Induced pluripotent stem cells for the study of cardiovascular disease

Journal of the American College of Cardiology

Volumn 64, Issue 5, 2014, Pages 512-519

  Savla, Jainy J ^a   Nelson, Bradley C ^a   Perry, Cynthia N ^b   Adler, Eric D ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Paul L Foster School of Medicine   (United States)

Author keywords

cardiomyocyte; cardiomyopathy; differentiation; long QT syndrome; pluripotent stem cell

Indexed keywords

ALFUZOSIN; KRUPPEL LIKE FACTOR 4; LAMIN A; LAMIN C; MYC PROTEIN; MYOSIN HEAVY CHAIN BETA; OCTAMER TRANSCRIPTION FACTOR 4; PLAKOPHILIN; POTASSIUM CHANNEL HERG; POTASSIUM CHANNEL KCNQ1; PROTEIN TYROSINE PHOSPHATASE SHP 2; RETROVIRUS VECTOR; RYANODINE RECEPTOR 2; TRANSCRIPTION FACTOR SOX2; TROPONIN T; VERAPAMIL;

ARTICLE; BIOCHEMISTRY; CACNA1C GENE; CARDIOVASCULAR DISEASE; CASQ2 GENE; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; CELL CULTURE; CELL DIFFERENTIATION; CELL RENEWAL; CELL TYPE; CONGESTIVE CARDIOMYOPATHY; DISEASE MODEL; DRUG SCREENING; EMBRYONIC STEM CELL; GENE; GLYCOGEN STORAGE DISEASE TYPE 2; HEART MUSCLE CELL; HEART RIGHT VENTRICLE DYSPLASIA; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; KCNH2 GENE; KCNQ1 GENE; LEOPARD SYNDROME; LMNA GENE; LONG QT SYNDROME; MEDICAL RESEARCH; MISSENSE MUTATION; MYH7 GENE; NONHUMAN; NONSENSE MUTATION; PKP2 GNENE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PTPN11 GENE; RYR2 GENE; SCN5A GENE; SKIN BIOPSY; SKIN FIBROBLAST; SOMATIC CELL; TNNT2 GENE;

CARDIOMYOCYTE; CARDIOMYOPATHY; DIFFERENTIATION; LONG QT SYNDROME; PLURIPOTENT STEM CELL;

CARDIOVASCULAR DISEASES; CELL DIFFERENTIATION; CELL- AND TISSUE-BASED THERAPY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MYOCYTES, CARDIAC;

EID: 84905159229     PISSN: 07351097     EISSN: 15583597     Source Type: Journal    
DOI: 10.1016/j.jacc.2014.05.038     Document Type: Review

References (72)

