Mathematical modelling of the action potential of human embryonic stem cell derived cardiomyocytes

BioMedical Engineering Online

Volumn 11, Issue , 2012, Pages

  Paci, Michelangelo ^a   Sartiani, Laura ^b   Del Lungo, Martina ^b   Jaconi, Marisa ^c   Mugelli, Alessandro ^b   Cerbai, Elisabetta ^b   Severi, Stefano ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Action potential; Computer simulation; Embryonic stem cells; Pharmacology

Indexed keywords

ACTION POTENTIALS; CARDIOMYOCYTES; CHANNEL BLOCKERS; COMPUTATIONAL MODEL; DEVELOPMENTAL STAGE; EARLY-TO-LATE; ELECTROPHYSIOLOGICAL RECORDINGS; EMBRYONIC STEM CELLS; FUNCTIONAL PROPERTIES; HIGH POTENTIAL; HUMAN EMBRYONIC STEM CELLS; IN-VITRO; IONIC CHANNELS; LATE STAGE; MODELLING TOOLS; PHARMACOLOGY; PHYSIOLOGICAL PROPERTIES; POTASSIUM CURRENTS; PROOF OF CONCEPT; SARCOPLASMIC RETICULUM; SIMULATION PLATFORM;

CALCIUM; CELL GROWTH; ELECTROPHYSIOLOGY; POTASSIUM; SODIUM;

COMPUTER SIMULATION;

CALCIUM; POTASSIUM CHANNEL BLOCKING AGENT;

ACTION POTENTIAL; ARTICLE; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECT; ELECTRIC CONDUCTIVITY; EMBRYONIC STEM CELL; FIBROBLAST; HEART MUSCLE CELL; HUMAN; INTRACELLULAR SPACE; METABOLISM; TIME;

ACTION POTENTIALS; CALCIUM; CELL DIFFERENTIATION; ELECTRIC CONDUCTIVITY; EMBRYONIC STEM CELLS; FIBROBLASTS; HUMANS; INTRACELLULAR SPACE; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; POTASSIUM CHANNEL BLOCKERS; TIME FACTORS;

EID: 84865344484     PISSN: None     EISSN: 1475925X     Source Type: Journal    
DOI: 10.1186/1475-925X-11-61     Document Type: Article

References (54)

