In vitro uses of human pluripotent stem cell-derived cardiomyocytes

Journal of Cardiovascular Translational Research

Volumn 5, Issue 5, 2012, Pages 581-592

  Matsa, Elena ^a   Denning, Chris ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Cardiomyocytes; Disease modelling; Drug screening; Genetic manipulation; Human pluripotent stem cells; Safety pharmacology; Toxicology

Indexed keywords

BETA ADRENERGIC RECEPTOR BLOCKING AGENT; BIOLOGICAL MARKER;

ARTICLE; AUTOMATION; BRUGADA SYNDROME; CARDIOTOXICITY; CELL MATURATION; CELL REGENERATION; CELL TYPE; DNA REPLICATION; DRUG RESPONSE; DRUG SCREENING; EMBRYONIC STEM CELL; GENETIC MANIPULATION; HEART ARRHYTHMIA; HEART DEVELOPMENT; HEART DISEASE; HEART MUSCLE CELL; HEART VENTRICLE TACHYCARDIA; HUMAN; IN VITRO STUDY; LONG QT SYNDROME; NONHUMAN; PATIENT SAFETY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REGENERATIVE MEDICINE; ROBOTICS; SHORT QT SYNDROME; STEM CELL CULTURE; TREATMENT INDICATION; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL SEPARATION; CULTURE TECHNIQUE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; METABOLISM; MORPHOGENESIS; PATHOLOGY; PHENOTYPE; REVIEW; TOXICITY TESTING;

ANIMALS; BIOLOGICAL MARKERS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; HEART DISEASES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MORPHOGENESIS; MYOCYTES, CARDIAC; PHENOTYPE; TOXICITY TESTS;

EID: 84874180623     PISSN: 19375387     EISSN: 19375395     Source Type: Journal    
DOI: 10.1007/s12265-012-9376-5     Document Type: Article

References (116)

1. Thomson, J. A.; Itskovitz-Eldor, J.; Shapiro, S. S.; Waknitz, M. A.; Swiergiel, J. J.; Marshall, V. S.; et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science, 282(5391), 1145-1147.
2. Reubinoff, B. E.; Pera, M. F.; Fong, C. Y.; Trounson, A.; Bongso, A. (2000). Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nature Biotechnology, 18(4), 399-404. doi: 10.1038/74447.
3. Yu, J.; Vodyanik, M. A.; Smuga-Otto, K.; Antosiewicz-Bourget, J.; Frane, J. L.; Tian, S.; et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science, 318(5858), 1917-1920. doi: 10.1126/science. 1151526.
4. Okita, K.; Ichisaka, T.; Yamanaka, S. (2007). Generation of germline-competent induced pluripotent stem cells. Nature, 448(7151), 313-317. doi: 10.1038/nature05934.
5. Davis, R. P.; van den Berg, C. W.; Casini, S.; Braam, S. R.; Mummery, C. L. (2011). Pluripotent stem cell models of cardiac disease and their implication for drug discovery and development. Trends in Molecular Medicine, 17(9), 475-484. doi: 10.1016/j.molmed.2011.05.001.
6. Pera, M. F.; Reubinoff, B.; Trounson, A. (2000). Human embryonic stem cells. Journal of Cell Science, 113(Pt 1), 5-10.
7. Denning, C.; Allegrucci, C.; Priddle, H.; Barbadillo-Munoz, M. D.; Anderson, D.; Self, T.; et al. (2006). Common culture conditions for maintenance and cardiomyocyte differentiation of the human embryonic stem cell lines, BG01 and HUES-7. International Journal of Developmental Biology, 50(1), 27-37. doi: 10.1387/ijdb.052107cd.
8. Harb, N.; Archer, T. K.; Sato, N. (2008). The Rho-Rock-Myosin signaling axis determines cell-cell integrity of self-renewing pluripotent stem cells. PLoS One, 3(8), e3001. doi: 10.1371/journal.pone.0003001.
9. Mahlstedt, M. M.; Anderson, D.; Sharp, J. S.; McGilvray, R.; Munoz, M. D.; Buttery, L. D.; et al. (2009). Maintenance of pluripotency in human embryonic stem cells cultured on a synthetic substrate in conditioned medium. Biotechnology and Bioengineering, 105(1), 130-140. doi: 10.1002/bit.22520.
