Functional maturation of human pluripotent stem cell derived cardiomyocytes invitro - Correlation between contraction force andelectrophysiology

Biomaterials

Volumn 51, Issue , 2015, Pages 138-150

  Ribeiro, Marcelo C ^a   Tertoolen, Leon G ^a   Guadix, Juan A ^a,b   Bellin, Milena ^a   Kosmidis, Georgios ^a   D'Aniello, Cristina ^a   Monshouwer Kloots, Jantine ^a   Goumans, Marie Jose ^a   Wang, Yu li ^c   Feinberg, Adam W ^c   Mummery, Christine L ^a   Passier, Robert ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF MÁLAGA   (Spain)

^c CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

Cardiomyocyte contraction force; Cardiomyocyte maturation; Human fetal cardiomyocytes; Human pluripotent stem cells

Indexed keywords

ELECTRON DEVICE MANUFACTURE; ELECTROPHYSIOLOGY; GENE EXPRESSION; JUNCTION GATE FIELD EFFECT TRANSISTORS;

CARDIOMYOCYTE CONTRACTION; CARDIOMYOCYTES; CONTRACTION STRESS; MEMBRANE POTENTIALS; MICRO CONTACT PRINTING; PLURIPOTENT STEM CELLS; POLYACRYLAMIDE GELS; STRONG CORRELATION;

STEM CELLS;

ACTININ; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; POLYACRYLAMIDE GEL; POTASSIUM CHANNEL KCNQ1; RYANODINE RECEPTOR 2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM CHANNEL NAV1.5;

ACTION POTENTIAL; ARTICLE; CELL MATURATION; CONTRACTION STRESS; GENE EXPRESSION; HEART DEVELOPMENT; HEART ELECTROPHYSIOLOGY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MEMBRANE STEADY POTENTIAL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SARCOMERE; BIOMECHANICS; CELL DIFFERENTIATION; CYTOLOGY; ELECTROPHYSIOLOGY; FETUS; GENE EXPRESSION REGULATION; HEART CONTRACTION; HUMAN EMBRYONIC STEM CELL; METABOLISM; PHYSIOLOGICAL STRESS;

BIOMECHANICAL PHENOMENA; CELL DIFFERENTIATION; ELECTROPHYSIOLOGICAL PHENOMENA; FETUS; GENE EXPRESSION REGULATION; HUMAN EMBRYONIC STEM CELLS; HUMANS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS; SARCOMERES; STRESS, PHYSIOLOGICAL;

EID: 84924874555     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.01.067     Document Type: Article

References (52)