1. Thomson JA. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
2. Rao TP, Kühl M. An updated overview on Wnt signaling pathways: a prelude for more. Circ Res 2010, 106:1798-1806. 10.1161/CIRCRESAHA.110.219840, 20576942.
3. Phillips BW, Crook JM. Pluripotent human stem cells: a novel tool in drug discovery. BioDrugs 2010, 24:99-108. 10.2165/11532270-000000000-00000, 20199125.
4. Bel A, Planat-Bernard V, Saito A, Bonnevie L, Bellamy V, Sabbah L, Bellabas L, Brinon B, Vanneaux V, Pradeau P, Peyrard S, Larghero J, Pouly J, Binder P, Garcia S, Shimizu T, Sawa Y, Okano T, Bruneval P, Desnos M, Hagège AA, Casteilla L, Pucéat M, Menasché P. Composite cell sheets: a further step toward safe and effective myocardial regeneration by cardiac progenitors derived from embryonic stem cells. Circulation 2010, 122:S118-S123. 10.1161/CIRCULATIONAHA.109.927293, 20837902.
5. Pekkanen-Mattila M, Kerkelä E, Tanskanen JMA, Pietilä M, Pelto-Huikko M, Hyttinen J, Skottman H, Suuronen R, Aalto-Setälä K. Substantial variation in the cardiac differentiation of human embryonic stem cell lines derived and propagated under the same conditions-a comparison of multiple cell lines. Ann Med 2009, 41:360-370. 10.1080/07853890802609542, 19165643.
6. Sartiani L, Bettiol E, Stillitano F, Mugelli A, Cerbai E, Jaconi ME. Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: a molecular and electrophysiological approach. Stem Cells 2007, 25(5):1136-1144. 10.1634/stemcells.2006-0466, 17255522.
7. Zeevi-Levin N, Itskovitz-Eldor J, Binah O. Functional properties of human embryonic stem cell-derived cardiomyocytes. Crit Rev Eukaryot Gene Expr 2010, 20:51-59. 10.1615/CritRevEukarGeneExpr.v20.i1.40, 20528737.
8. Asai Y, Tada M, Otsuji TG, 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 2010, 5:227-232. 10.2174/157488810791824502, 20214558.
9. Kim C, Majdi M, Xia P, Wei KA, Talantova M, Spiering S, Nelson B, Mercola M, Chen H-SV. Non-cardiomyocytes influence the electrophysiological maturation of human embryonic stem cell-derived cardiomyocytes during differentiation. Stem Cells Dev 2010, 19:783-795. 10.1089/scd.2009.0349, 3135229, 20001453.
10. Lieu DK, Liu J, Siu C-W, Mcnerney GP, Tse H-F, Abu-Khalil A, Huser T, Li RA. Absence of transverse tubules contributes to non-uniform ca2 + wavefronts in mouse and human embryonic stem cell-derived cardiomyocytes. Stem Cells Dev 2009, 18:1493-1500. 10.1089/scd.2009.0052, 3139544, 19290776.
11. Liu J, Fu JD, Siu CW, Li RA. Functional sarcoplasmic reticulum for calcium handling of human embryonic stem cell-derived cardiomyocytes: insights for driven maturation. Stem Cells 2007, 25:3038-3044. 10.1634/stemcells.2007-0549, 17872499.
12. Satin J, Itzhaki I, Rapoport S, Schroder EA, Izu L, Arbel G, Beyar R, Balke CW, Schiller J, Gepstein L. Calcium handling in human embryonic stem cell-derived cardiomyocytes. Stem Cells 2008, 26:1961-1972. 10.1634/stemcells.2007-0591, 18483424.
13. Itzhaki I, Schiller J, Beyar R, Satin J, Gepstein L. Calcium handling in embryonic stem cell-derived cardiac myocytes: of mice and men. Ann N Y Acad Sci 2006, 1080:207-215. 10.1196/annals.1380.017, 17132785.
14. Noble D. Computational models of the heart and their use in assessing the actions of drugs. J Pharmacol Sci 2008, 107:107-117. 10.1254/jphs.CR0070042, 18566519.
15. Grandi E, Pasqualini FS, Pes C, Corsi C, Zaza A, Severi S. Theoretical investigation of action potential duration dependence on extracellular Ca2+ in human cardiomyocytes. J Mol Cell Cardiol 2009, 46(3):332-342. 10.1016/j.yjmcc.2008.12.002, 19121322.
16. ten Tusscher KHWJ, Noble D, Noble PJ, Panfilov AV. A model for human ventricular tissue. Am J Physiol Heart Circ Physiol 2004, 286(4):H1573-H1589.
17. Hodgkin A, Huxley A. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol (Lond) 1952, 117:500-544.
18. Ferron L, Capuano V, Deroubaix E, Coulombe A, Renaud J-F. Functional and molecular characterization of a T-type Ca(2+) channel during fetal and postnatal rat heart development. J Mol Cell Cardiol 2002, 34:533-546. 10.1006/jmcc.2002.1535, 12056857.
19. Davies MP, An RH, Doevendans P, Kubalak S, Chien KR, Kass RS. Developmental changes in ionic channel activity in the embryonic murine heart. Circ Res 1996, 78:15-25. 10.1161/01.RES.78.1.15, 8603498.