10. Desbordes, S. C.; Placantonakis, D. G.; Ciro, A.; Socci, N. D.; Lee, G.; Djaballah, H.; et al. (2008). High-throughput screening assay for the identification of compounds regulating self-renewal and differentiation in human embryonic stem cells. Cell Stem Cell, 2(6), 602-612. doi: 10.1016/j.stem.2008. 05.010.
11. Krawetz, R.; Taiani, J. T.; Liu, S.; Meng, G.; Li, X.; Kallos, M. S.; et al. (2009). Large-scale expansion of pluripotent human embryonic stem cells in stirred-suspension bioreactors. Tissue Engineering. Part C, Methods, 16(4), 573-582. doi: 10.1089/ten.TEC.2009.0228.
12. Li, Y.; Powell, S.; Brunette, E.; Lebkowski, J.; Mandalam, R. (2005). Expansion of human embryonic stem cells in defined serum-free medium devoid of animal-derived products. Biotechnology and Bioengineering, 91(6), 688-698. doi: 10.1002/bit.20536.
13. Ludwig, T. E.; Bergendahl, V.; Levenstein, M. E.; Yu, J.; Probasco, M. D.; Thomson, J. A. (2006). Feeder-independent culture of human embryonic stem cells. Nature Methods, 3(8), 637-646. doi: 10.1038/nmeth902.
14. Wang, L.; Schulz, T. C.; Sherrer, E. S.; Dauphin, D. S.; Shin, S.; Nelson, A. M.; et al. (2007). Self-renewal of human embryonic stem cells requires insulin-like growth factor-1 receptor and ERBB2 receptor signaling. Blood, 110(12), 4111-4119. doi: 10.1182/blood-2007-03-082586.
15. Chen, G.; Gulbranson, D. R.; Hou, Z.; Bolin, J. M.; Ruotti, V.; Probasco, M. D.; et al. (2011). Chemically defined conditions for human iPSC derivation and culture. Nature Methods, 8(5), 424-429. doi: 10.1038/nmeth.1593.
16. Thomas, R. J.; Anderson, D.; Chandra, A.; Smith, N. M.; Young, L. E.; Williams, D.; et al. (2009). Automated, scalable culture of human embryonic stem cells in feeder-free conditions. Biotechnology and Bioengineering, 102(6), 1636-1644. doi: 10.1002/bit.22187.
17. Moore, J. C.; van Laake, L. W.; Braam, S. R.; Xue, T.; Tsang, S. Y.; Ward, D.; et al. (2005). Human embryonic stem cells: Genetic manipulation on the way to cardiac cell therapies. Reproductive Toxicology, 20(3), 377-391. doi: 10.1016/j.reprotox.2005.04.012.
18. Gropp, M.; Itsykson, P.; Singer, O.; Ben-Hur, T.; Reinhartz, E.; Galun, E.; et al. (2003). Stable genetic modification of human embryonic stem cells by lentiviral vectors. Molecular Therapy, 7(2), 281-287.
19. Vallier, L.; Rugg-Gunn, P. J.; Bouhon, I. A.; Andersson, F. K.; Sadler, A. J.; Pedersen, R. A. (2004). Enhancing and diminishing gene function in human embryonic stem cells. Stem Cells, 22(1), 2-11. doi: 10.1634/stemcells.22-1-2.
20. Liu, Y. P.; Dovzhenko, O. V.; Garthwaite, M. A.; Dambaeva, S. V.; Durning, M.; Pollastrini, L. M.; et al. (2004). Maintenance of pluripotency in human embryonic stem cells stably over-expressing enhanced green fluorescent protein. Stem Cells and Development, 13(6), 636-645. doi: 10.1089/scd.2004.13. 636.
21. Eiges, R.; Schuldiner, M.; Drukker, M.; Yanuka, O.; Itskovitz-Eldor, J.; Benvenisty, N. (2001). Establishment of human embryonic stem cell-transfected clones carrying a marker for undifferentiated cells. Current Biology, 11(7), 514-518.
22. Gerrard, L.; Zhao, D.; Clark, A. J.; Cui, W. (2005). Stably transfected human embryonic stem cell clones express OCT4-specific green fluorescent protein and maintain self-renewal and pluripotency. Stem Cells, 23(1), 124-133. doi: 10.1634/stemcells.2004-0102.
23. Braam, S. R.; Denning, C.; Matsa, E.; Young, L. E.; Passier, R.; Mummery, C. L. (2008). Feeder-free culture of human embryonic stem cells in conditioned medium for efficient genetic modification. Nature Protocols, 3(9), 1435-1443. doi: 10.1038/nprot.2008.140.
