Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: Insights into the development of cell-based pacemakers

Circulation

Volumn 111, Issue 1, 2005, Pages 11-20

  Xue, Tian ^a   Cho, Hee Cheol ^a   Akar, Fadi G ^a   Tsang, Suk Ying ^a   Jones, Steven P ^a   Marbán, Eduardo ^a   Tomaselli, Gordon F ^a   Li, Ronald A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac development; Gene therapy; Pacemakers; Stem cells; Viruses

Indexed keywords

4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; ISOPRENALINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ARTIFICIAL HEART PACEMAKER; BLASTOCYST; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; ELECTRIC ACTIVITY; EMBRYO; EMBRYONIC STEM CELL; GENE THERAPY; GENETIC ENGINEERING; GUINEA PIG; HEART CONTRACTION; HEART DEPOLARIZATION; HEART ELECTROPHYSIOLOGY; HEART LEFT VENTRICLE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMPLANTATION; IN VITRO STUDY; IN VIVO STUDY; LENTIVIRINAE; MEMBRANE DEPOLARIZATION; NEWBORN; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RAT; STEM CELL TRANSPLANTATION; SYNCYTIUM; VIRUS RECOMBINANT;

ACTION POTENTIALS; ADRENERGIC BETA-AGONISTS; ANIMALS; CELL DIFFERENTIATION; CELL FUSION; CELLS, CULTURED; DEFECTIVE VIRUSES; ELECTROPHYSIOLOGY; FEMALE; GENES, REPORTER; GENETIC VECTORS; GIANT CELLS; GREEN FLUORESCENT PROTEINS; GUINEA PIGS; HEART; HEART CONDUCTION SYSTEM; HEART VENTRICLES; HIV-1; HUMANS; ISOPROTERENOL; LIDOCAINE; MICE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; ORGAN CULTURE TECHNIQUES; PERICARDIUM; PLURIPOTENT STEM CELLS; PYRIMIDINES; RATS; TRANSDUCTION, GENETIC;

EID: 11244249952     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000151313.18547.A2     Document Type: Article

