Stem cells for cardiac repair: An introduction

Journal of Geriatric Cardiology

Volumn 10, Issue 2, 2013, Pages 186-197

  Du Pré, Bastiaan C ^a   Doevendans, Pieter A ^a,b   Van Laake, Linda W ^a,c  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

^c HUBRECHT INSTITUTE   (Netherlands)

Author keywords

Cardiomyocytes; Heart; Regeneration; Stem cell

Indexed keywords

ADULT STEM CELL; CARDIOMYOPATHY; CELL DIFFERENTIATION; DNA MODIFICATION; EMBRYONIC STEM CELL; GAP JUNCTION; GRAFT REJECTION; HEART ELECTROPHYSIOLOGY; HEART FUNCTION; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE CELL; HEART MUSCLE REGENERATION; HEART MUSCLE REVASCULARIZATION; HEMATOPOIETIC STEM CELL; HUMAN; IN VITRO STUDY; ISCHEMIC CARDIOMYOPATHY; ISCHEMIC HEART DISEASE; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; MUSCLE REGENERATION; NONHUMAN; PERCUTANEOUS CORONARY INTERVENTION; PLURIPOTENT STEM CELL; REGULATORY T LYMPHOCYTE; REVIEW; STEM CELL TRANSPLANTATION; T LYMPHOCYTE;

EID: 84883268465     PISSN: 16715411     EISSN: None     Source Type: Journal    
DOI: 10.3969/j.issn.1671-5411.2013.02.003     Document Type: Review

References (116)

