Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2018, Article ID 6067096, 14 pages
https://doi.org/10.1155/2018/6067096
Research Article

Ion Channel Expression and Characterization in Human Induced Pluripotent Stem Cell-Derived Cardiomyocytes

1First Department of Medicine, Faculty of Medicine, University Medical Centre Mannheim (UMM), University of Heidelberg, Mannheim, Germany
2DZHK (German Center for Cardiovascular Research), Partner Sites, Heidelberg-Mannheim and Göttingen, Mannheim, Germany
3Key Laboratory of Medical Electrophysiology of Ministry of Education, Institute of Cardiovascular Research, Southwest Medical University, Luzhou, Sichuan, China
4Institute of Pharmacology and Toxicology, University of Göttingen, Göttingen, Germany
5Stem Cell Unit, Clinic for Cardiology and Pneumology, University Medical Center Göttingen, Göttingen, Germany
6Skin Cancer Unit, German Cancer Research Center (DKFZ), Heidelberg, Germany
7Department of Dermatology, Venereology and Allergology, University Medical Center Mannheim, University of Heidelberg, Mannheim, Germany
8Institute of Experimental and Clinical Pharmacology and Toxicology, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany

Correspondence should be addressed to Xiao-Bo Zhou; ed.grebledieh-inu.amdem@uohz.oboaix

Received 17 March 2017; Revised 1 August 2017; Accepted 4 December 2017; Published 8 January 2018

