Cardiac repair by embryonic stem-derived cells

Handbook of Experimental Pharmacology

Volumn 174, Issue , 2006, Pages 73-100

  Rubart, M ^a   Field, L J ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac regeneration; Cardiomyocytes; Cell transplantation; Embryonic stem cell; Heart disease

Indexed keywords

EID: 85099485887     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/3-540-31265-x_4     Document Type: Article

References (124)

1. Agbulut O, Menot ML, Li Z, Marotte F, Paulin D, Hagege AA, Chomienne C, Samuel JL, Menasche P (2003) Temporal patterns of bone marrow cell differentiation following transplantation in doxorubicin-induced cardiomyopathy. Cardiovasc Res 58:451-459
2. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A (2003) Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425:968-973
3. Anversa P, Kajstura J (1998) Ventricular myocytes are not terminally differentiated in the adult mammalian heart. Circ Res 83:1-14
4. Anversa P, Nadal-Ginard B (2002) Myocyte renewal and ventricular remodelling. Nature 415:240-243
5. Arceci RJ, King AA, Simon MC, Orkin SH, Wilson DB (1993) Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol Cell Biol 13:2235-2246
6. Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grunwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM (2002) Transplantation of progenitor cells and regeneration enhancement in acutemyocardial infarction (TOPCAREAMI) . Circulation 106:3009-3017
7. Bader A, Al-DubaiH, Weitzer G (2000) Leukemia inhibitory factor modulates cardiogenesis in embryoid bodies in opposite fashions. Circ Res 86:787-794
8. Bader A, Gruss A, Hollrigl A, Al-Dubai H, Capetanaki Y, Weitzer G (2001) Paracrine promotion of cardiomyogenesis in embryoid bodies by LIF modulated endoderm. Differentiation 68:31-43
9. Balsam LB, WagersAJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC (2004) Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428:668-673
10. Banach K, HalbachMD, Hu P, Hescheler J, Egert U (2003) Development of electrical activity in cardiac myocyte aggregates derived from mouse embryonic stem cells. Am J Physiol Heart Circ Physiol 284:H2114-H2123
11. Behfar A, Zingman LV, Hodgson DM, Rauzier JM, Kane GC, Terzic A, PuceatM (2002) Stem cell differentiation requires a paracrine pathway in the heart. FASEB J 16:1558-1566
12. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763-776
13. Bittner RE, Schofer C, Weipoltshammer K, Ivanova S, Streubel B, Hauser E, Freilinger M, Hoger H, Elbe-Burger A, Wachtler F (1999) Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice. Anat Embryol (Berl) 199:391-396
14. Bock-Marquette I, Saxena A, WhiteMD, Dimaio JM, SrivastavaD (2004) Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 432:466-472
15. Boheler KR, Czyz J, Tweedie D, Yang HT, Anisimov SV, Wobus AM (2002) Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res 91:189-201
16. Caspi O, Gepstein L (2004) Potential applications of human embryonic stem cell-derived cardiomyocytes. Ann N Y Acad Sci 1015:285-298
17. Czyz J, Wobus A (2001) Embryonic stem cell differentiation: the role of extracellular factors. Differentiation 68:167-174
18. Dang SM, Kyba M, Perlingeiro R, Daley GQ, Zandstra PW (2002) Efficiency of embryoid body formation and hematopoietic development fromembryonic stem cells in different culture systems. Biotechnol Bioeng 78:442-453