24. Chang, T.; Zheng, W.; Tsark, W.; Bates, S.; Huang, H.; Lin, R. J.; et al. (2011). Brief report: Phenotypic rescue of induced pluripotent stem cell-derived motoneurons of a spinal muscular atrophy patient. Stem Cells, 29(12), 2090-2093. doi: 10.1002/stem.749.
25. Hay, D. C.; Sutherland, L.; Clark, J.; Burdon, T. (2004). Oct-4 knockdown induces similar patterns of endoderm and trophoblast differentiation markers in human and mouse embryonic stem cells. Stem Cells, 22(2), 225-235. doi: 10.1634/stemcells.22-2-225.
26. Liu, G. H.; Barkho, B. Z.; Ruiz, S.; Diep, D.; Qu, J.; Yang, S. L.; et al. (2011). Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome. Nature, 472(7342), 221-225. doi: 10.1038/nature09879.
27. Costa, M.; Dottori, M.; Sourris, K.; Jamshidi, P.; Hatzistavrou, T.; Davis, R.; et al. (2007). A method for genetic modification of human embryonic stem cells using electroporation. Nature Protocols, 2(4), 792-796. doi: 10.1038/nprot.2007.105.
28. Hockemeyer, D.; Wang, H.; Kiani, S.; Lai, C. S.; Gao, Q.; Cassady, J. P.; et al. (2011). Genetic engineering of human pluripotent cells using TALE nucleases. Nature Biotechnology, 29(8), 731-734. doi: 10.1038/nbt.1927.
29. Zwaka, T. P.; Thomson, J. A. (2003). Homologous recombination in human embryonic stem cells. Nature Biotechnology, 21(3), 319-321. doi: 10.1038/nbt788.
30. Elliott, D. A.; Braam, S. R.; Koutsis, K.; Ng, E. S.; Jenny, R.; Lagerqvist, E. L.; et al. (2011). NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nature Methods, 8(12), 1037-1040. doi: 10.1038/nmeth.1740.
31. Davis RP, Grandela C, Sourris K, Hatzistavrou T, Dottori M, Elefanty AG, Stanley EG, Costa M (2009) Generation of human embryonic stem cell reporter knock-in lines by homologous recombination. Curr Protoc Stem Cell Biol Chapter 5:Unit 5B 1 1 1-34. doi: 10.1002/9780470151808.sc05b01s11
32. Nieminen, M.; Tuuri, T.; Savilahti, H. (2010). Genetic recombination pathways and their application for genome modification of human embryonic stem cells. Experimental Cell Research, 316(16), 2578-2586. doi: 10.1016/j.yexcr. 2010.06.004.
33. Tolar, J.; Xia, L.; Riddle, M. J.; Lees, C. J.; Eide, C. R.; McElmurry, R. T.; et al. (2011). Induced pluripotent stem cells from individuals with recessive dystrophic epidermolysis bullosa. The Journal of Investigative Dermatology, 131(4), 848-856. doi: 10.1038/jid.2010.346.
34. Sebastiano, V.; Maeder, M. L.; Angstman, J. F.; Haddad, B.; Khayter, C.; Yeo, D. T.; et al. (2011). In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases. Stem Cells, 29(11), 1717-1726. doi: 10.1002/stem.718.
35. Wang, Y.; Zheng, C. G.; Jiang, Y.; Zhang, J.; Chen, J.; Yao, C.; et al. (2012). Genetic correction of beta-thalassemia patient-specific iPS cells and its use in improving hemoglobin production in irradiated SCID mice. Cell Research. doi: 10.1038/cr.2012.23.
36. Narsinh, K.; Narsinh, K. H.; Wu, J. C. (2011). Derivation of human induced pluripotent stem cells for cardiovascular disease modeling. Circulation Research, 108(9), 1146-1156. doi: 10.1161/CIRCRESAHA.111.240374.
37. Warren, L.; Manos, P. D.; Ahfeldt, T.; Loh, Y. H.; Li, H.; Lau, F.; et al. (2010). Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell, 7(5), 618-630. doi: 10.1016/j.stem.2010.08.012.
38. Onder, T. T.; Kara, N.; Cherry, A.; Sinha, A. U.; Zhu, N.; Bernt, K. M.; et al. (2012). Chromatin-modifying enzymes as modulators of reprogramming. Nature. doi: 10.1038/nature10953.
