Abnormal calcium handling properties underlie familial hypertrophic cardiomyopathy pathology in patient-specific induced pluripotent stem cells

Cell Stem Cell

Volumn 12, Issue 1, 2013, Pages 101-113

  Lan, Feng ^a   Lee, Andrew S ^a   Liang, Ping ^a   Sanchez Freire, Veronica ^a   Nguyen, Patricia K ^a   Wang, Li ^a   Han, Leng ^a   Yen, Michelle ^a   Wang, Yongming ^a   Sun, Ning ^a   Abilez, Oscar J ^a   Hu, Shijun ^a   Ebert, Antje D ^a   Navarrete, Enrique G ^a   Simmons, Chelsey S ^b   Wheeler, Matthew ^a   Pruitt, Beth ^b   Lewis, Richard ^a   Yamaguchi, Yoshinori ^c   Ashley, Euan A ^a   Bers, Donald M ^d   Robbins, Robert C ^a   Longaker, Michael T ^a   Wu, Joseph C ^a   more..

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Stanford University   (United States)

^c OSAKA UNIVERSITY   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CONTRACTILE PROTEIN;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CELL ENLARGEMENT; CLINICAL ARTICLE; CONTROLLED STUDY; FAMILIAL HYPERTROPHIC CARDIOMYOPATHY; FEMALE; HEART ELECTROPHYSIOLOGY; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HUMAN; HUMAN CELL; MALE; MISSENSE MUTATION; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL;

CALCIUM; CARDIAC MYOSINS; CARDIOMYOPATHY, HYPERTROPHIC, FAMILIAL; CELLS, CULTURED; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MUTATION, MISSENSE; MYOSIN HEAVY CHAINS;

EID: 84872026086     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.10.010     Document Type: Article

References (37)