References (39)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998;.282:1145-1147.
2. Xu C, Police S, Rao N, Carpenter MK. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res. 2002;91:501-508.
3. Kehat I, Kenyagin-Karsend D, Snir M, Segev H, Amit M, Gepstein A, Livne E, Binah O, Itskovitz-Eldor J, Gepstein L. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest. 2001;108:407-414.
4. He JQ, Ma Y, Lee Y, Thomson JA, Kamp TJ. Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res. 2003;93:32-39.
5. Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den Brink S, Hassink R, van der Heyden M, Opthof T, Pera M, de la Riviere AB, Passier R, Tertoolen L. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation. 2003;107:2733-2740.
6. Kehat I, Gepstein A, Spira A, Itskovitz-Eldor J, Gepstein L. High-resolution electrophysiological assessment of human embryonic stem cell-derived cardiomyocytes: a novel in vitro model for the study of conduction. Circ Res. 2002;91:659-661.
7. Cho H, Xue T, Akar F, Jones S, Tomaselli GF, Marbán E, Li RA. Genetically-engineered human embryonic stem cell-derived cardiomyocytes can form a functional electrical syncytium with normally-quiescent recipient ventricular cells after transplantation. Biophys J. 2003;86:293a. Abstract.
8. Xue T, Chan C, Henrikson C, Sang D, Marban E, Li R. Lentivirus-mediated genetic manipulations of human embryonic stem cells and their cardiac derivatives. Circulation. 2003;108(suppl IV):IV-33. Abstract.
9. Trono D. Lentiviral Vectors. New York/Berlin/Heidelberg: Springer-Verlag; 2002.
10. Fleury S, Simeoni E, Zuppinger C, Deglon N, von Segesser LK, Kappenberger L, Vassalli G. Multiply attenuated, self-inactivating lentiviral vectors efficiently deliver and express genes for extended periods of time in adult rat cardiomyocytes in vivo. Circulation. 2003;107: 2375-2382.
11. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol. 1998;72:9873-9880.
12. + channel mutant probed by viral gene transfer in cardiomyocytes. J Physiol. 2001;533: 127-133.
13. Poelzing S, Akar FG, Baron E, Rosenbaum DS. Heterogeneous connexin43 expression produces electrophysiological heterogeneities across ventricular wall. Am J Physiol Heart Circ Physiol. 2004;286: H2001-H2009.
14. Ma Y, Ramezani A, Lewis R, Hawley RG, Thomson JA. High-level sustained transgene expression in human embryonic stem cells using lentiviral vectors. Stem Cells. 2003;21:111-117.
15. Jahner D, Stuhlmann H, Stewart CL, Harbers K, Lohler J, Simon I, Jaenisch R. De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature. 1982;298:623-628.
16. Niwa O, Yokota Y, Ishida H, Sugahara T. Independent mechanisms involved in suppression of the Moloney leukemia virus genome during differentiation of murine teratocarcinoma cells. Cell. 1983;32: 1105-1113.
17. Sperelakis N. An electric field mechanism for transmission of excitation between myocardial cells. Circ Res. 2002;91:985-987.
18. Anderson KP, Walker R, Lux RL, Ershler PR, Menlove R, Williams MR, Krall R, Moddrelle D. Conduction velocity depression and drug-induced ventricular tachyarrhythmias: effects of lidocaine in the intact canine heart. Circulation. 1990;81:1024-1038.
19. Nesterenko VV, Anyukhovsky EP, Starmer CF, Beloshapko GG, Ivanovoch T, Makielski JC, Bugrij EM, Mazaev AV, Rosenshtraukh LV. Modulating intraventricular conduction through competition of two class 1 anti-arrhythmic agents: experience with ethacizin and lidocaine in canine heart. J Mol Cell Cardiol. 1991;23(suppl 1):115-124.
20. Jalife J, Sicouri S, Delmar M, Michaels DC. Electrical uncoupling and impulse propagation in isolated sheep Purkinje fibers. Am J Physiol. 1989;257:H179-H189.
21. Lakatta EG, Maltsev VA, Bogdanov KY, Stern MD, Vinogradova TM. Cyclic variation of intracellular calcium: a critical factor for cardiac pacemaker cell dominance. Circ Res. 2003;92:e45-e50.
22. Robinson RB, Siegelbaum SA. Hyperpolarization-activated cation currents: from molecules to physiological functions. Anna Rev Physiol. 2003;65:453-480.
23. Satin J, Kehat I, Caspi O, Huber I, Arbel G, Izhaki I, Magyar J, Schroder EA, Perlman I, Gepstein L. Mechanism of spontaneous excitability in human embryonic stem cell derived cardiomyocyles. J Physiol. 2004; 559(pt 2):479-496.
24. BoSmith RE, Briggs I, Sturgess NC. Inhibitory actions of ZENECA ZD7288 on whole-cell hyperpolarization activated inward current (If) in guinea-pig dissociated sinoatrial node cells. Br J Pharmacol. 1993;110: 343-349.
25. 2+-waves in mammalian cardiac and vascular smooth muscle cells. Cell Calcium. 1991;12: 241-254.
26. Rubart M, Pasumarthi KB, Nakajima H, Soonpaa MH, Nakajima HO, Field LJ. Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ Res. 2003;92:1217-1224.
27. Klug MG, Soonpaa MH, Koh GY, Field LJ. Genetically selected cardiomyocytes from differentiating embryonic stem cells form stable intracardiac grafts. J Clin Invest. 1996;98:216-224.
28. Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L. Petersen BE, Scott EW. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature. 2002; 416:542-545.
29. Ying QL, Nichols J, Evans EP, Smith AG. Changing potency by spontaneous fusion. Nature. 2002;416:545-548.
30. Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature. 2004;428:668-673.
31. Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, Pasumarthi KB, Virag JI, Bartelmez SH, Poppa V, Bradford G, Dowell JD, Williams DA, Field LJ. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature. 2004;428:664-668.
32. Boheler KR, Czyz J, Tweedie D, Yang HT, Anisimov SV, Wobus AM. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res. 2002;91:189-201.
33. Muller M, Fleischmann BK, Selbert S, Ji GJ, Endl E, Middeler G, Muller OJ, Schlenke P, Frese S, Wobus AM, Hescheler J, Katus HA, Franz WM. Selection of ventricular-like cardiomyocytes from ES cells in vitro. FASEB J. 2000;14:2540-2548.
34. Hassink RJ, Dowell JD, Brutel de la Riviere A, Doevendans PA, Field LJ. Stem cell therapy for ischemic heart disease. Trends Mol Med. 2003;9: 436-441.
35. Miake J, Marban E, Nuss HB. Biological pacemaker created by gene transfer. Nature. 2002;419:132-133.
36. Qu J, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Cohen IS, Robinson RB, Rosen MR. Expression and function of a biological pacemaker in canine heart. Circulation. 2003;107:1106-1109.
37. Potapova I, Plotnikov A, Lu Z, Danilo P Jr, Valiunas V, Qu J, Doronin S, Zuckerman J, Shlapakova IN, Gao J, Pan Z, Herron AJ, Robinson RB, Brink PR, Rosen MR, Cohen IS. Human mesenchymal stem cells as a gene delivery system to create cardiac pacemakers. Circ Res. 2004;94: 952-959.
38. Tsang, SY, Lesso, H, Li RA. Dissecting the structural and functional roles of the S3-S4 linker of pacemaker (HCN) channels by systematic length alterations. J Biol Chem. 2004;279:43752-43759.
39. Xue T, Cho HC, Li RA. Induction of ventricular automaticity by over-expression of an engineered HCN1 construct. Biophys J. In press.