Physiological differences between transplanted and host tissue cause functional decoupling after in vitro transplantation of human embryonic stem cell-derived cardiomyocytes

Cellular Physiology and Biochemistry

Volumn 23, Issue 1-3, 2009, Pages 65-74

  Pillekamp, Frank ^a   Halbach, Marcel ^a   Reppel, Michael ^a   Pfannkuche, Kurt ^a   Nazzal, Rewa ^a   Nguemo, Filomain ^a   Matzkies, Matthias ^a   Rubenchyk, Olga ^a   Hannes, Tobias ^a   Khalil, Markus ^a   Bloch, Wilhelm ^b   Sreeram, Narayanswami ^a   Brockmeier, Konrad ^a   Hescheler, Juergen ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b GERMAN SPORT UNIVERSITY COLOGNE   (Germany)

Author keywords

Action potentials; Arrhythmia; Beta adrenergic agonists; Cardiac myocyte; Electrophysiology; Engraftment; Human embryonic stem cells; Xenogeneic stem cell transplantation

Indexed keywords

CONNEXIN 43; HEPTANOL;

ANIMAL TISSUE; ARTICLE; BETA ADRENERGIC STIMULATION; CELL INTERACTION; CELL STRUCTURE; ELECTROPHYSIOLOGY; EMBRYONIC STEM CELL; GAP JUNCTION; HEART ARRHYTHMIA; HEART MUSCLE CELL; HEART PACING; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION;

MURINAE;

EID: 60549092108     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000204093     Document Type: Article

References (36)