1. Lenhoff S, Lenhoff H. Hydra and the birth of experimental biology, 1744: Abraham Trembley's Memoirs concerning the natural history of a type of freshwater polyp with arms shaped like horns; Boxwood Press: Pacific Grove, California, USA, 1986.
2. Spallanzani L. Prodromo di un opera da imprimersi sopra la riproduzioni animali (An essay on animal reproduction); T. Becket & de Hondt: London, UK, 1769.
3. Higgins G, Anderson R. Experimental pathology of the liver. I. Restoration of the liver of the white rat following partial surgical removal. Arch Pathol 1933; 12: 186-202.
4. Schram G, Pourrier M, Melnyk P, et al. Differential distribution of cardiac ion channel expression as a basis for regional specialization in electrical function. Circ Res 2002; 90: 939-950. (Pubitemid 34633859)
5. Chien KR, Domian IJ, Parker KK. Cardiogenesis and the complex biology of regenerative cardiovascular medicine. Science 2008; 322: 1494-1497.
6. Gherghiceanu M, Popescu LM. Cardiomyocyte precursors and telocytes in epicardial stem cell niche: electron microscope images. J Cell Mol Med 2010; 14: 871-877.
7. He JQ, Ma Y, Lee Y, et al. Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res 2003; 93: 32-39. (Pubitemid 36859038)
8. Wong SS, Bernstein HS. Cardiac regeneration using human embryonic stem cells: producing cells for future therapy. Regen Med 2010; 5: 763-775.
9. Dierickx P, Doevendans PA, Geijsen N, et al. Embryonic Template-Based Generation and Purification of Pluripotent Stem Cell-Derived Cardiomyocytes for Heart Repair. J Cardiovasc Transl Res 2012; 5: 566-580.
10. Segers VF, Lee RT. Stem-cell therapy for cardiac disease. Nature 2008; 451: 937-942. (Pubitemid 351301749)
11. Segers VF, Lee RT. Biomaterials to enhance stem cell function in the heart. Circ Res 2011; 109: 910-922.
12. Hsieh PC, Segers VF, Davis ME, et al. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 2007; 13: 970-974. (Pubitemid 47222045)
13. Rodrigo SF, van Ramshorst J, Beeres SL, et al. Intramyocardial injection of bone marrow mononuclear cells in chronic myocardial ischemia patients after previous placebo injection improves myocardial perfusion and anginal symptoms: an intra-patient comparison. Am Heart J 2012; 164: 771-778.
14. Madonna R, Geng YJ, De Caterina R. Adipose tissue-derived stem cells: characterization and potential for cardiovascular repair. Arterioscler Thromb Vasc Biol 2009; 29: 1723-1729.
15. Houtgraaf JH, Dejong R, Monkhorst K, et al. Feasibility of intracoronary GLP-1 eluting CellBead infusion in acute myocardial infarction. Cell Transplant 2012; 22: 535-543.
16. Hare JM, Traverse JH, Henry TD, et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 2009; 54: 2277-2286.
17. van Laake LW, van Donselaar EG, Monshouwer-Kloots J, et al. Extracellular matrix formation after transplantation of human embryonic stem cell-derived cardiomyocytes. Cell Mol Life Sci 2010; 67: 277-290.
18. Landa N, Miller L, Feinberg MS, et al. Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat. Circulation 2008; 117: 1388-1396. (Pubitemid 351506386)
19. Leor J, Tuvia S, Guetta V, et al. Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in Swine. J Am Coll Cardiol 2009; 54: 1014-1023.
20. Dobner S, Bezuidenhout D, Govender P, et al. A synthetic non-degradable polyethylene glycol hydrogel retards adverse post-infarct left ventricular remodeling. J Card Fail 2009; 15: 629-636.
21. Kofidis T, Lebl DR, Martinez EC, et al. Novel injectable bioartificial tissue facilitates targeted, less invasive, large-scale tissue restoration on the beating heart after myocardial injury. Circulation 2005; 112: I173-I177. (Pubitemid 41266670)
22. Frederick JR, Fitzpatrick JR, 3rd, McCormick RC, et al. Stromal cell-derived factor-1alpha activation of tissue-engineered endothelial progenitor cell matrix enhances ventricular function after myocardial infarction by inducing neovasculogenesis. Circulation 2010; 122: S107-S117.
23. Danoviz ME, Nakamuta JS, Marques FL, et al. Rat adipose tissue-derived stem cells transplantation attenuates cardiac dysfunction post infarction and biopolymers enhance cell retention. PloS One 2010; 5: e12077.
24. Lin YD, Yeh ML, Yang YJ, et al. Intramyocardial peptide nanofiber injection improves postinfarction ventricular remodeling and efficacy of bone marrow cell therapy in pigs. Circulation 2010; 122: S132-S141.
25. Segers VF, Lee RT. Local delivery of proteins and the use of self-assembling peptides. Drug Discov Today 2007; 12: 561-568. (Pubitemid 47031660)
26. Stephan MT, Moon JJ, Um SH, et al. Therapeutic cell engineering with surface-conjugated synthetic nanoparticles. Nat Med 2010; 16: 1035-1041.