19. Dang SM, Gerecht-Nir S, Chen J, Itskovitz-Eldor J, Zandstra PW (2004) Controlled, scalable embryonic stem cell differentiation culture. Stem Cells 22:275-282
20. Dell'Era P, Ronca R, Coco L, Nicoli S, Metra M, Presta M (2003) Fibroblast growth factor receptor-1 is essential for in vitro cardiomyocyte development. Circ Res 93:414-420
21. Doetschman TC, Eistetter H, Katz M, SchmidtW, Kemler R (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87:27-45
22. Doevendans PA, Kubalak SW, An RH, Becker DK, Chien KR, Kass RS (2000) Differentiation of cardiomyocytes in floating embryoid bodies is comparable to fetal cardiomyocytes. J Mol Cell Cardiol 32:839-851
23. Dowell JD, Field LJ, Pasumarthi KB (2003a) Cell cycle regulation to repair the infarcted myocardium. Heart Fail Rev 8:293-303
24. Dowell JD, Rubart M, Pasumarthi KB, Soonpaa MH, Field LJ (2003b) Myocyte andmyogenic stem cell transplantation in the heart. Cardiovasc Res 58:336-350
25. Fassler R, Rohwedel J, Maltsev V, Bloch W, Lentini S, Guan K, Gullberg D, Hescheler J, Addicks K, Wobus AM (1996) Differentiation and integrity of cardiac muscle cells are impaired in the absence of beta 1 integrin. J Cell Sci 109:2989-2999
26. Fijnvandraat AC, Lekanne Deprez RH, Christoffels VM, Ruijter JM, Moorman AF (2003a) TBX5 overexpression stimulates differentiation of chambermyocardiumin P19C16 embryonic carcinoma cells. J Muscle Res Cell Motil 24:211-218
27. Fijnvandraat AC, van Ginneken AC, de Boer PA, Ruijter JM, Christoffels VM, Moorman AF, Lekanne Deprez RH (2003b) Cardiomyocytes derived fromembryonic stem cells resemble cardiomyocytes of the embryonic heart tube. Cardiovasc Res 58:399-409
28. Fijnvandraat AC, van Ginneken AC, Schumacher CA, Boheler KR, Lekanne Deprez RH, Christoffels VM, Moorman AF (2003c) Cardiomyocytes purified from differentiated embryonic stem cells exhibit characteristics of early chamber myocardium. J Mol Cell Cardiol 35:1461-1472
29. Gajovic S, St-Onge L, Yokota Y, Gruss P (1997) Retinoic acid mediates Pax6 expression during in vitro differentiation of embryonic stem cells. Differentiation 62:187-192
30. Grepin C, Nemer G, Nemer M (1997) Enhanced cardiogenesis in embryonic stem cells overexpressing the GATA-4 transcription factor. Development 124:2387-2395
31. Guan K, Furst DO, Wobus AM (1999) Modulation of sarcomere organization during embryonic stem cell-derived cardiomyocyte differentiation. Eur J Cell Biol 78:813-823
32. Hagege AA, Carrion C, Menasche P, Vilquin JT, DubocD, Marolleau JP, Desnos M, Bruneval P (2003) Viability and differentiation of autologous skeletal myoblast grafts in ischaemic cardiomyopathy. Lancet 361:491-492
33. Hassink RJ, Dowell JD, Brutel de la Riviere A, Doevendans PA, Field LJ (2003) Stem cell therapy for ischemic heart disease. Trends Mol Med 9:436-441
34. He JQ, Ma Y, Lee Y, Thomson JA, Kamp TJ (2003) Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res 93:32-39
35. Herreros J, Prosper F, Perez A, Gavira JJ, Garcia-Velloso MJ, Barba J, Sanchez PL, Canizo C, Rabago G, Marti-Climent JM, Hernandez M, Lopez-Holgado N, Gonzalez-Santos JM, Martin-Luengo C, Alegria E (2003) Autologous intramyocardial injection of cultured skeletalmuscle-derived stem cells in patients with non-acutemyocardial infarction. Eur Heart J 24:2012-2020