1. Roell W, Lu ZJ, Bloch W, Siedner S, Tiemann K, Xia Y, Stoecker E, Fleischmann M, Bohlen H, Stehle R, Kolossov E, Brem G, Addicks K, Pfitzer G, Welz A, Hescheler J, Fleischmann BK: Cellular cardiomyoplasty improves survival after myocardial injury. Circulation 2002;105:2435-2441.
2. Kolossov E, Bostani T, Roell W, Breitbach M, Pillekamp F, Nygren JM, Sasse P, Rubenchik O, Fries JW, Wenzel D, Geisen C, Xia Y, Lu Z, Duan Y, Kettenhofen R, Jovinge S, Bloch W, Bohlen H, Welz A, Hescheler J, Jacobsen SE, Fleischmann BK: Engraftment of engineered ES cell-derived cardiomyocytes but not BM cells restores contractile function to the infarcted myocardium. J Exp Med 2006;203:2315-2327.
3. Murry CE, Field LJ, Menasche P: Cell-based cardiac repair: reflections at the 10-year point. Circulation 2005;112:3174-3183.
4. 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(5391):1145-1147.
5. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA: Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917-1920.
6. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S: Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
7. Kehat I, Khimovich L, Caspi O, Gepstein A, Shofti R, Arbel G, Huber I, Satin J, Itskovitz-Eldor J, Gepstein L: Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 2004;22:1282-1289.
8. Snir M, Kehat I, Gepstein A, Coleman R, Itskovitz-Eldor J, Livne E, Gepstein L: Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. Am J Physiol Heart Circ Physiol 2003; 285:2355-2363.
9. 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.
10. Reppel M, Boettinger C, Hescheler J: Beta-adrenergic and muscarinic modulation of human embryonic stem cell-derived cardiomyocytes. Cell Physiol Biochem 2004;14:187-196.
11. 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 2004;559:479-496.
12. Pillekamp F, Reppel M, Rubenchyk O, Pfannkuche K, Matzkies M, Bloch W, Sreeram N, Brockmeier K, Hescheler J: Force measurements of human embryonic stem cell-derived cardiomyocytes in an in vitro transplantation model. Stem Cells 2007;25:174-180.
13. Leobon B, Garcin I, Menasche P, Vilquin JT, Audinat E, Charpak S: Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc Natl Acad Sci U SA 2003;100:7808-7811.
14. Fernandes S, Amirault JC, Lande G, Nguyen JM, Forest V, Bignolais O, Lamirault G, Heudes D, Orsonneau JL, Heymann MF, Charpentier F, Lemarchand P: Autologous myoblast transplantation after myocardial infarction increases the inducibility of ventricular arrhythmias. Cardiovasc Res 2006;69:348-358.
15. 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.
16. Rubart M: Two-photon microscopy of cells and tissue. Circ Res 2004;95:1154-1166.
17. Pillekamp F, Reppel M, Dinkelacker V, Duan Y, Jazmati N, Bloch W, Brockmeier K, Hescheler J, Fleischmann BK, Koehling R: Establishment and characterization of a mouse embryonic heart slice preparation. Cell Physiol Biochem 2005;16:127-132.
18. 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.
19. Passier R, Oostwaard DW, Snapper J, Kloots J, Hassink RJ, Kuijk E, Roelen B, de la Riviere AB, Mummery C: Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells 2005;23:772-780.
20. Pillekamp F, Reppel M, Brockmeier K, Hescheler J: Impulse propagation in late-stage embryonic and neonatal murine ventricular slices. J Electrocardiol 2006;39:425.e1-4.
21. Robinson RB: Autonomic receptor-effector coupling during post-natal development. Cardiovasc Res 1996;31:E68-76.
22. Xue T, Cho HC, Akar FG, Tsang SY, Jones SP, Marbán E, Tomaselli GF, Li RA: 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 2005;111:11-20.
23. Ypey DL, Clapham DE, De Haan RL: Development of electrical coupling and action potential synchrony between paired aggregated of embryonic heart cells. Membr Biol 1979;51;75-96.
24. Hannes T, Halbach M, Nazzal R, Frenzel L, Saric T, Khalil M, Hescheler J, Brockmeier K, Pillekamp F: Biological pacemakers: characterization in an in vitro coculture model. J Electrocardiol 2008;41:562-566.
25. Trautwein W, Uchizono K: Electron microscopic and electrophysiologic study of the pacemaker in the sino-atrial node of the rabbit heart. Z Zellforsch Mikrosk Anat 1963;61:96-109.
26. Camelliti P, Green CR, LeGrice I, Kohl P: Fibroblast network in rabbit sinoatrial node. Structural and functional identification of homogenous and heterogenous cell coupling. Circ Res 2004;94:828-835.
27. Gaudesius G, Miragoli M, Thomas SP, Rohr S: Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin. Circ Res 2003;93:421-428.
28. Fahrenbach JP, Meija-Alvarez R, Banach K: The relevance of non-excitable cells for cardiac pacemaker function. J Physiol 2007;585:565-578.
29. 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;25:1136-1144.
30. Lipshultz S, Shanfield J, Chacko S: Emergence of beta-adrenergic sensitivity in the developing chicken heart. Proc Natl Acad Sci USA 1981;78:288-292.
31. Antzelevitch C: Basic mechanisms of reentrant arrhythmias. Curr Opin Cardiol 2001;16:1-7.
32. Ji GJ, Fleischmann BK, Bloch W, Feelisch M, Andressen C, Addicks K, Hescheler J: Regulation of the L-type Ca2+ channel during cardiomyogenesis: switch from NO to adenylyl cyclase-mediated inhibition. FASEB J 1999;13:313-324.
33. Naebauer M, Beuckelmann DJ, Uberfuhr P, Steinbeck G: Regional differences in current density and rate-dependent properties of the transient outward current in subepicardial and subendocardial myocytes of human left ventricle. Circulation 1996;93:168-177.
34. Wang Y, Cheng J, Joyner RW, Wagner MB, Hill JA: Remodeling of early-phase repolarization: a mechanism of abnormal impulse conduction in heart failure. Circulation 2006;113:1849-1856.
35. Hasenfuss G: Animal models of human cardiovascular disease, heart failure and hypertrophy. Cardiovasc Res 1998;39:60-76.
36. 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.