1. Mummery C.L., Zhang J., Ng E.S., Elliott D a, Elefanty A.G., Kamp T.J. Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: a methods overview. Circ Res 2012, 111(3):344-358.
2. Bellin M., Marchetto M.C., Gage F.H., Mummery C.L. Induced pluripotent stem cells: the new patient?. Nat Rev Mol Cell Biol Nat Publ Group 2012, 13(11):713-726.
3. Davis R.P., van den Berg C.W., Casini S., Braam S.R., Mummery C.L. Pluripotent stem cell models of cardiac disease and their implication for drug discovery and development. Trends Mol Med 2011, 17(9):475-484. Elsevier Ltd.
4. Synnergren J., Améen C., Jansson A., Sartipy P. Global transcriptional profiling reveals similarities and differences between human stem cell-derived cardiomyocyte clusters and heart tissue. Physiol Genomics 2012, 44(4):245-258.
5. Mummery C., Ward-van Oostwaard D., Doevendans P., Spijker R., van den Brink S., Hassink R., et al. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 2003, 107(21):2733-2740.
6. Lopaschuk G.D., Jaswal J.S. Energy metabolic phenotype of the cardiomyocyte during development, differentiation, and postnatal maturation. JCardiovasc Pharmacol 2010, 56(2):130-140.
7. Maillet M., van Berlo J.H., Molkentin J.D. Molecular basis of physiological heart growth: fundamental concepts and new players. Nat Rev Mol Cell Biol 2013, 14(1):38-48. Nature Publishing Group.
8. Yang X., Pabon L., Murry C.E. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res 2014, 114(3):511-523.
9. Kita-Matsuo H., Barcova M., Prigozhina N., Salomonis N., Wei K., Jacot J.G., et al. Lentiviral vectors and protocols for creation of stable hESC lines for fluorescent tracking and drug resistance selection of cardiomyocytes. PLoS One 2009, 4(4):e5046.
10. Stoehr A., Neuber C., Baldauf C., Vollert I., Friedrich F.W., Flenner F., et al. Automated analysis of contractile force and Ca2+ transients in engineered heart tissue. Am J Physiol Heart Circ Physiol 2014, 306(9):H1353-H1363.
11. Kensah G., Roa Lara A., Dahlmann J., Zweigerdt R., Schwanke K., Hegermann J., et al. Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue invitro. Eur Heart J 2013, 34(15):1134-1146.
12. Zhang D., Shadrin I.Y., Lam J., Xian H.-Q., Snodgrass H.R., Bursac N. Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 2013, 34(23):5813-5820. Elsevier Ltd.
13. Hazeltine L.B., Simmons C.S., Salick M.R., Lian X., Badur M.G., Han W., et al. Effects of substrate mechanics on contractility of cardiomyocytes generated from human pluripotent stem cells. Int J Cell Biol 2012, 2012:508294.
14. 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 2013, 22(14):1991-2002.
15. Jacot J.G., McCulloch A.D., Omens J.H. Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys J 2008, 95(7):3479-3487.
16. Kuo P.-L., Lee H., Bray M.-A., Geisse N a, Huang Y.-T., Adams W.J., et al. Myocyte shape regulates lateral registry of sarcomeres and contractility. Am J Pathol 2012, 181(6):2030-2037. Elsevier Inc.
17. Gerdes a.M., Kellerman S.E., Moore J.a., Muffly K.E., Clark L.C., Reaves P.Y., et al. Structural remodeling of cardiac myocytes in patients with ischemic cardiomyopathy. Circulation 1992, 86(2):426-430.
18. Xia Yang, Maximilian Buja L., Scarpulla Richard C., JBM Electrical stimulation of neonatal cardiomyocytes results in the sequential activation of nuclear genes governing mitochondrial. Proc Natl Acad Sci 1997, 94:11399-11404. (October).
19. Mihic A., Li J., Miyagi Y., Gagliardi M., Li S.-H., Zu J., et al. The effect of cyclic stretch on maturation and 3D tissue formation of human embryonic stem cell-derived cardiomyocytes. Biomaterials 2014, 35(9):2798-2808. Elsevier Ltd.
20. Kim C., Wong J., Wen J., Wang S., Wang C., Spiering S., et al. Studying arrhythmogenic right ventricular dysplasia with patient-specific iPSCs. Nature 2013, 494(7435):105-110. Nature Publishing Group.
21. Snir M., Kehat I., Gepstein A., Coleman R., Itskovitz-Eldor J., Livne E., et al. Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. Am J Physiol Heart Circ Physiol 2003, 285(6):H2355-H2363.
22. Kadota S., Minami I., Morone N., Heuser J.E., Agladze K., Nakatsuji N. Development of a reentrant arrhythmia model in human pluripotent stem cell-derived cardiac cell sheets. Eur Heart J 2013, 34(15):1147-1156.
23. Chopra A., Tabdanov E., Patel H., Janmey P a, Kresh J.Y. Cardiac myocyte remodeling mediated by N-cadherin-dependent mechanosensing. Am J Physiol Heart Circ Physiol 2011, 300(4):H1252-H1266.
24. McCain M.L., Parker K.K. Mechanotransduction: the role of mechanical stress, myocyte shape, and cytoskeletal architecture on cardiac function. Pflugers Arch 2011, 462(1):89-104.
25. Pijnappels D a, Schalij M.J., Ramkisoensing A a, van Tuyn J., de Vries A.a F., van der Laarse A., et al. Forced alignment of mesenchymal stem cells undergoing cardiomyogenic differentiation affects functional integration with cardiomyocyte cultures. Circ Res 2008, 103(2):167-176.
26. Kléber A.G., Rudy Y. Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol Rev 2004, 84(2):431-488.