20. Kato Y, Masumiya H, Agata N, Tanaka H, Shigenobu K. Developmental changes in action potential and membrane currents in fetal, neonatal and adult guinea-pig ventricular myocytes. J Mol Cell Cardiol 1996, 28:1515-1522. 10.1006/jmcc.1996.0141, 8841938.
21. Liu W, Yasui K, Opthof T, Ishiki R, Lee JK, Kamiya K, Yokota M, Kodama I. Developmental changes of Ca(2+) handling in mouse ventricular cells from early embryo to adulthood. Life Sci 2002, 71:1279-1292. 10.1016/S0024-3205(02)01826-X, 12106593.
22. Masuda H, Sperelakis N. Inwardly rectifying potassium current in rat fetal and neonatal ventricular cardiomyocytes. Am J Physiol 1993, 265:H1107-H1111.
23. Satin J, Kehat I, Caspi O, Huber I, Arbel G, Itzhaki I, Magyar J, Schroder EA, Perlman I, Gepstein L. Mechanism of spontaneous excitability in human embryonic stem cell derived cardiomyocytes. J Physiol (Lond) 2004, 559:479-496.
24. Itoh H, Naito Y, Tomita M. Simulation of developmental changes in action potentials with ventricular cell models. Syst Synth Biol 2007, 1:11-23. 10.1007/s11693-006-9002-4, 2533146, 19003434.
25. Ono K, Iijima T. Cardiac T-type Ca(2+) channels in the heart. J Mol Cell Cardiol 2010, 48:65-70. 10.1016/j.yjmcc.2009.08.021, 19729018.
26. Yanagi K, Takano M, Narazaki G, Uosaki H, Hoshino T, Ishii T, Misaki T, Yamashita JK. Hyperpolarization-activated cyclic nucleotide-gated channels and T-type calcium channels confer automaticity of embryonic stem cell-derived cardiomyocytes. Stem Cells 2007, 25:2712-2719. 10.1634/stemcells.2006-0388, 17656646.
27. Maltsev V, Lakatta EG. Synergism of coupled subsarcolemmal Ca2+ clocks and sarcolemmal voltage clocks confers robust and flexible pacemaker function in a novel pacemaker cell model. Am J Physiol Heart Circ Physiol 2009, 296:H594-H615. 10.1152/ajpheart.01118.2008, 2660239, 19136600.
28. Courtemanche M, Ramirez RJ, Nattel S. Ionic mechanisms underlying human atrial action potential properties: insights from a mathematical model. Am J Physiol 1998, 275:H301-H321.
29. Spence SG, Vetter C, Hoe CM. Effects of the class III antiarrhythmic, dofetilide (UK-68,798) on the heart rate of midgestation rat embryos, in vitro. Teratology 1994, 49:282-292. 10.1002/tera.1420490408, 8073367.
30. Chun KR, Koenen M, Katus HA, Zehelein J. Expression of the IKr components KCNH2 (rERG) and KCNE2 (rMiRP1) during late rat heart development. Exp Mol Med 2004, 36:367-371.
31. Wang L, Feng ZP, Kondo CS, Sheldon RS, Duff HJ. Developmental changes in the delayed rectifier K + channels in mouse heart. Circ Res 1996, 79:79-85. 10.1161/01.RES.79.1.79, 8925572.
32. Wang K, Terrenoire C, Sampson KJ, Iyer V, Osteen JD, Lu J, Keller G, Kotton DN, Kass RS. Biophysical properties of slow potassium channels in human embryonic stem cell derived cardiomyocytes implicate subunit stoichiometry. J Physiol 2011, 589(Pt 24):6093-6104.
33. DiFrancesco D. A new interpretation of the pace-maker current in calf Purkinje fibres. J Physiol (Lond) 1981, 314:359-376.
34. Otsu K, Kuruma A, Yanagida E, Shoji S, Inoue T, Hirayama Y, Uematsu H, Hara Y, Kawano S. Na+/K + ATPase and its functional coupling with Na+/Ca2+ exchanger in mouse embryonic stem cells during differentiation into cardiomyocytes. Cell Calcium 2005, 37:137-151. 10.1016/j.ceca.2004.08.004, 15589994.
35. Romero L, Pueyo E, Fink M, Rodriguez B. Impact of ionic current variability on human ventricular cellular electrophysiology. AJP: Heart and Circulatory Physiology 2009, 297:H1436-H1445.
36. Romero L, Carbonell B, Trenor B, Rodríguez B, Saiz J, Ferrero JM. Systematic characterization of the ionic basis of rabbit cellular electrophysiology using two ventricular models. Prog Biophys Mol Biol 2011, 107:60-73. 10.1016/j.pbiomolbio.2011.06.012, 21749896.
37. MacCannell KA, Bazzazi H, Chilton L, Shibukawa Y, Clark RB, Giles WR. A mathematical model of electrotonic interactions between ventricular myocytes and fibroblasts. Biophys J 2007, 92:4121-4132. 10.1529/biophysj.106.101410, 1868994, 17307821.