39. Hanna, J.; Markoulaki, S.; Schorderet, P.; Carey, B. W.; Beard, C.; Wernig, M.; et al. (2008). Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell, 133(2), 250-264. doi: 10.1016/j.cell.2008.03.028.
40. Aoi, T.; Yae, K.; Nakagawa, M.; Ichisaka, T.; Okita, K.; Takahashi, K.; Chiba, T.; Yamanaka, S. (2008). Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science, 321(5889), 699-702. doi: 10.1126/science.1154884
41. Haase, A.; Olmer, R.; Schwanke, K.; Wunderlich, S.; Merkert, S.; Hess, C.; et al. (2009). Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell, 5(4), 434-441. doi: 10.1016/j.stem.2009.08.021.
42. Ghosh, Z.; Wilson, K. D.; Wu, Y.; Hu, S.; Quertermous, T.; Wu, J. C. (2010). Persistent donor cell gene expression among human induced pluripotent stem cells contributes to differences with human embryonic stem cells. PLoS One, 5(2), e8975. doi: 10.1371/journal.pone.0008975.
43. Burridge, P. W.; Anderson, D.; Priddle, H.; Barbadillo Munoz, M. D.; Chamberlain, S.; Allegrucci, C.; et al. (2007). Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability. Stem Cells, 25(4), 929-938. doi: 10.1634/stemcells.2006-0598.
44. Burridge, P. W.; Keller, G.; Gold, J. D.; Wu, J. C. (2012). Production of de novo cardiomyocytes: Human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell, 10(1), 16-28. doi: 10.1016/j.stem.2011.12.013.
45. Mummery, C.; Ward-van Oostwaard, D.; Doevendans, P.; Spijker, R.; van den Brink, S.; Hassink, R.; et al. (2003). Differentiation of human embryonic stem cells to cardiomyocytes: Role of coculture with visceral endoderm-like cells. Circulation, 107(21), 2733-2740. doi: 10.1161/01.CIR.0000068356.38592.68.
46. Burridge, P. W.; Thompson, S.; Millrod, M. A.; Weinberg, S.; Yuan, X.; Peters, A.; et al. (2011). A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS One, 6(4), e18293. doi: 10.1371/journal.pone. 0018293.
47. Kattman, S. J.; Witty, A. D.; Gagliardi, M.; Dubois, N. C.; Niapour, M.; Hotta, A.; et al. (2011). Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell, 8(2), 228-240. doi: 10.1016/j.stem.2010.12.008.
48. Yu, P.; Pan, G.; Yu, J.; Thomson, J. A. (2011). FGF2 sustains NANOG and switches the outcome of BMP4-induced human embryonic stem cell differentiation. Cell Stem Cell, 8(3), 326-334. doi: 10.1016/j.stem.2011.01.001.
49. Paige, S. L.; Osugi, T.; Afanasiev, O. K.; Pabon, L.; Reinecke, H.; Murry, C. E. (2010). Endogenous Wnt/beta-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One, 5(6), e11134. doi: 10.1371/journal.pone. 0011134.
50. Martinez-Fernandez, A.; Nelson, T. J.; Ikeda, Y.; Terzic, A. (2010). c-MYC independent nuclear reprogramming favors cardiogenic potential of induced pluripotent stem cells. Journal of Cardiovascular Translational Research, 3(1), 13-23. doi: 10.1007/s12265-009-9150-5.
51. Anderson, D.; Self, T.; Mellor, I. R.; Goh, G.; Hill, S. J.; Denning, C. (2007). Transgenic enrichment of cardiomyocytes from human embryonic stem cells. Molecular Therapy, 15(11), 2027-2036. doi: 10.1038/sj.mt.6300303.
52. Huber, I.; Itzhaki, I.; Caspi, O.; Arbel, G.; Tzukerman, M.; Gepstein, A.; et al. (2007). Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. The FASEB Journal, 21(10), 2551-2563. doi: 10.1096/fj.05-5711com.
53. Dubois, N. C.; Craft, A. M.; Sharma, P.; Elliott, D. A.; Stanley, E. G.; Elefanty, A. G.; et al. (2011). SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nature Biotechnology, 29(11), 1011-1018. doi: 10.1038/nbt.2005.
54. Van Hoof, D.; Dormeyer, W.; Braam, S. R.; Passier, R.; Monshouwer-Kloots, J.; Ward-van Oostwaard, D.; et al. (2010). Identification of cell surface proteins for antibody-based selection of human embryonic stem cell-derived cardiomyocytes. Journal of Proteome Research, 9(3), 1610-1618. doi: 10.1021/pr901138a.
