Two dimensional electrophysiological characterization of human pluripotent stem cell-derived cardiomyocyte system

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Zhu, Huanqi ^a   Scharnhorst, Kelsey S ^a   Stieg, Adam Z ^a,b   Gimzewski, James K ^a,b,c   Minami, Itsunari ^d   Nakatsuji, Norio ^d,e   Nakano, Haruko ^a   Nakano, Atsushi ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d KYOTO UNIVERSITY   (Japan)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIAC MUSCLE CELL; CELL CULTURE TECHNIQUE; CELL DIFFERENTIATION; ELECTROPHYSIOLOGY; HUMAN; PHYSIOLOGY; PLURIPOTENT STEM CELL;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; ELECTROPHYSIOLOGICAL PHENOMENA; HUMANS; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS;

EID: 85014782613     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep43210     Document Type: Article

References (47)

1. Thomson, J. A., et al. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147 (1998).
2. Suemori, H., et al. Efficient establishment of human embryonic stem cell lines and long-term maintenance with stable karyotype by enzymatic bulk passage. Biochem Biophys Res Commun 345, 926-932 (2006).
3. Takahashi, K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (2007).
4. Yu, J., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920 (2007).
5. Hescheler, J., et al. Determination of electrical properties of ES cell-derived cardiomyocytes using MEAs. J Electrocardiol 37 Suppl, 110-116 (2004).
6. Himmel, H. M. Drug-induced functional cardiotoxicity screening in stem cell-derived human and mouse cardiomyocytes: effects of reference compounds. J Pharmacol Toxicol Methods 68, 97-111 (2013).
7. Clements, M., Thomas, N. High-throughput multi-parameter profiling of electrophysiological drug effects in human embryonic stem cell derived cardiomyocytes using multi-electrode arrays. Toxicol Sci 140, 445-461 (2014).
8. Mummery, C., et al. Cardiomyocyte differentiation of mouse and human embryonic stem cells. J Anat 200, 233-242 (2002).
9. Laflamme, M. A., et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25, 1015-1024 (2007).
10. Kattman, S. J., 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, 228-240 (2011).
11. Willems, E., et al. Small-molecule inhibitors of the Wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm. Circ Res 109, 360-364 (2011).
12. Minami, I., et al. A small molecule that promotes cardiac differentiation of human pluripotent stem cells under defined, cytokineand xeno-free conditions. Cell Rep 2, 1448-1460 (2012).
13. Arshi, A., et al. Rigid microenvironments promote cardiac differentiation of mouse and human embryonic stem cells. Sci Technol Adv Mater 14, doi: 10. 1088/1468-6996/14/2/025003 (2013).
14. Tulloch, N. L., et al. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res 109, 47-59 (2011).
15. Lieu, D. K., et al. Mechanism-based facilitated maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Arrhythm Electrophysiol 6, 191-201 (2013).
16. Zhang, D., et al. Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 34, 5813-5820 (2013).
17. Nunes, S. S., et al. Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat Methods 10, 781-787 (2013).
18. Snir, M., et al. Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. Am J Physiol Heart Circ Physiol 285, H2355-2363 (2003).
19. McDevitt, T. C., Laflamme, M. A., Murry, C. E. Proliferation of cardiomyocytes derived from human embryonic stem cells is mediated via the IGF/PI 3-kinase/Akt signaling pathway. J Mol Cell Cardiol 39, 865-873 (2005).
20. Caspi, O., et al. Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 100, 263-272 (2007).
21. Dolnikov, K., et al. Functional properties of human embryonic stem cell-derived cardiomyocytes: intracellular Ca2+ handling and the role of sarcoplasmic reticulum in the contraction. Stem Cells 24, 236-245 (2006).
22. Liu, J., Fu, J. D., Siu, C. W., Li, R. A. Functional sarcoplasmic reticulum for calcium handling of human embryonic stem cellderived cardiomyocytes: insights for driven maturation. Stem Cells 25, 3038-3044 (2007).
23. Satin, J., et al. Calcium handling in human embryonic stem cell-derived cardiomyocytes. Stem Cells 26, 1961-1972 (2008).