38. Kohl P, Kamkin AG, Kiseleva IS, Noble D. Mechanosensitive fibroblasts in the sino-atrial node region of rat heart: interaction with cardiomyocytes and possible role. Exp Physiol 1994, 79:943-956.
39. Jacquemet V, Henriquez CS. Modelling cardiac fibroblasts: interactions with myocytes and their impact on impulse propagation. Europace 2007, 9(Suppl. 6):vi29-vi37.
40. Song DK, Earm YE, Ho WK. Blockade of the delayed rectifier K + currents, IKr, in rabbit sinoatrial node cells by external divalent cations. Pflugers Arch 1999, 438:147-153. 10.1007/s004240050892, 10370100.
41. Oudit GY, Kassiri Z, Sah R, Ramirez RJ, Zobel C, Backx PH. The molecular physiology of the cardiac transient outward potassium current (I(to)) in normal and diseased myocardium. J Mol Cell Cardiol 2001, 33:851-872. 10.1006/jmcc.2001.1376, 11343410.
42. Cerbai E, Pino R, Sartiani L, Mugelli A. Influence of postnatal-development on I(f) occurrence and properties in neonatal rat ventricular myocytes. Cardiovasc Res 1999, 42:416-423. 10.1016/S0008-6363(99)00037-1, 10533577.
43. Yasui K, Liu W, Opthof T, Kada K, Lee JK, Kamiya K, Kodama I. I(f) current and spontaneous activity in mouse embryonic ventricular myocytes. Circ Res 2001, 88:536-542. 10.1161/01.RES.88.5.536, 11249878.
44. Qu Y, Ghatpande A, El-Sherif N, Boutjdir M. Gene expression of Na+/Ca2+ exchanger during development in human heart. Cardiovasc Res 2000, 45:866-873. 10.1016/S0008-6363(99)00402-2, 10728412.
45. Fu J-D, Jiang P, Rushing S, Liu J, Chiamvimonvat N, Li RA. Na+/Ca2+ exchanger is a determinant of excitation-contraction coupling in human embryonic stem cell-derived ventricular cardiomyocytes. Stem Cells Dev 2010, 19:773-782. 10.1089/scd.2009.0184, 3135244, 19719399.
46. Zahanich I, Sirenko SG, Maltseva LA, Tarasova YS, Spurgeon HA, Boheler KR, Stern MD, Lakatta EG, Maltsev VA. Rhythmic beating of stem cell-derived cardiac cells requires dynamic coupling of electrophysiology and Ca cycling. J Mol Cell Cardiol 2011, 50:66-76. 10.1016/j.yjmcc.2010.09.018, 3018669, 20920509.
47. Liu J, Lieu DK, Siu CW, Fu J-D, Tse H-F, Li RA. Facilitated maturation of Ca2+ handling properties of human embryonic stem cell-derived cardiomyocytes by calsequestrin expression. Am J Physiol Cell Physiol 2009, 297:C152-C159. 10.1152/ajpcell.00060.2009, 2711646, 19357236.
48. Yang H, Tweedie D, Wang S, Guia A, Vinogradova T, Bogdanov K, Allen PD, Stern MD, Lakatta EG, Boheler KR. The ryanodine receptor modulates the spontaneous beating rate of cardiomyocytes during development. Proc Natl Acad Sci USA 2002, 99:9225-9230. 10.1073/pnas.142651999, 123122, 12089338.
49. O'hara T, Virág L, Varró A, Rudy Y, Mcculloch A. Simulation of the undiseased human cardiac ventricular action potential: model formulation and experimental validation. PLoS Comput Biol 2011, 7:e1002061. 10.1371/journal.pcbi.1002061, 3102752, 21637795.
50. Bettiol E, Sartiani L, Chicha L, Krause KH, Cerbai E, Jaconi ME. Fetal bovine serum enables cardiac differentiation of human embryonic stem cells. Differentiation; research in biological diversity 2007, 75:669-681. 10.1111/j.1432-0436.2007.00174.x, 23024929.
51. Yazawa M, Hsueh B, Jia X, Pasca AM, Bernstein JA, Hallmayer J, Dolmetsch RE. Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome. Nature 2011, 471:230-234. 10.1038/nature09855, 3077925, 21307850.
52. Matsa E, Rajamohan D, Dick E, Young L, Mellor I, Staniforth A, Denning C. Drug evaluation in cardiomyocytes derived from human induced pluripotent stem cells carrying a long QT syndrome type 2 mutation. Eur Heart J 2011, 32:952-962. 10.1093/eurheartj/ehr073, 3076668, 21367833.
53. Sartiani L, Cerbai E, Lonardo G, DePaoli P, Tattoli M, Cagiano R, Carratù MR, Cuomo V, Mugelli A. Prenatal exposure to carbon monoxide affects postnatal cellular electrophysiological maturation of the rat heart: a potential substrate for arrhythmogenesis in infancy. Circulation 2004, 109(3):419-423. 10.1161/01.CIR.0000109497.73223.4D, 14718404.
54. Barbieri M, Varani K, Cerbai E, Guerra L, Li Q, Borea PA, Mugelli A. Electrophysiological basis for the enhanced cardiac arrhythmogenic effect of isoprenaline in aged spontaneously hypertensive rats. J Mol Cell Cardiol 1994, 26(7):849-860. 10.1006/jmcc.1994.1102, 7966353.