27. Penn MS, Mangi AA. Genetic enhancement of stem cell engraftment, survival, and efficacy. Circ Res 2008; 102: 1471-1482.
28. Baker M. RNA interference: Homing in on delivery. Nature 2010; 464: 1225-1228.
29. Houtgraaf JH, den Dekker WK, van Dalen BM, et al. First experience in humans using adipose tissue-derived regenerative cells in the treatment of patients with ST-segment elevation myocardial infarction. J Am Coll Cardiol 2012; 59: 539-540.
30. Iyer RK, Chiu LL, Reis LA, et al. Engineered cardiac tissues. Curr Opin Biotechnol 2011; 22: 706-714.
31. Radisic M, Park H, Martens TP, et al. Pre-treatment of synthetic elastomeric scaffolds by cardiac fibroblasts improves engineered heart tissue. J Biomed Mater Res A 2008; 86: 713-724.
32. Sekine H, Shimizu T, Hobo K, et al. Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 2008; 118: S145-S152.
33. van Laake LW, Passier R, den Ouden K, et al. Improvement of mouse cardiac function by hESC-derived cardiomyocytes correlates with vascularity but not graft size. Stem Cell Res 2009; 3: 106-112.
34. Saif J, Schwarz TM, Chau DY, et al. Combination of injectable multiple growth factor-releasing scaffolds and cell therapy as an advanced modality to enhance tissue neovascularization. Arterioscler Thromb Vasc Biol 2010; 30: 1897-1904.
35. Jay SM, Shepherd BR, Andrejecsk JW, et al. Dual delivery of VEGF and MCP-1 to support endothelial cell transplantation for therapeutic vascularization. Biomaterials 2010; 31: 3054-3062.
36. Madden LR, Mortisen DJ, Sussman EM, et al. Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc Natl Acad Sci USA 2010; 107: 15211-15216.
37. Bradley JA, Bolton EM, Pedersen RA. Stem cell medicine encounters the immune system. Nat Rev Immunol 2002; 2: 859-871. (Pubitemid 37328708)
38. Zimmermann A, Preynat-Seauve O, Tiercy JM, et al. Haplotype-based banking of human pluripotent stem cells for transplantation: potential and limitations. Stem Cells Dev 2012; 21: 2364-2373.
39. Zhao T, Zhang ZN, Rong Z, et al. Immunogenicity of induced pluripotent stem cells. Nature 2011; 474: 212-215.
40. Lui KO, Waldmann H, Fairchild PJ. Embryonic stem cells: overcoming the immunological barriers to cell replacement therapy. Curr Stem Cell Res Ther 2009; 4: 70-80.
41. Zijlstra M, Bix M, Simister NE, et al. Beta 2-microglobulin deficient mice lack CD4-8+ cytolytic T cells. Nature 1990; 344: 742-746.
42. Zuidema MY, Zhang C. Ischemia/reperfusion injury: The role of immune cells. World J Cardiol 2010; 2: 325-332.
43. Vilahur G, Juan-Babot O, Pena E, et al. Molecular and cellular mechanisms involved in cardiac remodeling after acute myocardial infarction. J Mol Cell Cardiol 2011; 50: 522-533.
44. Timmers L, Pasterkamp G, de Hoog VC, et al. The innate immune response in reperfused myocardium. Cardiovasc Res 2012; 94: 276-283.
45. Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002; 99: 3838-3843. (Pubitemid 34534559)
46. Kooreman NG, Wu JC. Tumorigenicity of pluripotent stem cells: biological insights from molecular imaging. J R Soc Interface 2010; 7 (Suppl 6): S753-S763.
47. Blum B, Bar-Nur O, Golan-Lev T, et al. The anti-apoptotic gene survivin contributes to teratoma formation by human embryonic stem cells. Nat Biotechnol 2009; 27: 281-287.
48. Amariglio N, Hirshberg A, Scheithauer BW, et al. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med 2009; 6: e1000029.
49. Cao F, Drukker M, Lin S, et al. Molecular imaging of embryonic stem cell misbehavior and suicide gene ablation. Cloning Stem Cells 2007; 9: 107-117. (Pubitemid 46642075)
50. Cao F, Li Z, Lee A, et al. Noninvasive de novo imaging of human embryonic stem cell-derived teratoma formation. Cancer Res 2009; 69: 2709-2713.
51. Menasche P. Stem cell therapy for heart failure: are arrhythmias a real safety concern? Circulation 2009; 119: 2735-2740.
52. Leobon B, Garcin I, Menasche P, et al. Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc Natl Acad Sci U S A 2003; 100: 7808-7811. (Pubitemid 36760051)
53. Makkar RR, Lill M, Chen PS. Stem cell therapy for myocardial repair: is it arrhythmogenic? J Am Coll Cardiol 2003; 42: 2070-2072. (Pubitemid 37549886)
54. Rubart M, Soonpaa MH, Nakajima H, et al. Spontaneous and evoked intracellular calcium transients in donor-derived myocytes following intracardiac myoblast transplantation. J Clin Invest 2004; 114: 775-783. (Pubitemid 39578736)
55. Mills WR, Mal N, Kiedrowski MJ, et al. Stem cell therapy enhances electrical viability in myocardial infarction. J Mol Cell Cardiol 2007; 42: 304-314. (Pubitemid 46135598)