55. Chan, J. W.; Lieu, D. K.; Huser, T.; Li, R. A. (2009). Label-free separation of human embryonic stem cells and their cardiac derivatives using Raman spectroscopy. Analytical Chemistry, 81(4), 1324-1331. doi: 10.1021/ac801665m.
56. Pascut, F. C.; Goh, H. T.; George, V.; Denning, C.; Notingher, I. (2011). Toward label-free Raman-activated cell sorting of cardiomyocytes derived from human embryonic stem cells. Journal of Biomedical Optics, 16(4), 045002. doi: 10.1117/1.3570302.
57. Zhang, J.; Wilson, G. F.; Soerens, A. G.; Koonce, C. H.; Yu, J.; Palecek, S. P.; et al. (2009). Functional cardiomyocytes derived from human induced pluripotent stem cells. Circulation Research, 104(4), e30-e41. doi: 10.1161/CIRCRESAHA.108.192237.
58. Fu, J.-D.; H-f, T.; Siu, C.-W.; Moore, J. C.; Lieu, D. K.; Liao, S.-Y.; et al. (2008). Driven maturation of embryonic stem cell-derived cardiomyocytes confers post-transplantation safety. Cell Research, 18(S1), S132.
59. Otsuji, T. G.; Minami, I.; Kurose, Y.; Yamauchi, K.; Tada, M.; Nakatsuji, N. (2010). Progressive maturation in contracting cardiomyocytes derived from human embryonic stem cells: Qualitative effects on electrophysiological responses to drugs. Stem Cell Research, 4(3), 201-213. doi: 10.1016/j.scr.2010. 01.002.
60. Rajala, K.; Pekkanen-Mattila, M.; Aalto-Setala, K. (2011). Cardiac differentiation of pluripotent stem cells. Stem Cells International, 2011, 383709. doi: 10.4061/2011/383709.
61. Beqqali, A.; Kloots, J.; Ward-van Oostwaard, D.; Mummery, C.; Passier, R. (2006). Genome-wide transcriptional profiling of human embryonic stem cells differentiating to cardiomyocytes. Stem Cells, 24(8), 1956-1967. doi: 10.1634/stemcells.2006-0054.
62. Bu, L.; Jiang, X.; Martin-Puig, S.; Caron, L.; Zhu, S.; Shao, Y.; et al. (2009). Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature, 460(7251), 113-117. doi: 10.1038/nature08191.
63. Xu, H.; Yi, B. A.; Chien, K. R. (2011). Shortcuts to making cardiomyocytes. Nature Cell Biology, 13(3), 191-193. doi: 10.1038/ncb0311-191.
64. Hudson, J. E.; Zimmermann, W. H. (2011). Tuning Wnt-signaling to enhance cardiomyogenesis in human embryonic and induced pluripotent stem cells. Journal of Molecular and Cellular Cardiology, 51(3), 277-279. doi: 10.1016/j.yjmcc.2011. 06.011.
65. Dickson, M.; Gagnon, J. P. (2004). Key factors in the rising cost of new drug discovery and development. Nature Reviews. Drug Discovery, 3(5), 417-429.
66. Terrar, D. A.; Wilson, C. M.; Graham, S. G.; Bryant, S. M.; Heath, B. M. (2007). Comparison of guinea-pig ventricular myocytes and dog Purkinje fibres for in vitro assessment of drug-induced delayed repolarization. Journal of Pharmacological and Toxicological Methods, 56(2), 171-185. doi: 10.1016/j.vascn.2007.04.005.
67. Pouton, C. W.; Haynes, J. M. (2007). Embryonic stem cells as a source of models for drug discovery. Nature Reviews. Drug Discovery, 6(8), 605-616. doi: 10.1038/nrd2194.
68. Fermini, B.; Fossa, A. A. (2003). The impact of drug-induced QT interval prolongation on drug discovery and development. Nature Reviews. Drug Discovery, 2(6), 439-447. doi: 10.1038/nrd1108.
69. Dick, E.; Rajamohan, D.; Ronksley, J.; Denning, C. (2010). Evaluating the utility of cardiomyocytes from human pluripotent stem cells for drug screening. Biochemical Society Transactions, 38(4), 1037-1045. doi: 10.1042/BST0381037.