36. Hidaka K, Lee JK, Kim HS, Ihm CH, Iio A, Ogawa M, Nishikawa S, Kodama I, Morisaki T (2003) Chamber-specific differentiation of Nkx2.5-positive cardiac precursor cells from murine embryonic stem cells. FASEB J 17:740-742
37. Hierlihy AM, Seale P, Lobe CG, Rudnicki MA, Megeney LA (2002) The post-natal heart contains a myocardial stem cell population. FEBS Lett 530:239-243
38. Hodgson DM, Behfar A, Zingman LV, Kane GC, Perez-Terzic C, Alekseev AE, Puceat M, Terzic A (2004) Stable benefit of embryonic stem cell therapy in myocardial infarction. Am J Physiol Heart Circ Physiol 287:H471-H479
39. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, MajeskyMW, EntmanML, Michael LH, Hirschi KK, Goodell MA (2001) Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107:1395-1402
40. Johkura K, Cui L, SuzukiA, TengR, KamiyoshiA, Okamura S, Kubota S, Zhao X, Asanuma K, Okouchi Y, Ogiwara N, Tagawa Y, Sasaki K (2003) Survival and function of mouse embryonic stem cell-derived cardiomyocytes in ectopic transplants. Cardiovasc Res 58:435-443
41. Kajstura J, Leri A, FinatoN, DiLoretoC, Beltrami CA, AnversaP (1998) Myocyteproliferation in end-stage cardiac failure in humans. Proc Natl Acad Sci U S A 95:8801-8805
42. Kanno S, Kim PK, Sallam K, Lei J, Billiar TR, Shears LL, 2nd (2004) Nitric oxide facilitates cardiomyogenesis in mouse embryonic stem cells. Proc Natl Acad Sci U S A 101:12277-12281
43. Kawai T, Takahashi T, EsakiM, Ushikoshi H, Nagano S, Fujiwara H, Kosai K (2004) Efficient cardiomyogenic differentiation of embryonic stem cell by fibroblast growth factor 2 and bone morphogenetic protein 2. Circ J 68:691-702
44. Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, Livne E, Binah O, Itskovitz-Eldor J, Gepstein L (2001) Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108:407-414
45. Kehat I, Khimovich L, Caspi O, Gepstein A, Shofti R, Arbel G, Huber I, Satin J, Itskovitz-Eldor J, Gepstein L (2004) Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 22:1282-1289
46. Klug MG, Soonpaa MH, Field LJ (1995) DNA synthesis and multinucleation in embryonic stem cell-derived cardiomyocytes. Am J Physiol 269:H1913-H1921
47. Klug MG, Soonpaa MH, Koh GY, Field LJ (1996) Genetically selected cardiomyocytes from differentiating embryonic stemcells formstable intracardiac grafts. J Clin Invest 98:216-224
48. Kofidis T, de Bruin JL, Hoyt G, Lebl DR, Tanaka M, Yamane T, Chang CP, Robbins RC (2004) Injectable bioartificial myocardial tissue for large-scale intramural cell transfer and functional recovery of injured heart muscle. J Thorac Cardiovasc Surg 128:571-578
49. Koh GY, Klug MG, Soonpaa MH, Field LJ (1993a) Differentiation and long-term survival of C2C12 myoblast grafts in heart. J Clin Invest 92:1548-1554
50. KohGY, SoonpaaMH, Klug MG, Field LJ (1993b) Long-termsurvival ofAT-1 cardiomyocyte grafts in syngeneic myocardium. Am J Physiol 264:H1727-H1733
51. Koh GY, Soonpaa MH, Klug MG, Pride HP, Cooper BJ, Zipes DP, Field LJ (1995) Stable fetal cardiomyocyte grafts in the hearts of dystrophic mice and dogs. J Clin Invest 96:2034-2042
52. Kolossov E, Fleischmann BK, Liu Q, Bloch W, Viatchenko-Karpinski S, Manzke O, Ji GJ, Bohlen H, Addicks K, Hescheler J (1998) Functional characteristics of ES cell-derived cardiac precursor cells identified by tissue-specific expression of the green fluorescent protein. J Cell Biol 143:2045-2056
53. Leobon B, Garcin I, Menasche P, Vilquin JT, Audinat E, Charpak S (2003) Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc Natl Acad Sci U S A 100:7808-7811