1. A.S. Adabag, B.J. Maron, E. Appelbaum, C.J. Harrigan, J.L. Buros, C.M. Gibson, J.R. Lesser, C.A. Hanna, J.E. Udelson, W.J. Manning, and M.S. Maron Occurrence and frequency of arrhythmias in hypertrophic cardiomyopathy in relation to delayed enhancement on cardiovascular magnetic resonance J. Am. Coll. Cardiol. 51 2008 1369 1374
2. M. Arad, J.G. Seidman, and C.E. Seidman Phenotypic diversity in hypertrophic cardiomyopathy Hum. Mol. Genet. 11 2002 2499 2506
3. J.R. Berlin, M.B. Cannell, and W.J. Lederer Cellular origins of the transient inward current in cardiac myocytes. Role of fluctuations and waves of elevated intracellular calcium Circ. Res. 65 1989 115 126
4. D.M. Bers Calcium cycling and signaling in cardiac myocytes Annu. Rev. Physiol. 70 2008 23 49
5. P.W. Burridge, G. Keller, J.D. Gold, and J.C. Wu Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming Cell Stem Cell 10 2012 16 28
6. F. Cao, R.A. Wagner, K.D. Wilson, X. Xie, J.D. Fu, M. Drukker, A. Lee, R.A. Li, S.S. Gambhir, and I.L. Weissman Transcriptional and functional profiling of human embryonic stem cell-derived cardiomyocytes PLoS One 3 2008 e3474
7. X. Carvajal-Vergara, A. Sevilla, S.L. D'Souza, Y.S. Ang, C. Schaniel, D.F. Lee, L. Yang, A.D. Kaplan, E.D. Adler, and R. Rozov Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome Nature 465 2010 808 812
8. G.M. De Ferrari, M.C. Viola, E. D'Amato, R. Antolini, and S. Forti Distinct patterns of calcium transients during early and delayed afterdepolarizations induced by isoproterenol in ventricular myocytes Circulation 91 1995 2510 2515
9. D. Fatkin, and R.M. Graham Molecular mechanisms of inherited cardiomyopathies Physiol. Rev. 82 2002 945 980
10. D. Fatkin, M.E. Christe, O. Aristizabal, B.K. McConnell, S. Srinivasan, F.J. Schoen, C.E. Seidman, D.H. Turnbull, and J.G. Seidman Neonatal cardiomyopathy in mice homozygous for the Arg403Gln mutation in the alpha cardiac myosin heavy chain gene J. Clin. Invest. 103 1999 147 153
11. D. Fatkin, B.K. McConnell, J.O. Mudd, C. Semsarian, I.G. Moskowitz, F.J. Schoen, M. Giewat, C.E. Seidman, and J.G. Seidman An abnormal Ca(2+) response in mutant sarcomere protein-mediated familial hypertrophic cardiomyopathy J. Clin. Invest. 106 2000 1351 1359
12. A.A. Geisterfer-Lowrance, S. Kass, G. Tanigawa, H.P. Vosberg, W. McKenna, C.E. Seidman, and J.G. Seidman A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation Cell 62 1990 999 1006
13. E.J. Gruver, D. Fatkin, G.A. Dodds, J. Kisslo, B.J. Maron, J.G. Seidman, and C.E. Seidman Familial hypertrophic cardiomyopathy and atrial fibrillation caused by Arg663His beta-cardiac myosin heavy chain mutation Am. J. Cardiol. 83 12A 1999 13H 18H
14. M.M. Hossain, E. Shimizu, M. Saito, S.R. Rao, Y. Yamaguchi, and E. Tamiya Non-invasive characterization of mouse embryonic stem cell derived cardiomyocytes based on the intensity variation in digital beating video Analyst (Lond.) 135 2010 1624 1630
15. I. Itzhaki, L. Maizels, I. Huber, L. Zwi-Dantsis, O. Caspi, A. Winterstern, O. Feldman, A. Gepstein, G. Arbel, and H. Hammerman Modelling the long QT syndrome with induced pluripotent stem cells Nature 471 2011 225 229
16. V. Iyer, R.J. Hajjar, and A.A. Armoundas Mechanisms of abnormal calcium homeostasis in mutations responsible for catecholaminergic polymorphic ventricular tachycardia Circ. Res. 100 2007 e22 e31
17. B.C. Knollmann, P. Kirchhof, S.G. Sirenko, H. Degen, A.E. Greene, T. Schober, J.C. Mackow, L. Fabritz, J.D. Potter, and M. Morad Familial hypertrophic cardiomyopathy-linked mutant troponin T causes stress-induced ventricular tachycardia and Ca2+-dependent action potential remodeling Circ. Res. 92 2003 428 436
18. A.M. Lompre, J.J. Mercadier, C. Wisnewsky, P. Bouveret, C. Pantaloni, A. D'Albis, and K. Schwartz Species- and age-dependent changes in the relative amounts of cardiac myosin isoenzymes in mammals Dev. Biol. 84 1981 286 290