24. Doss, M. X., et al. Maximum diastolic potential of human induced pluripotent stem cell-derived cardiomyocytes depends critically on I(Kr). PLoS One 7, e40288 (2012).
25. Feinberg, A. W., et al. Functional Differences in Engineered Myocardium from Embryonic Stem Cell-Derived versus Neonatal Cardiomyocytes. Stem cell reports 1, 387-396 (2013).
26. Lu, T. Y., et al. Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells. Nat Commun 4, 2307 (2013).
27. Hazeltine, L. B., et al. Effects of substrate mechanics on contractility of cardiomyocytes generated from human pluripotent stem cells. Int J Cell Biol 2012, 508294 (2012).
28. Nakashima, Y., et al. Nkx2-5 suppresses the proliferation of atrial myocytes and conduction system. Circ Res 114, 1103-1113 (2014).
29. Sartiani, L., et al. Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: a molecular and electrophysiological approach. Stem Cells 25, 1136-1144 (2007).
30. Lundy, S. D., Zhu, W. Z., Regnier, M., Laflamme, M. A. Structural and Functional Maturation of Cardiomyocytes Derived from Human Pluripotent Stem Cells. Stem Cells Dev 22, 1991-2002 (2013).
31. Robertson, C., Tran, D. D., George, S. C. Concise review: maturation phases of human pluripotent stem cell-derived cardiomyocytes. Stem Cells 31, 829-837 (2013).
32. Yang, X., Pabon, L., Murry, C. E. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res 114, 511-523 (2014).
33. Engler, A. J., et al. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J Cell Sci 121, 3794-3802 (2008).
34. Bajaj, P., Tang, X., Saif, T. A., Bashir, R. Stiffness of the substrate influences the phenotype of embryonic chicken cardiac myocytes. J Biomed Mater Res A 95, 1261-1269 (2010).
35. Forte, G., et al. Substrate Stiffness Modulates Gene Expression and Phenotype in Neonatal Cardiomyocytes In Vitro. Tissue Eng Part A 18, 1837-1848 (2012).
36. Guo, L., et al. Estimating the risk of drug-induced proarrhythmia using human induced pluripotent stem cell-derived cardiomyocytes. Toxicol Sci 123, 281-289 (2011).
37. Asai, Y., Tada, M., Otsuji, T. G., Nakatsuji, N. Combination of functional cardiomyocytes derived from human stem cells and a highly-efficient microelectrode array system: an ideal hybrid model assay for drug development. Curr Stem Cell Res Ther 5, 227-232 (2010).
38. Caspi, O., et al. In vitro electrophysiological drug testing using human embryonic stem cell derived cardiomyocytes. Stem Cells Dev 18, 161-172 (2009).
39. Egashira, T., et al. Disease characterization using LQTS-specific induced pluripotent stem cells. Cardiovasc Res 95, 419-429 (2012).
40. Harding, S. E., Ali, N. N., Brito-Martins, M., Gorelik, J. The human embryonic stem cell-derived cardiomyocyte as a pharmacological model. Pharmacol Ther 113, 341-353 (2007).
41. van den Heuvel, N. H., van Veen, T. A., Lim, B., Jonsson, M. K. Lessons from the heart: Mirroring electrophysiological characteristics during cardiac development to in vitro differentiation of stem cell derived cardiomyocytes. J Mol Cell Cardiol 67C, 12-25 (2013).
42. Kujala, V. J., et al. Averaging in vitro cardiac field potential recordings obtained with microelectrode arrays. Comput Methods Programs Biomed 104, 199-205 (2011).
43. Navarrete, E. G., et al. Screening drug-induced arrhythmia [corrected] using human induced pluripotent stem cell-derived cardiomyocytes and low-impedance microelectrode arrays. Circulation 128, S3-13 (2013).
44. Otsuji, T. G., et al. Progressive maturation in contracting cardiomyocytes derived from human embryonic stem cells: Qualitative effects on electrophysiological responses to drugs. Stem Cell Res 4, 201-213 (2010).
45. Kim, C., et al. Non-cardiomyocytes influence the electrophysiological maturation of human embryonic stem cell-derived cardiomyocytes during differentiation. Stem Cells Dev 19, 783-795 (2010).
46. Ma, J., et al. High purity human-induced pluripotent stem cell-derived cardiomyocytes: electrophysiological properties of action potentials and ionic currents. Am J Physiol Heart Circ Physiol 301, H2006-2017 (2011).
47. Bedut, S., et al. High-throughput drug profiling with voltage-and calcium-sensitive fluorescent probes in human iPSC-derived cardiomyocytes. Am J Physiol Heart Circ Physiol 311, H44-53 (2016).