54. Maltsev VA, Rohwedel J, Hescheler J, Wobus AM (1993) Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech Dev 44:41-50
55. Mangi AA, Noiseux N, Kong D, He H, Rezvani M, Ingwall JS, Dzau VJ (2003) Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 9:1195-1201
56. Martin CM, Meeson AP, Robertson SM, Hawke TJ, Richardson JA, Bates S, Goetsch SC, Gallardo TD, Garry DJ (2004) Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev Biol 265:262-275
57. Menasche P, Hagege AA, Vilquin JT, Desnos M, Abergel E, Pouzet B, Bel A, Sarateanu S, Scorsin M, Schwartz K, Bruneval P, Benbunan M, Marolleau JP, Duboc D (2003) Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J Am Coll Cardiol 41:1078-1083
58. Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, Salio M, Battaglia M, LatronicoMV, Coletta M, Vivarelli E, Frati L, Cossu G, Giacomello A (2004) Isolation and expansion of adult cardiac stem cells fromhuman andmurine heart. Circ Res 95:911-921
59. Miller-Hance WC, LaCorbiere M, Fuller SJ, Evans SM, Lyons G, Schmidt C, Robbins J, Chien KR (1993) In vitro chamber specification during embryonic stem cell cardiogenesis. Expression of the ventricularmyosin light chain-2 gene is independent of heart tube formation. J Biol Chem 268:25244-25252
60. Min JY, Yang Y, Converso KL, Liu L, Huang Q, Morgan JP, Xiao YF (2002) Transplantation of embryonic stem cells improves cardiac function in postinfarcted rats. J Appl Physiol 92:288-296
61. Morali OG, Jouneau A, McLaughlin KJ, Thiery JP, Larue L (2000) IGF-II promotes mesoderm formation. Dev Biol 227:133-145
62. Muller-Ehmsen J, Peterson KL, Kedes L, Whittaker P, Dow JS, Long TI, LairdPW, Kloner RA (2002) Rebuilding a damaged heart: long-term survival of transplanted neonatal rat cardiomyocytes after myocardial infarction and effect on cardiac function. Circulation 105:1720-1726
63. Mummery C, Ward D, van den Brink CE, Bird SD, Doevendans PA, Opthof T, Brutel de la Riviere A, Tertoolen L, van der Heyden M, PeraM (2002) Cardiomyocyte differentiation of mouse and human embryonic stem cells. J Anat 200:233-242
64. 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 (2003) Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107:2733-2740
65. Murry CE, Wiseman RW, Schwartz SM, Hauschka SD (1996) Skeletal myoblast transplantation for repair of myocardial necrosis. J Clin Invest 98:2512-2523
66. Murry CE, SoonpaaMH, ReineckeH, Nakajima H, NakajimaHO, RubartM, Pasumarthi KB, Virag JI, Bartelmez SH, Poppa V, Bradford G, Dowell JD, Williams DA, Field LJ (2004) Haematopoietic stem cells do not transdifferentiate into cardiacmyocytes inmyocardial infarcts. Nature 428:664-668
67. NaitoH, NishizakiK, YoshikawaM, YamadaT, SatohH, Nagasaka S, KijiT, Taniguchi S (2004) Xenogeneic embryonic stem cell-derived cardiomyocyte transplantation. Transplant Proc 36:2507-2508
68. Nakajima H, Nakajima HO, Tsai SC, Field LJ (2004) Expression of mutant p193 and p53 permits cardiomyocyte cell cycle reentry aftermyocardial infarction in transgenic mice. Circ Res 94:1606-1614
69. Nygren JM, Jovinge S, Breitbach M, Sawen P, RollW, Hescheler J, Taneera J, Fleischmann BK, Jacobsen SE (2004) Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. NatMed 10:494-501
70. Odorico JS, Kaufman DS, Thomson JA (2001) Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19:193-204
71. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, Schneider MD (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100:12313-12318
72. Orlic D, Kajstura J, Chimenti S, Bodine DM, Leri A, Anversa P (2001a) Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann N Y Acad Sci 938:221-229; discussion 229-230
73. Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine DM, Leri A, Anversa P (2001b) Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A 98:10344-10349
74. Pagani FD, DerSimonian H, Zawadzka A, Wetzel K, Edge AS, Jacoby DB, Dinsmore JH, Wright S, Aretz TH, Eisen HJ, Aaronson KD (2003) Autologous skeletalmyoblasts transplanted to ischemia-damaged myocardium in humans. Histological analysis of cell survival and differentiation. J Am Coll Cardiol 41:879-888
75. Pandur P, Lasche M, Eisenberg LM, Kuhl M (2002) Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418:636-641
76. Paquin J, Danalache BA, Jankowski M, McCann SM, Gutkowska J (2002) Oxytocin induces differentiation of P19 embryonic stem cells to cardiomyocytes. Proc Natl Acad Sci U S A 99:9550-9555
77. Parisi S, D'Andrea D, Lago CT, Adamson ED, Persico MG, Minchiotti G (2003) Nodaldependent Cripto signaling promotes cardiomyogenesis and redirects the neural fate of embryonic stem cells. J Cell Biol 163:303-314
78. Pasumarthi KB, Field LJ (2002) Cardiomyocyte cell cycle regulation. Circ Res 90:1044-1054
79. Pasumarthi KB, Nakajima H, Nakajima HO, Soonpaa MH, Field LJ (2005) Targeted expression of cyclin D2 results in cardiomyocyte DNA synthesis and infarct regression in transgenic mice. Circ Res 96:110-118
80. Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Carvalho AC, Dutra HS, Dohmann HJ, Silva GV, Belem L, Vivacqua R, Rangel FO, EsporcatteR, Geng YJ, VaughnWK, Assad JA, Mesquita ET, Willerson JT (2003) Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 107:2294-2302
81. Puceat M, Travo P, Quinn MT, Fort P (2003) A dual role of the GTPase Rac in cardiac differentiation of stem cells. Mol Biol Cell 14:2781-2792
82. Reinecke H, Minami E, Poppa V, Murry CE (2004) Evidence for fusion between cardiac and skeletal muscle cells. Circ Res 94:e56-e60
83. Reinlib L, Field L (2000) Cell transplantation as future therapy for cardiovascular disease?: Aworkshop of theNationalHeart, Lung, and Blood Institute. Circulation 101:E182-E187
84. RoellW, Lu ZJ, BlochW, 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 (2002) Cellular cardiomyoplasty improves survival after myocardial injury. Circulation 105:2435-2441
85. Rubart M, Pasumarthi KB, Nakajima H, Soonpaa MH, Nakajima HO, Field LJ (2003a) Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ Res 92:1217-1224
86. Rubart M, Wang E, Dunn KW, Field LJ (2003b) Two-photon molecular excitation imaging of Ca2+ transients in Langendorff-perfused mouse hearts. Am J Physiol Cell Physiol 284:C1654-C1668
87. Rubart M, SoonpaaMH, Nakajima H, Field LJ (2004) Spontaneous and evoked intracellular calcium transients in donor-derived myocytes following intracardiac myoblast transplantation. J Clin Invest 114:775-783
88. Rudnicki MA, Jackowski G, Saggin L, McBurney MW (1990) Actin and myosin expression during development of cardiac muscle from cultured embryonal carcinoma cells. Dev Biol 138:348-358
89. Rudy-Reil D, Lough J (2004) Avian precardiac endoderm/mesoderm induces cardiac myocyte differentiation in murine embryonic stem cells. Circ Res 94:e107-e116