19. S. Lowey, L.M. Lesko, A.S. Rovner, A.R. Hodges, S.L. White, R.B. Low, M. Rincon, J. Gulick, and J. Robbins Functional effects of the hypertrophic cardiomyopathy R403Q mutation are different in an alpha- or beta-myosin heavy chain backbone J. Biol. Chem. 283 2008 20579 20589
20. A.J. Marian, G. Zhao, Y. Seta, R. Roberts, and Q.T. Yu Expression of a mutant (Arg92Gln) human cardiac troponin T, known to cause hypertrophic cardiomyopathy, impairs adult cardiac myocyte contractility Circ. Res. 81 1997 76 85
21. B.J. Maron Hypertrophic cardiomyopathy: a systematic review JAMA 287 2002 1308 1320
22. B.J. Maron, J.M. Gardin, J.M. Flack, S.S. Gidding, T.T. Kurosaki, and D.E. Bild Prevalence of hypertrophic cardiomyopathy in a general population of young adults. Echocardiographic analysis of 4111 subjects in the CARDIA Study. Coronary Artery Risk Development in (Young) Adults Circulation 92 1995 785 789
23. B.J. Maron, J. Shirani, L.C. Poliac, R. Mathenge, W.C. Roberts, and F.O. Mueller Sudden death in young competitive athletes. Clinical, demographic, and pathological profiles JAMA 276 1996 199 204
24. M.S. Maron, I. Olivotto, S. Betocchi, S.A. Casey, J.R. Lesser, M.A. Losi, F. Cecchi, and B.J. Maron Effect of left ventricular outflow tract obstruction on clinical outcome in hypertrophic cardiomyopathy N. Engl. J. Med. 348 2003 295 303
25. J.D. Molkentin, J.R. Lu, C.L. Antos, B. Markham, J. Richardson, J. Robbins, S.R. Grant, and E.N. Olson A calcineurin-dependent transcriptional pathway for cardiac hypertrophy Cell 93 1998 215 228
26. A. Moretti, M. Bellin, A. Welling, C.B. Jung, J.T. Lam, L. Bott-Flügel, T. Dorn, A. Goedel, C. Höhnke, and F. Hofmann Patient-specific induced pluripotent stem-cell models for long-QT syndrome N. Engl. J. Med. 363 2010 1397 1409
27. K. Narsinh, K.H. Narsinh, and J.C. Wu Derivation of human induced pluripotent stem cells for cardiovascular disease modeling Circ. Res. 108 2011 1146 1156
28. K.H. Narsinh, N. Sun, V. Sanchez-Freire, A.S. Lee, P. Almeida, S. Hu, T. Jan, K.D. Wilson, D. Leong, and J. Rosenberg Single cell transcriptional profiling reveals heterogeneity of human induced pluripotent stem cells J. Clin. Invest. 121 2011 1217 1221
29. J.G. Seidman, and C. Seidman The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms Cell 104 2001 557 567
30. C. Semsarian, I. Ahmad, M. Giewat, D. Georgakopoulos, J.P. Schmitt, B.K. McConnell, S. Reiken, U. Mende, A.R. Marks, and D.A. Kass The L-type calcium channel inhibitor diltiazem prevents cardiomyopathy in a mouse model J. Clin. Invest. 109 2002 1013 1020
31. N. Sun, M. Yazawa, J. Liu, L. Han, V. Sanchez-Freire, O.J. Abilez, E.G. Navarrete, S. Hu, L. Wang, and A. Lee Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy Sci. Transl. Med. 4 2012 130ra147
32. M.A. Sussman, H.W. Lim, N. Gude, T. Taigen, E.N. Olson, J. Robbins, M.C. Colbert, A. Gualberto, D.F. Wieczorek, and J.D. Molkentin Prevention of cardiac hypertrophy in mice by calcineurin inhibition Science 281 1998 1690 1693
33. D. Teare Asymmetrical hypertrophy of the heart in young adults Br. Heart J. 20 1958 1 8
34. M.J. Tyska, E. Hayes, M. Giewat, C.E. Seidman, J.G. Seidman, and D.M. Warshaw Single-molecule mechanics of R403Q cardiac myosin isolated from the mouse model of familial hypertrophic cardiomyopathy Circ. Res. 86 2000 737 744
35. C.M. Wolf, I.P. Moskowitz, S. Arno, D.M. Branco, C. Semsarian, S.A. Bernstein, M. Peterson, M. Maida, G.E. Morley, and G. Fishman Somatic events modify hypertrophic cardiomyopathy pathology and link hypertrophy to arrhythmia Proc. Natl. Acad. Sci. USA 102 2005 18123 18128
36. L. Yang, M.H. Soonpaa, E.D. Adler, T.K. Roepke, S.J. Kattman, M. Kennedy, E. Henckaerts, K. Bonham, G.W. Abbott, and R.M. Linden Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population Nature 453 2008 524 528
37. M. Yazawa, B. Hsueh, X. Jia, A.M. Pasca, J.A. Bernstein, J. Hallmayer, and R.E. Dolmetsch Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome Nature 471 2011 230 234