1. P. Perel, I. Roberts, and E. Sena et al. Comparison of treatment effects between animal experiments and clinical trials: systematic review BMJ 334 2007 197
2. P. Pound, S. Ebrahim, P. Sandercock, M.B. Bracken, and I. Roberts Where is the evidence that animal research benefits humans? BMJ 328 2004 514 517
3. P. Sandercock, and I. Roberts Systematic reviews of animal experiments Lancet 360 2002 586
4. D.G. Hackam, and D.A. Redelmeier Translation of research evidence from animals to humans JAMA 296 2006 1731 1732
5. M.J. Evans, and M.H. Kaufman Establishment in culture of pluripotential cells from mouse embryos Nature 292 1981 154 156
6. J.A. Thomson, J. Itskovitz-Eldor, and S.S. Shapiro et al. Embryonic stem cell lines derived from human blastocysts Science 282 1998 1145 1147
7. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676
8. K. Takahashi, K. Tanabe, and M. Ohnuki et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872
9. J. Yu, M.A. Vodyanik, and K. Smuga-Otto et al. Induced pluripotent stem cell lines derived from human somatic cells Science 318 2007 1917 1920
10. I.-H. Park, R. Zhao, and J.A. West et al. Reprogramming of human somatic cells to pluripotency with defined factors Nature 451 2008 141 146
11. K. Si-Tayeb, F.K. Noto, and M. Nagaoka et al. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells Hepatology 51 2010 297 305
12. D. Zhang, W. Jiang, and M. Liu et al. Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells Cell Res 19 2009 429 438
13. J. Zhang, G.F. Wilson, and A.G. Soerens et al. Functional cardiomyocytes derived from human induced pluripotent stem cells Circ Res 104 2009 e30 e41
14. C. Mummery, D. Ward-van Oostwaard, and P. Doevendans et al. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells Circulation 107 2003 2733 2740
15. R. Passier, D.W. Oostwaard, and J. Snapper et al. Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures Stem Cells 23 2005 772 780
16. C. Freund, D. Ward-van Oostwaard, and J. Monshouwer-Kloots et al. Insulin redirects differentiation from cardiogenic mesoderm and endoderm to neuroectoderm in differentiating human embryonic stem cells Stem Cells 26 2008 724 733
17. R. Graichen, X. Xu, and S.R. Braam et al. Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK Differentiation 76 2008 357 370
18. X.Q. Xu, R. Graichen, and S.Y. Soo et al. Chemically defined medium supporting cardiomyocyte differentiation of human embryonic stem cells Differentiation 76 2008 958 970
19. J. Itskovitz-Eldor, M. Schuldiner, and D. Karsenti et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers Mol Med 6 2000 88 95
20. I. Kehat, D. Kenyagin-Karsenti, and M. Snir et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes J Clin Invest 108 2001 407 414
21. C. Xu, S. Police, N. Rao, and M.K. Carpenter Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells Circ Res 91 2002 501 508
22. S. Takei, H. Ichikawa, and K. Johkura et al. Bone morphogenetic protein-4 promotes induction of cardiomyocytes from human embryonic stem cells in serum-based embryoid body development Am J Physiol Heart Circ Physiol 296 2009 H1793 H1803
23. T.H. Tran, X. Wang, and C. Browne et al. Wnt3a-induced mesoderm formation and cardiomyogenesis in human embryonic stem cells Stem Cells 27 2009 1869 1878
24. L. Yang, M.H. Soonpaa, and E.D. Adler et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population Nature 453 2008 524 528
25. Y. Ren, M.Y. Lee, and S. Schliffke et al. Small molecule Wnt inhibitors enhance the efficiency of BMP-4-directed cardiac differentiation of human pluripotent stem cells J Mol Cell Cardiol 51 2011 280 287
26. S.J. Kattman, A.D. Witty, and M. Gagliardi et al. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines Cell Stem Cell 8 2011 228 240
27. E. Willems, S. Spiering, and H. Davidovics et al. Small-molecule inhibitors of the Wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm Circ Res 109 2011 360 364
