Functional abnormalities in iPSC-derived cardiomyocytes generated from CPVT1 and CPVT2 patients carrying ryanodine or calsequestrin mutations

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 8, 2015, Pages 2006-2018

  Novak, Atara ^a   Barad, Lili ^a   Lorber, Avraham ^a,b   Gherghiceanu, Mihaela ^c   Reiter, Irina ^a   Eisen, Binyamin ^a   Eldor, Liron ^b   Itskovitz Eldor, Joseph ^a   Eldar, Michael ^d   Arad, Michael ^d   Binah, Ofer ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b Department of Pediatric Cardiology ^*  (Israel)

^c VICTOR BABES NATIONAL INSTITUTE OF PATHOLOGY   (Romania)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

Arrhythmias; Ca2+ transients; Cardiomyocytes; Catacholaminergic polymorphic ventricular tachycardia; Induced pluripotent stem cells

Indexed keywords

CAFFEINE; CALCIUM ION; CALSEQUESTRIN; ISOPRENALINE; RYANODINE; RYANODINE RECEPTOR;

ADRENERGIC SYSTEM; ADULT; ARTICLE; CASE REPORT; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; HEART ARRHYTHMIA; HEART MUSCLE CELL; HUMAN; HUMAN TISSUE; INOTROPISM; MUTATION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SARCOLEMMA; SKIN BIOPSY; TRANSMISSION ELECTRON MICROSCOPY; CALCIUM SIGNALING; CARDIAC MUSCLE CELL; DRUG EFFECTS; GENETICS; GENOTYPING TECHNIQUE; HEART VENTRICLE TACHYCARDIA; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; SARCOPLASMIC RETICULUM; ULTRASTRUCTURE;

BASE SEQUENCE; CAFFEINE; CALCIUM SIGNALING; CALSEQUESTRIN; CELL DIFFERENTIATION; GENOTYPING TECHNIQUES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; ISOPROTERENOL; MOLECULAR SEQUENCE DATA; MUTATION; MYOCYTES, CARDIAC; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; TACHYCARDIA, VENTRICULAR;

EID: 84938206204     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12581     Document Type: Article

References (40)