90. Rumiantsev PP (1991) Growth and hyperplasia of cardiacmuscle cells. Harwood Academic, London
91. Sachinidis A, Gissel C, Nierhoff D, Hippler-Altenburg R, Sauer H, Wartenberg M, Hescheler J (2003) Identification of plateled-derived growth factor-BB as cardiogenesis-inducing factor inmouseembryonic stemcells under serum-free conditions.Cell Physiol Biochem 13:423-429
92. Satin J, Kehat I, Caspi O, Huber I, Arbel G, Itzhaki I, Magyar J, Schroder EA, Perlman I, Gepstein L (2004) Mechanism of spontaneous excitability in human embryonic stem cell derived cardiomyocytes. J Physiol 559:479-496
93. Sauer H, Rahimi G, Hescheler J, Wartenberg M (2000) Role of reactive oxygen species and phosphatidylinositol 3-kinase in cardiomyocyte differentiation of embryonic stem cells. FEBS Lett 476:218-223
94. Sauer H, NeukirchenW, Rahimi G, Grunheck F, Hescheler J, Wartenberg M (2004) Involvement of reactive oxygen species in cardiotrophin-1-induced proliferation of cardiomyocytes differentiated from murine embryonic stem cells. Exp Cell Res 294:313-324
95. Schmidt MM, Guan K, Wobus AM (2001) Lithium influences differentiation and tissuespecific gene expression of mouse embryonic stem (ES) cells in vitro. Int J Dev Biol 45:421-429
96. SchroederM, Niebruegge S, WernerA, WillboldE, BurgM, RuedigerM, FieldLJ, LehmannJ, Zweigerdt R, Embryonic Stem Cell Differentiation and Lineage Selection in a Stirred Bench Scale Bioreactor with Automated Process Control. Biotechnol and Bioengin, in press
97. Smits PC, van Geuns RJ, Poldermans D, Bountioukos M, Onderwater EE, Lee CH, Maat AP, Serruys PW (2003) Catheter-based intramyocardial injection of autologous skeletal myoblasts as a primary treatment of ischemic heart failure: clinical experience with sixmonth follow-up. J Am Coll Cardiol 42:2063-2069
98. Snir M, Kehat I, Gepstein A, Coleman R, Itskovitz-Eldor J, Livne E, Gepstein L (2003) Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. Am J Physiol Heart Circ Physiol 285:H2355-H2363
99. Soonpaa MH, Field LJ (1994) Assessment of cardiomyocyte DNA synthesis during hypertrophy in adult mice. Am J Physiol 266:H1439-H1445
100. SoonpaaMH, Field LJ (1998) Survey of studies examining mammalian cardiomyocyte DNA synthesis. Circ Res 83:15-26
101. Soonpaa MH, Koh GY, Klug MG, Field LJ (1994) Formation of nascent intercalated disks between grafted fetal cardiomyocytes and host myocardium. Science 264:98-101
102. Steinhelper ME, Lanson NA Jr, Dresdner KP, Delcarpio JB, Wit AL, Claycomb WC, Field LJ (1990) Proliferation in vivo and in culture of differentiated adult atrial cardiomyocytes from transgenic mice. Am J Physiol 259:H1826-H1834
103. Sudou A, Muramatsu H, Kaname T, Kadomatsu K, Muramatsu T (1997) Le (X) structure enhances myocardial differentiation from embryonic stem cells. Cell Struct Funct 22:247-251
104. Takahashi T, Lord B, Schulze PC, Fryer RM, Sarang SS, Gullans SR, Lee RT (2003) Ascorbic acid enhances differentiation of embryonic stem cells into cardiacmyocytes. Circulation 107:1912-1916
105. Taylor DA, Atkins BZ, Hungspreugs P, Jones TR, Reedy MC, Hutcheson KA, Glower DD, Kraus WE (1998) Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat Med 4:929-933
106. Terami H, HidakaK, Katsumata T, IioA, Morisaki T (2004) Wnt11 facilitates embryonic stem cell differentiation to Nkx2.5-positive cardiomyocytes. Biochem Biophys Res Commun 325:968-975
107. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stemcell lines derived fromhumanblastocysts. Science 282:1145-1147
108. Ventura C, Maioli M (2000) Opioid peptide gene expression primes cardiogenesis in embryonal pluripotent stem cells. Circ Res 87:189-194
109. Ventura C, Zinellu E, Maninchedda E, Fadda M, MaioliM (2003) Protein kinase C signaling transduces endorphin-primed cardiogenesis in GTR1 embryonic stem cells. Circ Res 92:617-622
110. Ventura C, Maioli M, Asara Y, Santoni D, Scarlata I, Cantoni S, Perbellini A (2004) Butyric and retinoic mixed ester of hyaluronan. A novel differentiating glycoconjugate affording ahigh throughput of cardiogenesis inembryonic stemcells. JBiolChem279:23574-23579
111. Wang JF, Yang Y, Wang G, Min J, Sullivan MF, Ping P, Xiao YF, Morgan JP (2002) Embryonic stem cells attenuate viral myocarditis in murine model. Cell Transplant 11:753-758
112. Winnier G, Blessing M, Labosky PA, Hogan BL (1995) Bone morphogenetic protein-4 is required formesodermformation and patterning in themouse. Genes Dev 9:2105-2116
113. Wobus AM, Kaomei G, Shan J, Wellner MC, Rohwedel J, Ji G, Fleischmann B, Katus HA, Hescheler J, Franz WM (1997) Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J Mol Cell Cardiol 29:1525-1539
114. Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D, Arseniev L, Hertenstein B, Ganser A, Drexler H (2004) Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 364:141-148
115. Wu X, Ding S, Ding Q, Gray NS, Schultz PG (2004) Small molecules that induce cardiomyogenesis in embryonic stem cells. J Am Chem Soc 126:1590-1591
116. Xu C, Police S, Rao N, CarpenterMK (2002) Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 91:501-508
117. XueT, ChoHC, Akar FG, Tsang SY, Jones SP, Marban E, TomaselliGF, LiRA (2005) 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 111:11-20
118. Yang Y, Min JY, Rana JS, Ke Q, Cai J, Chen Y, Morgan JP, Xiao YF (2002) VEGF enhances functional improvement of postinfarcted hearts by transplantation of ESC-differentiated cells. J Appl Physiol 93:1140-1151
119. Yao M, Dieterle T, Hale SL, Dow JS, Kedes LH, Peterson KL, Kloner RA (2003) Longtermoutcome of fetal cell transplantation on postinfarction ventricular remodeling and function. J Mol Cell Cardiol 35:661-670
120. Zandstra PW, Bauwens C, Yin T, Liu Q, Schiller H, Zweigerdt R, Pasumarthi KB, Field LJ (2003) Scalable production of embryonic stem cell-derived cardiomyocytes. Tissue Eng 9:767-778
121. Zhang M, MethotD, PoppaV, Fujio Y, Walsh K, Murry CE (2001) Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J Mol Cell Cardiol 33:907-921
122. ZimmermannWH, Schneiderbanger K, Schubert P, Didie M, Munzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T (2002) Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90:223-230
123. Zweigerdt R, Burg M, Willbold E, Abts H, Ruediger M (2003a) Generation of confluent cardiomyocyte monolayers derived from embryonic stem cells in suspension: a cell source for new therapies and screening strategies. Cytotherapy 5:399-413
124. Zweigerdt R, Schroeder M, Werner A, Lehmann J, Zandstra PW, Field LJ, Abts H, Ruediger M, BurgM (2003b) Clinical scale generation of enriched embryonic stem cell derived cardiomyocytes (abstract 3083) . In: Keystone Symposia: From Stem Cells to Therapy, Steamboat Springs, CO, pp 136