Electrical stimulation promotes maturation of cardiomyocytes derived from human embryonic stem cells

Journal of Cardiovascular Translational Research

Volumn 6, Issue 6, 2013, Pages 989-999

  Chan, Yau Chi ^a   Ting, Sherwin ^b   Lee, Yee Ki ^a   Ng, Kwong Man ^a   Zhang, Jiao ^a   Chen, Zi ^a   Siu, Chung Wah ^a   Oh, Steve K W ^b   Tse, Hung Fat ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b AGENCY FOR SCIENCE   (Singapore)

Author keywords

Cardiomyocytes; Electrical stimulation; Human embryonic stem cells

Indexed keywords

CAFFEINE; CALCIUM; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; TROPONIN T;

ACTION POTENTIAL; ARTICLE; CALCIUM TRANSPORT; CANCER CELL CULTURE; CELL CULTURE; CELL DIFFERENTIATION; CELL ELONGATION; CELL FUNCTION; CELL MATURATION; CELL VIABILITY; CONTROLLED STUDY; ELECTRIC FIELD; ELECTRICAL EVOKED RESPONSE STIMULATOR; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EMBRYOID BODY; EMBRYONIC STEM CELL; FLOW CYTOMETRY; FLUORESCENCE IMAGING; GATA4 GENE; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HCN1 GENE; HEART BEAT; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE POTENTIAL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KV4.3 GENE; MEMBRANE DIASTOLIC POTENTIAL; MLC2V GENE; MOLECULAR BIOLOGY; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE STUDY; REPOLARIZATION; SCN5A GENE; SERCA GENE; UPREGULATION;

CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; ELECTRIC STIMULATION; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MEMBRANE POTENTIALS; MYOCYTES, CARDIAC; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PROTEIN KINASE INHIBITORS; TIME FACTORS;

EID: 84890462515     PISSN: 19375387     EISSN: 19375395     Source Type: Journal    
DOI: 10.1007/s12265-013-9510-z     Document Type: Article

References (38)