70. Ma, J.; Guo, L.; Fiene, S. J.; Anson, B. D.; Thomson, J. A.; Kamp, T. J.; et al. (2011). High purity human-induced pluripotent stem cell-derived cardiomyocytes: Electrophysiological properties of action potentials and ionic currents. American Journal of Physiology - Heart and Circulatory Physiology, 301(5), H2006-H2017. doi: 10.1152/ajpheart.00694.2011.
71. Mehta, A.; Chung, Y. Y.; Ng, A.; Iskandar, F.; Atan, S.; Wei, H.; et al. (2011). Pharmacological response of human cardiomyocytes derived from virus-free induced pluripotent stem cells. Cardiovascular Research, 91(4), 577-586. doi: 10.1093/cvr/cvr132.
72. Yokoo, N.; Baba, S.; Kaichi, S.; Niwa, A.; Mima, T.; Doi, H.; et al. (2009). The effects of cardioactive drugs on cardiomyocytes derived from human induced pluripotent stem cells. Biochemical and Biophysical Research Communications, 387(3), 482-488. doi: 10.1016/j.bbrc.2009.07.052.
73. Braam, S. R.; Tertoolen, L.; van de Stolpe, A.; Meyer, T.; Passier, R.; Mummery, C. L. (2010). Prediction of drug-induced cardiotoxicity using human embryonic stem cell-derived cardiomyocytes. Stem Cell Research, 4(2), 107-116. doi: 10.1016/j.scr.2009.11.004.
74. Mummery, C. L.; Davis, R. P.; Krieger, J. E. (2010). Challenges in using stem cells for cardiac repair. Science Translational Medicine, 2(27), 27ps17. doi: 10.1126/scitranslmed.3000558.
75. Foldes, G.; Mioulane, M.; Wright, J. S.; Liu, A. Q.; Novak, P.; Merkely, B.; et al. (2011). Modulation of human embryonic stem cell-derived cardiomyocyte growth: A testbed for studying human cardiac hypertrophy? Journal of Molecular and Cellular Cardiology, 50(2), 367-376. doi: 10.1016/j.yjmcc.2010.10.029.
76. Tropel, P.; Tournois, J.; Come, J.; Varela, C.; Moutou, C.; Fragner, P.; et al. (2010). High-efficiency derivation of human embryonic stem cell lines following pre-implantation genetic diagnosis. In Vitro Cellular & Developmental Biology - Animal, 46(3-4), 376-385. doi: 10.1007/s11626-010-9300- 8.
77. Verlinsky, Y.; Strelchenko, N.; Kukharenko, V.; Rechitsky, S.; Verlinsky, O.; Galat, V.; et al. (2005). Human embryonic stem cell lines with genetic disorders. Reproductive Biomedicine Online, 10(1), 105-110.
78. Puri, M. C.; Nagy, A. (2012). Concise review: Embryonic stem cells versus induced pluripotent stem cells: The game is on. Stem Cells, 30(1), 10-14. doi: 10.1002/stem.788.
79. Wu, S. M.; Hochedlinger, K. (2011). Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nature Cell Biology, 13(5), 497-505.
80. Park, I. H.; Arora, N.; Huo, H.; Maherali, N.; Ahfeldt, T.; Shimamura, A.; Lensch, M. W.; Cowan, C.; Hochedlinger, K.; Daley, G. Q. (2008). Disease-specific induced pluripotent stem cells. Cell, 134(5), 877-886. doi: 10.1016/j.cell.2008.07.041
81. Matsa, E.; Rajamohan, D.; Dick, E.; Young, L.; Mellor, I.; Staniforth, A.; et al. (2011). Drug evaluation in cardiomyocytes derived from human induced pluripotent stem cells carrying a long QT syndrome type 2 mutation. European Heart Journal, 32(8), 952-962. doi: 10.1093/eurheartj/ehr073.
82. Kazuki, Y.; Hiratsuka, M.; Takiguchi, M.; Osaki, M.; Kajitani, N.; Hoshiya, H.; et al. (2010). Complete genetic correction of ips cells from Duchenne muscular dystrophy. Molecular Therapy, 18(2), 386-393. doi: 10.1038/mt.2009.274.
83. Bokil, N. J.; Baisden, J. M.; Radford, D. J.; Summers, K. M. (2010). Molecular genetics of long QT syndrome. Molecular Genetics and Metabolism, 101(1), 1-8. doi: 10.1016/j.ymgme.2010.05.011.