1. Kontula K, Laitinen PJ, Lehtonen A, et al. Catecholaminergic polymorphic ventricular tachycardia: recent mechanistic insights. Cardiovasc Res. 2005; 67: 379-87.
2. Liu N, Priori SG. Disruption of calcium homeostasis and arrhythmogenesis induced by mutations in the cardiac ryanodine receptor and calsequestrin. Cardiovasc Res. 2008; 77: 293-301.
3. 2+ handling and arrhythmogenesis. Circ Res. 2012; 108: 871-83.
4. Fatima A, Xu G, Shao K, et al. In vitro modeling of ryanodine receptor 2 dysfunction using human induced pluripotent stem cells. Cell Physiol Biochem. 2011; 28: 579-92.
5. Itzhaki I, Maizels L, Huber I, et al. Modeling of catecholaminergic polymorphic ventricular tachycardia with patient-specific human-induced pluripotent stem cells. J Am Coll Cardiol. 2012; 60: 990-1000.
6. Jung CB, Moretti A, Mederos y Schnitzler 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: 180-91.
7. Novak A, Barad L, Zeevi-Levin N, et al. Cardiomyocytes generated from CPVTD307H patients are arrhythmogenic in response to beta-adrenergic stimulation. J Cell Mol Med. 2012; 16: 468-82.
8. 2+ signaling in human induced pluripotent stem cell-derived cardiomyocytes (iPS-CM) from normal and catecholaminergic polymorphic ventricular tachycardia (CPVT)-afflicted subjects. Cell Calcium. 2013; 54: 57-70.
9. Novak A, Shtrichman R, Germanguz I, et al. Enhanced reprogramming and cardiac differentiation of human keratinocytes derived from plucked hair follicles, using a single excisable lentivirus. Cell Reprogram. 2010; 12: 665-78.
10. Arad M, Glikson M, El-Ani D, et al. A family with recurrent sudden death and no clinical clue. Ann Noninvasive Electrocardiol. 2012; 17: 387-93.
11. Novak A, Lorber A, Itskovitz-Eldor J, et al. Modeling catecholaminergic polymorphic ventricular tachycardia using induced pluripotent stem cell-derived cardiomyocytes. Rambam Maimonides Med J. 2012; 3: e0015. Doi: 10.5041/RMMJ.10086.
12. Lee YK, Ng KM, Lai WH, et al. Calcium homeostasis in human induced pluripotent stem cell-derived cardiomyocytes. Stem Cell Rev. 2011; 7: 976-86.
13. Itzhaki I, Rapoport S, Huber I, et al. Calcium handling in human induced pluripotent stem cell derived cardiomyocytes. PLoS ONE. 2012; 6: e18037.
14. 2+ transients and contraction in cardiomyocytes derived from embryonic stem cells. FASEB J. 2006; 20: 181-3.
15. Kujala K, Paavola J, Lahti A, et al. Cell model of catecholaminergic polymorphic ventricular tachycardia reveals early and delayed afterdepolarizations. PLoS ONE. 2012; 7: e44660.
16. Di Pasquale E, Lodola F, Miragoli M, et al. CaMKII inhibition rectifies arrhythmic phenotype in a patient-specific model of catecholaminergic polymorphic ventricular tachycardia. Cell Death Dis. 2013; 4: e843.
17. 2+ release, and catecholaminergic polymorphic ventricular tachycardia. J Clin Invest. 2006; 116: 2510-20.
18. Postma AV, Denjoy I, Kamblock J, et al. Catecholaminergic polymorphic ventricular tachycardia: RYR2 mutations, bradycardia, and follow up of the patients. J Med Genet. 2005; 42: 863-70.
19. Song L, Alcalai R, Arad M, et al. Calsequestrin 2 (CASQ2) mutations increase expression of calreticulin and ryanodine receptors, causing catecholaminergic polymorphic ventricular tachycardia. J Clin Invest. 2007; 117: 1814-23.
20. Gherghiceanu M, Barad L, Novak A, et al. Cardiomyocytes derived from human embryonic and induced pluripotent stem cells: comparative ultrastructure. J Cell Mol Med. 2011; 15: 2539-51.
21. Kamakura T, Makiyama T, Sasaki K, et al. Ultrastructural maturation of human-induced pluripotent stem cell-derived cardiomyocytes in a long-term culture. Circ J. 2013; 77: 1307-14.
22. Kostin S, Klein G, Szalay Z, et al. Structural correlate of atrial fibrillation in human patients. Cardiovasc Res. 2002; 54: 361-79.
23. Kalyanasundaram A, Bal NC, Franzini-Armstrong C, et al. The calsequestrin mutation CASQ2D307H does not affect protein stability and targeting to the junctional sarcoplasmic reticulum but compromises its dynamic regulation of calcium buffering. J Biol Chem. 2010; 285: 3076-83.
24. Denegri M, Avelino-Cruz JE, Boncompagni S, et al. Viral gene transfer rescues arrhythmogenic phenotype and ultrastructural abnormalities in adult calsequestrin-null mice with inherited arrhythmias. Circ Res. 2013; 110: 663-8.
25. 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.
26. Valle G, Boncompagni S, Sacchetto R, et al. Post-natal heart adaptation in a knock-in mouse model of calsequestrin 2-linked recessive catecholaminergic polymorphic ventricular tachycardia. Exp Cell Res. 2013; 321: 178-89.
27. Marks AR. Calcium cycling proteins and heart failure: mechanisms and therapeutics. J Clin Invest. 2013; 123: 46-52.
28. Belevych AE, Radwanski PB, Carnes CA, et al. 'Ryanopathy': causes and manifestations of RyR2 dysfunction in heart failure. Cardiovasc Res. 2013; 98: 240-7.
29. Gaburjakova M, Bal NC, Gaburjakova J, et al. Functional interaction between calsequestrin and ryanodine receptor in the heart. Cell Mol Life Sci. 2013; 70: 2935-45.
30. 2+ handling and causes complex ventricular arrhythmias in mice. Cardiovasc Res. 2007; 75: 69-78.
31. Shan J, Kushnir A, Betzenhauser MJ, et al. Phosphorylation of the ryanodine receptor mediates the cardiac fight or flight response in mice. J Clin Invest. 2010; 120: 4388-98.
32. 2+ release. Am J Physiol. 1999; 276: C128-35.
33. 2+ current in ventricular cardiomyocytes. J Mol Cell Cardiol. 2010; 48: 26-36.
34. 2+-dependent inactivation of L-type calcium channels. Neuron. 1999; 22: 549-58.
35. Cerrone M, Noujaim SF, Tolkacheva EG, et al. Arrhythmogenic mechanisms in a mouse model of catecholaminergic polymorphic ventricular tachycardia. Circ Res. 2007; 101: 1039-48.
36. Kim E, Youn B, Kemper L, et al. Characterization of human cardiac calsequestrin and its deleterious mutants. J Mol Biol. 2007; 373: 1047-57.
37. Faggioni M, Knollmann BC. Calsequestrin 2 and arrhythmias. Am J Physiol Heart Circ Physiol. 2012; 302: H1250-60.
38. Bal NC, Jena N, Sopariwala D, et al. Probing cationic selectivity of cardiac calsequestrin and its CPVT mutants. Biochem J. 2011; 435: 391-9.
39. Germanguz I, Sedan O, Zeevi-Levin N, et al. Molecular characterization and functional properties of cardiomyocytes derived from human inducible pluripotent stem cells. J Mol Cell Med. 2011; 15: 38-51.
40. Satoh H. Electrophysiological actions of ryanodine on single rabbit sinoatrial nodal cells. Gen Pharmacol. 1997; 28: 31-8.