroengsak P, Shevchuk AI, Korchev YE, Lab MJ et al. Functional interaction between charged nanoparticles and cardiac tissue: A new paradigm for cardiac arrhythmia? Nanomedicine (Lond) 2012; 8: 725-737