Academic Editor: Jay L. Vivian

Copyright © 2018 Zhihan Zhao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Takahashi, K. Tanabe, M. Ohnuki et al., “Induction of pluripotent stem cells from adult human fibroblasts by defined factors,” Cell, vol. 131, no. 5, pp. 861–872, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Takahashi and S. Yamanaka, “Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors,” Cell, vol. 126, no. 4, pp. 663–676, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. J. Yu, M. A. Vodyanik, K. Smuga-Otto et al., “Induced pluripotent stem cell lines derived from human somatic cells,” Science, vol. 318, no. 5858, pp. 1917–1920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Zhang, G. F. Wilson, A. G. Soerens et al., “Functional cardiomyocytes derived from human induced pluripotent stem cells,” Circulation Research, vol. 104, no. 4, pp. e30–e41, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. I. Germanguz, O. Sedan, N. Zeevi-Levin et al., “Molecular characterization and functional properties of cardiomyocytes derived from human inducible pluripotent stem cells,” Journal of Cellular and Molecular Medicine, vol. 15, no. 1, pp. 38–51, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Ma, L. Guo, S. J. Fiene et al., “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, vol. 301, no. 5, pp. H2006–H2017, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. I. Itzhaki, L. Maizels, I. Huber et al., “Modelling the long QT syndrome with induced pluripotent stem cells,” Nature, vol. 471, no. 7337, pp. 225–229, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Moretti, M. Bellin, A. Welling et al., “Patient-specific induced pluripotent stem-cell models for long-QT syndrome,” The New England Journal of Medicine, vol. 363, no. 15, pp. 1397–1409, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Hoekstra, C. L. Mummery, A. A. Wilde, C. R. Bezzina, and A. O. Verkerk, “Induced pluripotent stem cell derived cardiomyocytes as models for cardiac arrhythmias,” Frontiers in Physiology, vol. 3, p. 346, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Yazawa, B. Hsueh, X. Jia et al., “Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome,” Nature, vol. 471, no. 7337, pp. 230–234, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Novak, L. Barad, N. Zeevi-Levin et al., “Cardiomyocytes generated from CPVTD307H patients are arrhythmogenic in response to β-adrenergic stimulation,” Journal of Cellular and Molecular Medicine, vol. 16, no. 3, pp. 468–482, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. M. A. Laflamme, K. Y. Chen, A. V. Naumova et al., “Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts,” Nature Biotechnology, vol. 25, no. 9, pp. 1015–1024, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Yang, M. H. Soonpaa, E. D. Adler et al., “Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population,” Nature, vol. 453, no. 7194, pp. 524–528, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. S. J. Kattman, A. D. Witty, 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, vol. 8, no. 2, pp. 228–240, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Uosaki, H. Fukushima, A. Takeuchi et al., “Efficient and scalable purification of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression,” PLoS One, vol. 6, no. 8, article e23657, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Xu, S. Police, N. Rao, and M. K. Carpenter, “Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells,” Circulation Research, vol. 91, no. 6, pp. 501–508, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. I. Huber, I. Itzhaki, O. Caspi et al., “Identification and selection of cardiomyocytes during human embryonic stem cell differentiation,” The FASEB Journal, vol. 21, no. 10, pp. 2551–2563, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Hattori, H. Chen, H. Yamashita et al., “Nongenetic method for purifying stem cell-derived cardiomyocytes,” Nature Methods, vol. 7, no. 1, pp. 61–66, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. N. C. Dubois, A. M. Craft, P. Sharma et al., “SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells,” Nature Biotechnology, vol. 29, no. 11, pp. 1011–1018, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. W. Rust, T. Balakrishnan, and R. Zweigerdt, “Cardiomyocyte enrichment from human embryonic stem cell cultures by selection of ALCAM surface expression,” Regenerative Medicine, vol. 4, no. 2, pp. 225–237, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Lin, J. Kim, Y. Li et al., “High-purity enrichment of functional cardiovascular cells from human iPS cells,” Cardiovascular Research, vol. 95, no. 3, pp. 327–335, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. B. C. Knollmann, “Induced pluripotent stem cell-derived cardiomyocytes: boutique science or valuable arrhythmia model?” Circulation Research, vol. 112, no. 6, pp. 969–976, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. L. Larribere, H. Wu, D. Novak et al., “NF1 loss induces senescence during human melanocyte differentiation in an iPSC-based model,” Pigment Cell & Melanoma Research, vol. 28, no. 4, pp. 407–416, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Maherali, T. Ahfeldt, A. Rigamonti, J. Utikal, C. Cowan, and K. Hochedlinger, “A high-efficiency system for the generation and study of human induced pluripotent stem cells,” Cell Stem Cell, vol. 3, no. 3, pp. 340–345, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Diecke, J. Lu, J. Lee et al., “Novel codon-optimized mini-intronic plasmid for efficient, inexpensive, and xeno-free induction of pluripotency,” Scientific Reports, vol. 5, no. 1, p. 8081, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. I. El-Battrawy, S. Lang, Z. Zhao et al., “Hyperthermia influences the effects of sodium channel blocking drugs in human-induced pluripotent stem cell-derived cardiomyocytes,” PLoS One, vol. 11, no. 11, article e0166143, 2016. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Yücel, Z. Zhao, I. El-Battrawy et al., “Lipopolysaccharides induced inflammatory responses and electrophysiological dysfunctions in human-induced pluripotent stem cell derived cardiomyocytes,” Scientific Reports, vol. 7, no. 1, p. 2935, 2017. View at Publisher · View at Google Scholar
  28. C. H. Orchard and H. E. Cingolani, “Acidosis and arrhythmias in cardiac muscle,” Cardiovascular Research, vol. 28, no. 9, pp. 1312–1319, 1994. View at Publisher · View at Google Scholar