28. M.A. Laflamme, K.Y. Chen, and A.V. Naumova et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts Nat Biotechnol 25 2007 1015 1024
29. S.L. Paige, T. Osugi, O.K. Afanasiev, L. Pabon, H. Reinecke, and C.E. Murry Endogenous Wnt/beta-catenin signaling is required for cardiac differentiation in human embryonic stem cells PLoS One 5 2010 e11134
30. H. Uosaki, H. Fukushima, and A. Takeuchi et al. Efficient and scalable purification of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression PLoS One 6 2011 e23657
31. J.E. Hudson, and W.-H. Zimmermann Tuning Wnt-signaling to enhance cardiomyogenesis in human embryonic and induced pluripotent stem cells J Mol Cell Cardiol 51 2011 277 279
32. X. Lian, C. Hsiao, and G. Wilson et al. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling Proc Natl Acad Sci U S A 109 2012 E1848 E1857
33. J.Q. He, Y. Ma, Y. Lee, J.A. Thomson, and T.J. Kamp Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization Circ Res 93 2003 32 39
34. H.S. Chen, C. Kim, and M. Mercola Electrophysiological challenges of cell-based myocardial repair Circulation 120 2009 2496 2508
35. N. Zeevi-Levin, J. Itskovitz-Eldor, and O. Binah Functional properties of human embryonic stem cell-derived cardiomyocytes Crit Rev Eukaryot Gene Expr 20 2010 51 59
36. M. Mercola, A. Colas, and E. Willems Induced pluripotent stem cells in cardiovascular drug discovery Circ Res 112 2013 534 548
37. X. Yang, L. Pabon, and C.E. Murry Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes Circ Res 114 2014 511 523
38. M. Snir, I. Kehat, and A. Gepstein et al. Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes Am J Physiol Heart Circ Physiol 285 2003 H2355 H2363
39. L. Zwi, O. Caspi, and G. Arbel et al. Cardiomyocyte differentiation of human induced pluripotent stem cells Circulation 120 2009 1513 1523
40. D.K. Lieu, J. Liu, and C.-W. Siu et al. Absence of transverse tubules contributes to non-uniform Ca(2+) wavefronts in mouse and human embryonic stem cell-derived cardiomyocytes Stem Cells Dev 18 2009 1493 1500
41. J. Satin, I. Itzhaki, and S. Rapoport et al. Calcium handling in human embryonic stem cell-derived cardiomyocytes Stem Cells 26 2008 1961 1972
42. X. Carvajal-Vergara, A. Sevilla, and S.L. D'Souza et al. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome Nature 465 2010 808 812
43. F. Lan, A.S. Lee, and P. Liang et al. Abnormal calcium handling properties underlie familial hypertrophic cardiomyopathy pathology in patient-specific induced pluripotent stem cells Cell Stem Cell 12 2013 101 113
44. J.C.Y. Ho, T. Zhou, and W.-H. Lai et al. Generation of induced pluripotent stem cell lines from 3 distinct laminopathies bearing heterogeneous mutations in lamin A/C Aging (Albany NY) 3 2011 380 390
45. C.W. Siu, Y.-K. Lee, and J.C.-Y. Ho et al. Modeling of lamin A/C mutation premature cardiac aging using patient-specific induced pluripotent stem cells Aging (Albany NY) 4 2012 803 822
46. N. Sun, M. Yazawa, and J. Liu et al. Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy Sci Transl Med 4 2012 130ra47
47. A. Moretti, M. Bellin, and A. Welling Patient-specific induced pluripotent stem-cell models for long-QT syndrome N Engl J Med 363 2010 1397 1409
48. T. Egashira, S. Yuasa, and T. Suzuki et al. Disease characterization using LQTS-specific induced pluripotent stem cells Cardiovasc Res 95 2012 419 429
49. I. Itzhaki, L. Maizels, and I. Huber et al. Modelling the long QT syndrome with induced pluripotent stem cells Nature 471 2011 225 229
50. E. Matsa, D. Rajamohan, and E. Dick et al. Drug evaluation in cardiomyocytes derived from human induced pluripotent stem cells carrying a long QT syndrome type 2 mutation Eur Heart J 32 2011 952 962
51. A.L. Lahti, V.J. Kujala, and H. Chapman et al. Model for long QT syndrome type 2 using human iPS cells demonstrates arrhythmogenic characteristics in cell culture Dis Model Mech 5 2012 220 230