1. Senyo, S. E.; Steinhauser, M. L.; Pizzimenti, C. L.; Yang, V. K.; Cai, L.; Wang, M.; et al. (2013). Mammalian heart renewal by pre-existing cardiomyocytes. Nature, 493(7432), 433-436.
2. Siu, C. W.; Tse, H. F. (2012). Cardiac regeneration: messages from CADUCEUS. Lancet, 379(9819), 870-871.
3. Liao, S. Y.; Liu, Y.; Siu, C. W.; Zhang, Y.; Lai, W. H.; Au, K. W.; et al. (2010). Proarrhythmic risk of embryonic stem cell-derived cardiomyocyte transplantation in infarcted myocardium. Heart Rhythm, 7(12), 1852-1859.
4. Liao, S. Y.; Tse, H. F.; Chan, Y. C.; Mei-Chu Yip, P.; Zhang, Y.; Liu, Y.; et al. (2013). Overexpression of Kir2.1 channel in embryonic stem cell-derived cardiomyocytes attenuates posttransplantation proarrhythmic risk in myocardial infarction. Heart Rhythm, 10(2), 273-282.
5. Ng, K. M.; Lee, Y. K.; Chan, Y. C.; Lai, W. H.; Fung, M. L.; Li, R. A.; et al. (2010). Exogenous expression of HIF-1 alpha promotes cardiac differentiation of embryonic stem cells. Journal of Molecular and Cellular Cardiology, 48(6), 1129-1137.
6. Ng, K. M.; Chan, Y. C.; Lee, Y. K.; Lai, W. H.; Au, K. W.; Fung, M. L.; et al. (2011). Cobalt chloride pretreatment promotes cardiac differentiation of human embryonic stem cells under atmospheric oxygen level. Cellular Reprogramming, 13(6), 527-537.
7. Cameron, I. L.; Hardman, W. E.; Winters, W. D.; Zimmerman, S.; Zimmerman, A. M. (1993). Environmental magnetic fields: influences on early embryogenesis. Journal of Cellular Biochemistry, 51(4), 417-425.
8. Robinson, K. R. (1985). The responses of cells to electrical fields: a review. The Journal of Cell Biology, 101(6), 2023-2027.
9. Chen, M. Q.; Xie, X.; Hollis Whittington, R.; Kovacs, G. T.; Wu, J. C.; Giovangrandi, L. (2008). Cardiac differentiation of embryonic stem cells with point-source electrical stimulation. Conference Proceedings, IEEE Engineering in Medicine and Biology Society, 2008, 1729-1732.
10. Sauer, H.; Rahimi, G.; Hescheler, J.; Wartenberg, M. (1999). Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells. Journal of Cellular Biochemistry, 75(4), 710-723.
11. Serena, E.; Figallo, E.; Tandon, N.; Cannizzaro, C.; Gerecht, S.; Elvassore, N.; et al. (2009). Electrical stimulation of human embryonic stem cells: cardiac differentiation and the generation of reactive oxygen species. Experimental Cell Research, 315(20), 3611-3619.
12. Choo, A.; Padmanabhan, J.; Chin, A.; Fong, W. J.; Oh, S. K. (2006). Immortalized feeders for the scale-up of human embryonic stem cells in feeder and feeder-free conditions. Journal of Biotechnology, 122(1), 130-141.
13. Ting, S.; Lecina, M.; Reuveny, S.; Oh, S. (2012). Differentiation of human embryonic stem cells to cardiomyocytes on microcarrier cultures. Current Protocols in Stem Cell Biology, Chapter 1, Unit1D 7.
14. Lecina, M.; Ting, S.; Choo, A.; Reuveny, S.; Oh, S. (2010). Scalable platform for human embryonic stem cell differentiation to cardiomyocytes in suspended microcarrier cultures. Tissue Engineering. Part C, Methods, 16(6), 1609-1619.
15. Chan, Y. C.; Siu, C. W.; Lau, Y. M.; Lau, C. P.; Li, R. A.; Tse, H. F. (2009). Synergistic effects of inward rectifier (I) and pacemaker (I) currents on the induction of bioengineered cardiac automaticity. Journal of Cardiovascular Electrophysiology, 20(9), 1048-1054.
16. Tandon, N.; Cannizzaro, C.; Chao, P. H.; Maidhof, R.; Marsano, A.; Au, H. T.; et al. (2009). Electrical stimulation systems for cardiac tissue engineering. Nature Protocols, 4(2), 155-173.
17. Pu, W. T.; Ishiwata, T.; Juraszek, A. L.; Ma, Q.; Izumo, S. (2004). GATA4 is a dosage-sensitive regulator of cardiac morphogenesis. Biology, 275(1), 235-244.
18. Zeisberg, E. M.; Ma, Q.; Juraszek, A. L.; Moses, K.; Schwartz, R. J.; Izumo, S.; et al. (2005). Morphogenesis of the right ventricle requires myocardial expression of Gata4. Journal of Clinical Investigation, 115(6), 1522-1531.
19. Charpentier, F.; Merot, J.; Loussouarn, G.; Baro, I. (2010). Delayed rectifier K(+) currents and cardiac repolarization. Journal of Molecular and Cellular Cardiology, 48(1), 37-44.
20. Ravens, U.; Wettwer, E. (1998). Electrophysiological aspects of changes in heart rate. Basic Research in Cardiology, 93(Suppl 1), 60-65.
21. Qu, Z.; Chung, D. (2012). Mechanisms and determinants of ultralong action potential duration and slow rate-dependence in cardiac myocytes. PLoS One, 7(8), e43587.
22. Genovese, J. A.; Spadaccio, C.; Chachques, E.; Schussler, O.; Carpentier, A.; Chachques, J. C.; et al. (2009). Cardiac pre-differentiation of human mesenchymal stem cells by electrostimulation. Frontiers in Bioscience, 14, 2996-3002.
23. Genovese, J. A.; Spadaccio, C.; Langer, J.; Habe, J.; Jackson, J.; Patel, A. N. (2008). Electrostimulation induces cardiomyocyte predifferentiation of fibroblasts. Biochemical and Biophysical Research Communications, 370(3), 450-455.
24. Gamry Instruments. (2005). Electrochemical impedance spectroscopy theory: a primer.
25. Setsukinai, K.; Urano, Y.; Kakinuma, K.; Majima, H. J.; Nagano, T. (2003). Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. Journal of Biological Chemistry, 278(5), 3170-3175.
26. Sauer, H.; Wartenberg, M. (2005). Reactive oxygen species as signaling molecules in cardiovascular differentiation of embryonic stem cells and tumor-induced angiogenesis. Antioxidants and Redox Signaling, 7(11-12), 1423-1434.
27. Puceat, M.; Travo, P.; Quinn, M. T.; Fort, P. (2003). A dual role of the GTPase Rac in cardiac differentiation of stem cells. Molecular Biology of the Cell, 14(7), 2781-2792.
28. Puceat, M. (2005). Role of Rac-GTPase and reactive oxygen species in cardiac differentiation of stem cells. Antioxidants and Redox Signaling, 7(11-12), 1435-1439.
29. Cannizzaro, C.; Tandon, N.; Figallo, E.; Park, H.; Gerecht, S.; Radisic, M.; et al. (2007). Practical aspects of cardiac tissue engineering with electrical stimulation. Methods in Molecular Medicine, 140, 291-307.
30. Huang, J. Z. C.; Zhang, W.; Zhou, X. (1997). Application of a platinum dual-disk microelectrode to measurement of the electron transfer number of dioxygen reduction. Journal of Electroanalytical Chemistry, 433, 33-39.
31. Li, J.; Stouffs, M.; Serrander, L.; Banfi, B.; Bettiol, E.; Charnay, Y.; et al. (2006). The NADPH oxidase NOX4 drives cardiac differentiation: role in regulating cardiac transcription factors and MAP kinase activation. Molecular Biology of the Cell, 17(9), 3978-3988.
32. Radisic, M.; Park, H.; Shing, H.; Consi, T.; Schoen, F. J.; Langer, R.; et al. (2004). Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proceedings of the National Academy of Sciences of the United States of America, 101(52), 18129-18134.
33. Satin, J.; Itzhaki, I.; Rapoport, S.; Schroder, E. A.; Izu, L.; Arbel, G.; et al. (2008). Calcium handling in human embryonic stem cell-derived cardiomyocytes. Stem Cells, 26(8), 1961-1972.
34. 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.
35. Loeb, G. E.; Zamin, C. J.; Schulman, J. H.; Troyk, P. R. (1991). Injectable microstimulator for functional electrical stimulation. Medical & Biological Engineering & Computing, 29(6), NS13-19.
36. Tandon, N.; Goh, B.; Marsano, A.; Chao, P. H.; Montouri-Sorrentino, C.; Gimble, J.; et al. (2009). Alignment and elongation of human adipose-derived stem cells in response to direct-current electrical stimulation. Conference Proceedings, IEEE Engineering in Medicine and Biology Society, 2009, 6517-6521.
37. Levin, M. (2003). Motor protein control of ion flux is an early step in embryonic left-right asymmetry. Bioessays, 25(10), 1002-1010.
38. Donaldson, N. D.; Donaldson, P. E. (1986). When are actively balanced biphasic ('lilly') stimulating pulses necessary in a neurological prosthesis? I. Historical background; Pt resting potential; Q studies. Medical & Biological Engineering & Computing, 24, 41-49.