  29. A. Aberra, K. Komukai, F. C. Howarth, and C. H. Orchard, “The effect of acidosis on the ECG of the rat heart,” Experimental Physiology, vol. 86, no. 1, pp. 27–31, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. G. A. Gintant and D. W. Liu, “Beta-adrenergic modulation of fast inward sodium current in canine myocardium. Syncytial preparations versus isolated myocytes,” Circulation Research, vol. 70, no. 4, pp. 844–850, 1992. View at Publisher · View at Google Scholar
  31. J. Liu, Z. Laksman, and P. H. Backx, “The electrophysiological development of cardiomyocytes,” Advanced Drug Delivery Reviews, vol. 96, pp. 253–273, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. N. H. van den Heuvel, T. A. van Veen, B. Lim, and M. K. Jonsson, “Lessons from the heart: mirroring electrophysiological characteristics during cardiac development to in vitro differentiation of stem cell derived cardiomyocytes,” Journal of Molecular and Cellular Cardiology, vol. 67, pp. 12–25, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. H. C. Hartzell, “Regulation of cardiac ion channels by catecholamines, acetylcholine and second messenger systems,” Progress in Biophysics and Molecular Biology, vol. 52, no. 3, pp. 165–247, 1988. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Barbuti, P. Benzoni, G. Campostrini, and P. Dell'Era, “Human derived cardiomyocytes: a decade of knowledge after the discovery of induced pluripotent stem cells,” Developmental Dynamics, vol. 245, no. 12, pp. 1145–1158, 2016. View at Publisher · View at Google Scholar · View at Scopus
  35. I. Karakikes, M. Ameen, V. Termglinchan, and J. C. Wu, “Human induced pluripotent stem cell-derived cardiomyocytes: insights into molecular, cellular, and functional phenotypes,” Circulation Research, vol. 117, no. 1, pp. 80–88, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. J. J. Matsuda, H. C. Lee, and E. F. Shibata, “Acetylcholine reversal of isoproterenol-stimulated sodium currents in rabbit ventricular myocytes,” Circulation Research, vol. 72, no. 3, pp. 517–525, 1993. View at Publisher · View at Google Scholar
  37. K. Ono and T. Iijima, “Cardiac T-type Ca2+ channels in the heart,” Journal of Molecular and Cellular Cardiology, vol. 48, no. 1, pp. 65–70, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Y. Ivashchenko, G. C. Pipes, I. M. Lozinskaya et al., “Human-induced pluripotent stem cell-derived cardiomyocytes exhibit temporal changes in phenotype,” American Journal of Physiology Heart and Circulatory Physiology, vol. 305, no. 6, pp. H913–H922, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. H. D. Devalla, V. Schwach, J. W. Ford et al., “Atrial-like cardiomyocytes from human pluripotent stem cells are a robust preclinical model for assessing atrial-selective pharmacology,” EMBO Molecular Medicine, vol. 7, no. 4, pp. 394–410, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Mori, T. Saito, Y. Masuda, and H. Nakaya, “Effects of class III antiarrhythmic drugs on the Na+-activated K+ channels in guinea-pig ventricular cells,” British Journal of Pharmacology, vol. 119, no. 1, pp. 133–141, 1996. View at Publisher · View at Google Scholar
  41. S. E. Dryer, “Na+-activated K+ channels: a new family of large-conductance ion channels,” Trends in Neurosciences, vol. 17, no. 4, pp. 155–160, 1994. View at Publisher · View at Google Scholar · View at Scopus
  42. S. H. Lee, Y. C. Chen, S. Y. Chen, C. I. Lin, Y. J. Chen, and S. A. Chen, “Swelling activated chloride currents in the electrical activity of pulmonary vein cardiomyocytes,” European Journal of Clinical Investigation, vol. 38, no. 1, pp. 17–23, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Xu, P. H. Dong, Z. Zhang, G. U. Ahmmed, and N. Chiamvimonvat, “Presence of a calcium-activated chloride current in mouse ventricular myocytes,” American Journal of Physiology - Heart and Circulatory Physiology, vol. 283, no. 1, pp. H302–H314, 2002. View at Publisher · View at Google Scholar
  44. M. Harada, X. Luo, X. Y. Qi et al., “Transient receptor potential canonical-3 channel-dependent fibroblast regulation in atrial fibrillation,” Circulation, vol. 126, no. 17, pp. 2051–2064, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. M. X. Doss, J. M. Di Diego, R. J. Goodrow et al., “Maximum diastolic potential of human induced pluripotent stem cell-derived cardiomyocytes depends critically on IKr,” PLoS One, vol. 7, no. 7, article e40288, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Mandel, A. Weissman, R. Schick et al., “Human embryonic and induced pluripotent stem cell–derived cardiomyocytes exhibit beat rate variability and power-law behavior,” Circulation, vol. 125, no. 7, pp. 883–893, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. C. B. Jung, A. Moretti, M. Mederos y Schnitzler et al., “Dantrolene rescues arrhythmogenic RYR2 defect in a patient-specific stem cell model of catecholaminergic polymorphic ventricular tachycardia,” EMBO Molecular Medicine, vol. 4, no. 3, pp. 180–191, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Tiburcy, J. E. Hudson, P. Balfanz et al., “Defined engineered human myocardium with advanced maturation for applications in heart failure modeling and repair,” Circulation, vol. 135, no. 19, pp. 1832–1847, 2017. View at Publisher · View at Google Scholar
  49. M. Finlay, S. C. Harmer, and A. Tinker, “The control of cardiac ventricular excitability by autonomic pathways,” Pharmacology & Therapeutics, vol. 174, pp. 97–111, 2017. View at Publisher · View at Google Scholar
  50. O. E. Brodde, “β1- and β2-Adrenoceptors in the human heart: properties, function, and alterations in chronic heart failure,” Pharmacological Reviews, vol. 43, no. 2, pp. 203–242, 1991. View at Google Scholar
  51. Z. Wang, H. Shi, and H. Wang, “Functional M3 muscarinic acetylcholine receptors in mammalian hearts,” British Journal of Pharmacology, vol. 142, no. 3, pp. 395–408, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Ben-Ari, S. Naor, N. Zeevi-Levin et al., “Developmental changes in electrophysiological characteristics of human-induced pluripotent stem cell-derived cardiomyocytes,” Heart Rhythm, vol. 13, no. 12, pp. 2379–2387, 2016. View at Publisher · View at Google Scholar
  53. S. D. Lundy, W. Z. Zhu, M. Regnier, and M. A. Laflamme, “Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells,” Stem Cells and Development, vol. 22, no. 14, pp. 1991–2002, 2013. View at Publisher · View at Google Scholar · View at Scopus