52. E. Matsa, J.E. Dixon, and C. Medway et al. Allele-specific RNA interference rescues the long-QT syndrome phenotype in human-induced pluripotency stem cell cardiomyocytes Eur Heart J 35 2014 1078 1087
53. M. Bellin, S. Casini, and R.P. Davis et al. Isogenic human pluripotent stem cell pairs reveal the role of a KCNH2 mutation in long-QT syndrome EMBO J 32 2013 3161 3175
54. C. Terrenoire, K. Wang, and K.W.C. Tung et al. Induced pluripotent stem cells used to reveal drug actions in a long QT syndrome family with complex genetics J Gen Physiol 141 2013 61 72
55. D. Ma, H. Wei, and Y. Zhao et al. Modeling type 3 long QT syndrome with cardiomyocytes derived from patient-specific induced pluripotent stem cells Int J Cardiol 168 2013 5277 5286
56. M. Yazawa, B. Hsueh, and X. Jia et al. Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome Nature 471 2011 230 234
57. C. Kim, J. Wong, and J. Wen et al. Studying arrhythmogenic right ventricular dysplasia with patient-specific iPSCs Nature 494 2013 105 110
58. D. Ma, H. Wei, and J. Lu et al. Generation of patient-specific induced pluripotent stem cell-derived cardiomyocytes as a cellular model of arrhythmogenic right ventricular cardiomyopathy Eur Heart J 34 2013 1122 1133
59. O. Caspi, I. Huber, and A. Gepstein et al. Modeling of arrhythmogenic right ventricular cardiomyopathy with human induced pluripotent stem cells Circ Cardiovasc Genet 6 2013 557 568
60. A. Fatima, G. Xu, and K. Shao et al. In vitro modeling of ryanodine receptor 2 dysfunction using human induced pluripotent stem cells Cell Physiol Biochem 28 2011 579 592
61. C.B. Jung, A. Moretti, and M. Mederos y Schnitzler et al. Dantrolene rescues arrhythmogenic RYR2 defect in a patient-specific stem cell model of catecholaminergic polymorphic ventricular tachycardia EMBO Mol Med 4 2012 180 191
62. X.H. Zhang, S. Haviland, and H. Wei et al. Ca2+ signaling in human induced pluripotent stem cell-derived cardiomyocytes (iPS-CM) from normal and catecholaminergic polymorphic ventricular tachycardia (CPVT)-afflicted subjects Cell Calcium 54 2013 57 70
63. I. Itzhaki, L. Maizels, and I. Huber et al. Modeling of catecholaminergic polymorphic ventricular tachycardia with patient-specific human-induced pluripotent stem cells J Am Coll Cardiol 60 2012 990 1000
64. K. Kujala, J. Paavola, and A. Lahti et al. Cell model of catecholaminergic polymorphic ventricular tachycardia reveals early and delayed afterdepolarizations PLoS One 7 2012 e44660
65. E. Di Pasquale, F. Lodola, and M. Miragoli et al. CaMKII inhibition rectifies arrhythmic phenotype in a patient-specific model of catecholaminergic polymorphic ventricular tachycardia Cell Death Dis 4 2013 e843
66. A. Novak, L. Barad, and N. Zeevi-Levin et al. Cardiomyocytes generated from CPVTD307H patients are arrhythmogenic in response to β-adrenergic stimulation J Cell Mol Med 16 2012 468 482
67. H.-P. Huang, P.-H. Chen, and W.-L. Hwu et al. Human Pompe disease-induced pluripotent stem cells for pathogenesis modeling, drug testing and disease marker identification Hum Mol Genet 20 2011 4851 4864
68. R.R. Shah Can pharmacogenetics help rescue drugs withdrawn from the market? Pharmacogenomics 7 2006 889 908
69. A.E. Lacerda, Y.A. Kuryshev, and Y. Chen et al. Alfuzosin delays cardiac repolarization by a novel mechanism J Pharmacol Exp Ther 324 2008 427 433
70. E.G. Navarrete, P. Liang, and F. Lan et al. Screening drug-induced arrhythmia events using human induced pluripotent stem cell-derived cardiomyocytes and low-impedance microelectrode arrays Circulation 128 2013 S3 S13
71. P. Liang, F. Lan, and A.S. Lee et al. Drug screening using a library of human induced pluripotent stem cell-derived cardiomyocytes reveals disease-specific patterns of cardiotoxicity Circulation 127 2013 1677 1691
72. D.C. Swinney, and J. Anthony How were new medicines discovered? Nat Rev Drug Discov 10 2011 507 519