84. Hofman, N.; van Lochem, L. T.; Wilde, A. A. (2010). Genetic basis of malignant channelopathies and ventricular fibrillation in the structurally normal heart. Future Cardiology, 6(3), 395-408. doi: 10.2217/fca.10.11.
85. Moretti, A.; Bellin, M.; Welling, A.; Jung, C. B.; Lam, J. T.; Bott-Flugel, L.; et al. (2010). Patient-specific induced pluripotent stem-cell models for long-QT syndrome. The New England Journal of Medicine, 363(15), 1397-1409. doi: 10.1056/NEJMoa0908679.
86. Robinton, D. A.; Daley, G. Q. (2012). The promise of induced pluripotent stem cells in research and therapy. Nature, 481(7381), 295-305. doi: 10.1038/nature10761.
87. Woodcock, J. (2007). The prospects for «personalized medicine» in drug development and drug therapy. Clinical Pharmacology and Therapeutics, 81(2), 164-169. doi: 10.1038/sj.clpt.6100063.
88. Han, Y.; Miller, A.; Mangada, J.; Liu, Y.; Swistowski, A.; Zhan, M.; et al. (2009). Identification by automated screening of a small molecule that selectively eliminates neural stem cells derived from hESCs but not dopamine neurons. PLoS One, 4(9), e7155. doi: 10.1371/journal.pone.0007155.
89. Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; et al. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131(5), 861-872.
90. Dimos, J. T.; Rodolfa, K. T.; Niakan, K. K.; Weisenthal, L. M.; Mitsumoto, H.; Chung, W.; et al. (2008). Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science, 321(5893), 1218-1221. doi: 10.1126/science.1158799.
91. Huangfu, D.; Osafune, K.; Maehr, R.; Guo, W.; Eijkelenboom, A.; Chen, S.; et al. (2008). Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nature Biotechnology, 26(11), 1269-1275.
92. Nakagawa, M.; Koyanagi, M.; Tanabe, K.; Takahashi, K.; Ichisaka, T.; Aoi, T.; et al. (2008). Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nature Biotechnology, 26(1), 101-106.
93. Hester, M. E.; Song, S.; Miranda, C. J.; Eagle, A.; Schwartz, P. H.; Kaspar, B. K. (2009). Two factor reprogramming of human neural stem cells into pluripotency. PLoS One, 4(9), e7044. doi: 10.1371/journal.pone.0007044.
94. Kim, J. B.; Greber, B.; Arauzo-Bravo, M. J.; Meyer, J.; Park, K. I.; Zaehres, H.; et al. (2009). Direct reprogramming of human neural stem cells by OCT4. Nature, 461(7264), 643-649. doi: 10.1038/nature08436.
95. Ebert, A. D.; Yu, J.; Rose, F. F.; Mattis, V. B.; Lorson, C. L.; Thomson, J. A.; et al. (2009). Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature, 457(7227), 277-280.
96. Carey, B. W.; Markoulaki, S.; Hanna, J.; Saha, K.; Gao, Q.; Mitalipova, M.; et al. (2009). Reprogramming of murine and human somatic cells using a single polycistronic vector. Proceedings of the National Academy of Sciences of the United States of America, 106(1), 157-162. doi: 10.1073/pnas.0811426106.
97. Soldner, F.; Hockemeyer, D.; Beard, C.; Gao, Q.; Bell, G. W.; Cook, E. G.; et al. (2009). Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell, 136(5), 964-977. doi: 10.1016/j.cell.2009.02.013.
98. Kaji, K.; Norrby, K.; Paca, A.; Mileikovsky, M.; Mohseni, P.; Woltjen, K. (2009). Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature, 458(7239), 771-775. doi: 10.1038/nature07864.
99. Zhou, W.; Freed, C. R. (2009). Adenoviral gene delivery can reprogram human fibroblasts to induced pluripotent stem cells. Stem Cells, 27(11), 2667-2674. doi: 10.1002/stem.201.
100. Si-Tayeb, K.; Noto, F. K.; Sepac, A.; Sedlic, F.; Bosnjak, Z. J.; Lough, J. W.; et al. (2010). Generation of human induced pluripotent stem cells by simple transient transfection of plasmid DNA encoding reprogramming factors. BMC Developmental Biology, 10, 81. doi: 10.1186/1471-213X-10-81.
101. Jia, F.; Wilson, K. D.; Sun, N.; Gupta, D. M.; Huang, M.; Li, Z.; et al. (2010). A nonviral minicircle vector for deriving human iPS cells. Nature Methods, 7(3), 197-199. doi: 10.1038/nmeth.1426.