27. Walsh K.B., Parks G.E. Changes in cardiac myocyte morphology alter the properties of voltage-gated ion channels. Cardiovasc Res 2002, 55(1):64-75.
28. Feinberg A.W., Feigel A., Shevkoplyas S.S., Sheehy S., Whitesides G.M., Parker K.K. Muscular thin films for building actuators and powering devices. Science 2007, 317(5843):1366-1370.
29. Bray M.-A., Sheehy S.P., Parker K.K. Sarcomere alignment is regulated by myocyte shape. Cell Motil Cytoskelet 2008, 65(8):641-651.
30. Pascual A., Aranda A. Thyroid hormone receptors, cell growth and differentiation. Biochim Biophys Acta 2013, 1830(7):3908-3916. Elsevier B.V.
31. Klein I., Danzi S. Thyroid disease and the heart. Circulation 2007, 116(15):1725-1735.
32. Lee Y.-K., Ng K.-M., Chan Y.-C., Lai W.-H., Au K.-W., Ho C.-Y.J., et al. Triiodothyronine promotes cardiac differentiation and maturation of embryonic stem cells via the classical genomic pathway. Mol Endocrinol 2010, 24(9):1728-1736.
33. Yang X., Rodriguez M., Pabon L., Fischer K a, Reinecke H., Regnier M., et al. Tri-iodo-l-thyronine promotes the maturation of human cardiomyocytes-derived from induced pluripotent stem cells. JMol Cell Cardiol 2014, 72:296-304. Elsevier Ltd.
34. Elliott D a, Braam S.R., Koutsis K., Ng E.S., Jenny R., Lagerqvist E.L., et al. NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat Methods 2011, 8(12):1037-1040.
35. Ng E.S., Davis R., Stanley E.G., Elefanty A.G. Aprotocol describing the use of a recombinant protein-based, animal product-free medium (APEL) for human embryonic stem cell differentiation as spin embryoid bodies. Nat Protoc 2008, 3(5):768-776.
36. Rape A.D., Guo W.-H., Wang Y.-L. The regulation of traction force in relation to cell shape and focal adhesions. Biomaterials 2011, 32(8):2043-2051. Elsevier Ltd.
37. Frey M.T., Engler A., Discher D.E., Lee J., Wang Y.-L. Microscopic methods for measuring the elasticity of gel substrates for cell culture: microspheres, microindenters, and atomic force microscopy. Methods Cell Biol 2007, 83(07):47-65.
38. Birket M.J., Casini S., Kosmidis G., Elliott D a, Gerencser A a, Baartscheer A., et al. PGC-1α and reactive oxygen species regulate human embryonic stem cell-derived cardiomyocyte function. Stem Cell Reports 2013, 1(6):560-574. The Authors.
39. Claire Robertson S.C.G. Maturation phases of human pluripotent stem cell-derived cardiomyocytes. Stem Cells 2013, 31(5):1-17.
40. Hasenfuss G., Mulieri L a., Blanchard E.M., Holubarsch C., Leavitt B.J., Ittleman F., et al. Energetics of isometric force development in control and volume- overload human myocardium. Comparison with animal species. Circ Res 1991, 68(3):836-846.
41. Iruretagoyena J.I., Davis W., Bird C., Olsen J., Radue R., Teo Broman a, et al. Metabolic gene profile in early human fetal heart development. Mol Hum Reprod 2014, 20(7):690-700.
42. Koncz I., Szél T., Bitay M., Cerbai E., Jaeger K., Fülöp F., et al. Electrophysiological effects of ivabradine in dog and human cardiac preparations: potential antiarrhythmic actions. Eur J Pharmacol 2011, 668(3):419-426. Elsevier B.V.
43. Feinberg A.W., Alford P.W., Jin H., Ripplinger C.M., Werdich A a, Sheehy S.P., et al. Controlling the contractile strength of engineered cardiac muscle by hierarchal tissue architecture. Biomaterials 2012, 33(23):5732-5741. Elsevier Ltd.
44. Li R.K., Mickle D a, Weisel R.D., Carson S., Omar S a, Tumiati L.C., et al. Human pediatric and adult ventricular cardiomyocytes in culture: assessment of phenotypic changes with passaging. Cardiovasc Res 1996, 32(2):362-373.
45. Xu X.Q., Soo S.Y., Sun W., Zweigerdt R. Global expression profile of highly enriched cardiomyocytes derived from human embryonic stem cells. Stem Cells 2009, 27(9):2163-2174.
46. Gorza L., Mercadier J.J., Schwartz K., Thornell L.E., Sartore S., Schiaffino S. Myosin types in the human heart. An immunofluorescence study of normal and hypertrophied atrial and ventricular myocardium. Circ Res 1984, 54(6):694-702.
47. Saggin L., Gorza L., Ausoni S., Schiaffino S. Troponin I switching in the developing heart. JBiol Chem 1989, 264(27):16299-16302.
48. Adriana Blazeski L.T. Cardiomyocytes derived from human induced pluripotent stem cells as models for normal and diseased cardiac electrophysiology and contractility. Prog Biophys Mol Biol 2012, 110(0):166-177.
49. Kim C., Majdi M., Xia P., Wei K a, Talantova M., Spiering S., et al. Non-cardiomyocytes influence the electrophysiological maturation of human embryonic stem cell-derived cardiomyocytes during differentiation. Stem Cells Dev 2010, 19(6):783-795.
50. Accili E a, Proenza C., Baruscotti M., DiFrancesco D. From funny current to HCN channels: 20 years of excitation. News Physiol Sci 2002, 17(6):32-37.
51. Weitzel J.M., Radtke C., Seitz H.J. Two thyroid hormone-mediated gene expression patterns invivo identified by cDNA expression arrays in rat. Nucleic Acids Res 2001, 29(24):5148-5155.
52. Sakaguchi Y., Cui G., Sen L. Acute effects of thyroid hormone on inward rectifier potassium channel currents in Guinea pig ventricular myocytes. Endocrinology 1996, 137(11):4744-4751.