102. Yu, J.; Hu, K.; Smuga-Otto, K.; Tian, S.; Stewart, R.; Slukvin, I. I.; et al. (2009). Human induced pluripotent stem cells free of vector and transgene sequences. Science, 324(5928), 797-801. doi: 10.1126/science.1172482.
103. Kim, D.; Kim, C.-H.; Moon, J.-I.; Chung, Y.-G.; Chang, M.-Y.; Han, B.-S.; et al. (2009). Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell, 4(6), 472-476.
104. Zhou, H.; Wu, S.; Joo, J. Y.; Zhu, S.; Han, D. W.; Lin, T.; et al. (2009). Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell, 4(5), 381-384. doi: 10.1016/j.stem.2009.04.005.
105. Fusaki, N.; Ban, H.; Nishiyama, A.; Saeki, K.; Hasegawa, M. (2009). Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proceedings of the Japan Academy. Series B, Physical and Biological Sciences, 85(8), 348-362. doi: JST.JSTAGE/pjab/85.348.
106. Miyoshi, N.; Ishii, H.; Nagano, H.; Haraguchi, N.; Dewi, D. L.; Kano, Y.; et al. (2011). Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell, 8(6), 633-638. doi: 10.1016/j.stem.2011.05. 001.
107. Tanaka, T.; Tohyama, S.; Murata, M.; Nomura, F.; Kaneko, T.; Chen, H.; et al. (2009). In vitro pharmacologic testing using human induced pluripotent stem cell-derived cardiomyocytes. Biochemical and Biophysical Research Communications, 385(4), 497-502. doi: 10.1016/j.bbrc.2009.05.073.
108. Zwi, L.; Caspi, O.; Arbel, G.; Huber, I.; Gepstein, A.; Park, I. H.; et al. (2009). Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation, 120(15), 1513-1523. doi: 10.1161/CIRCULATIONAHA.109.868885.
109. Dick, E.; Matsa, E.; Bispham, J.; Reza, M.; Guglieri, M.; Staniforth, A.; et al. (2011). Two new protocols to enhance the production and isolation of human induced pluripotent stem cell lines. Stem Cell Research, 6(2), 158-167. doi: 10.1016/j.scr.2010.10.002.
110. Carvajal-Vergara, X.; Sevilla, A.; D'Souza, S. L.; Ang, Y. S.; Schaniel, C.; Lee, D. F.; et al. (2010). Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature, 465(7299), 808-812. doi: 10.1038/nature09005.
111. Itzhaki, I.; Maizels, L.; Huber, I.; Zwi-Dantsis, L.; Caspi, O.; Winterstern, A.; et al. (2011). Modelling the long QT syndrome with induced pluripotent stem cells. Nature, 471(7337), 225-229.
112. Lahti, A. L.; Kujala, V. J.; Chapman, H.; Koivisto, A. P.; Pekkanen-Mattila, M.; Kerkela, E.; et al. (2011). Human disease model for long QT syndrome type 2 using iPS cells demonstrates arrhythmogenic characteristics in cell culture. Disease Models & Mechanisms. doi: 10.1242/dmm.008409.
113. Fatima, A.; Xu, G.; Shao, K.; Papadopoulos, S.; Lehmann, M.; Arnaiz-Cot, J. J.; et al. (2011). In vitro modeling of ryanodine receptor 2 dysfunction using human induced pluripotent stem cells. Cellular Physiology and Biochemistry, 28(4), 579-592. doi: 10.1159/000335753.
114. Jung, C. B.; Moretti, A.; Schnitzler, M. M.; Iop, L.; Storch, U.; Bellin, M.; et al. (2011). Dantrolene rescues arrhythmogenic RYR2 defect in a patient-specific stem cell model of catecholaminergic polymorphic ventricular tachycardia. EMBO Molecular Medicine. doi: 10.1002/emmm.201100194.
115. Yazawa, M.; Hsueh, B.; Jia, X.; Pasca, A. M.; Bernstein, J. A.; Hallmayer, J.; et al. (2011). Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome. Nature. doi: 10.1038/nature09855.
116. Pasca, S. P.; Portmann, T.; Voineagu, I.; Yazawa, M.; Shcheglovitov, A.; Pasca, A. M.; et al. (2011). Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome. Nature Medicine, 17(12), 1657-1662. doi: 10.1038/nm.2576.