56. Fernandes S, Amirault JC, Lande G, et al. Autologous myoblast transplantation after myocardial infarction increases the inducibility of ventricular arrhythmias. Cardiovasc Res 2006; 69: 348-358. (Pubitemid 43098791)
57. Dib N, Michler RE, Pagani FD, et al. Safety and feasibility of autologous myoblast transplantation in patients with ischemic cardiomyopathy: four-year follow-up. Circulation 2005; 112: 1748-1755. (Pubitemid 41368151)
58. Shiba Y, Fernandes S, Zhu WZ, et al. Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 2012; 489: 322-325.
59. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292: 154-156. (Pubitemid 11050741)
60. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282: 1145-1147. (Pubitemid 28516247)
61. Shiba Y, Hauch KD, Laflamme MA. Cardiac applications for human pluripotent stem cells. Curr Pharm Des 2009; 15: 2791-2806.
62. Mummery C, Ward-van Oostwaard D, Doevendans P, et al. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 2003; 107: 2733-2740.
63. Caspi O, Huber I, Kehat I, et al. Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J Am Coll Cardiol 2007; 50: 1884-1893. (Pubitemid 350007960)
64. Xue T, Cho HC, Akar FG, et al. 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. (Pubitemid 40070838)
65. van Laake LW, Passier R, Doevendans PA, et al. Human embryonic stem cell-derived cardiomyocytes and cardiac repair in rodents. Circ Res 2008; 102: 1008-1010. (Pubitemid 351667854)
66. van Laake LW, Passier R, Monshouwer-Kloots J, et al. Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Res 2007; 1: 9-24. (Pubitemid 350251944)
67. Laflamme MA, Chen KY, Naumova AV, et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 2007; 25: 1015-1024. (Pubitemid 47517637)
68. Jonsson MK, Vos MA, Mirams GR, et al. Application of human stem cell-derived cardiomyocytes in safety pharmacology requires caution beyond hERG. J Mol Cell Cardiol 2012; 52: 998-1008.
69. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-676. (Pubitemid 44233629)
70. Zhang J, Wilson GF, Soerens AG, et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 2009; 104: e30-e41.
71. van Laake LW, Qian L, Cheng P, et al. Reporter-based isolation of induced pluripotent stem cell and embryonic stem cell-derived cardiac progenitors reveals limited gene expression variance. Circ Res 2010; 107: 340-347.
72. Nelson TJ, Martinez-Fernandez A, Yamada S, et al. Repair of acute myocardial infarction by human stemness factors induced pluripotent stem cells. Circulation 2009; 120: 408-416.
73. Raper SE, Chirmule N, Lee FS, et al. Fatal systemic inflammatory response syndrome in an ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol Genet Metab 2003; 80: 148-158. (Pubitemid 37272241)
74. Thrasher AJ, Gaspar HB, Baum C, et al. Gene therapy: X-SCID transgene leukaemogenicity. Nature 2006; 443: E5-E6; discussion E-7.
75. Stadtfeld M, Nagaya M, Utikal J, et al. Induced pluripotent stem cells generated without viral integration. Science 2008; 322: 945-949.
76. Zhou H, Wu S, Joo JY, et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009; 4: 381-384.
77. Ieda M, Fu JD, Delgado-Olguin P, et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010; 142: 375-386.
78. Efe JA, Hilcove S, Kim J, et al. Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat Cell Biol 2011; 13: 215-222.
79. Song K, Nam YJ, Luo X, et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 2012; 485: 599-604.
80. Qian L, Huang Y, Spencer CI, et al. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012; 485: 593-598.
81. Dawn B, Bolli R. Adult bone marrow-derived cells: regenerative potential, plasticity, and tissue commitment. Basic Res Cardiol 2005; 100: 494-503. (Pubitemid 41662429)
82. Orlic D, Kajstura J, Chimenti S, et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001; 410: 701-705. (Pubitemid 32290358)
83. Kucia M, Dawn B, Hunt G, et al. Cells expressing early cardiac markers reside in the bone marrow and are mobilized into the peripheral blood after myocardial infarction. Circ Res 2004; 95: 1191-1199. (Pubitemid 39648210)
84. Wagers AJ, Sherwood RI, Christensen JL, et al. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 2002; 297: 2256-2259.
85. Chien KR. Stem cells: lost in translation. Nature 2004; 428: 607-608.
86. Murry CE, Soonpaa MH, Reinecke H, et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 2004; 428: 664-668. (Pubitemid 38524810)
87. Yousef M, Schannwell CM, Kostering M, et al. The BALANCE Study: clinical benefit and long-term outcome after intracoronary autologous bone marrow cell transplantation in patients with acute myocardial infarction. J Am Coll Cardiol 2009; 53: 2262-2269.
88. Martin-Rendon E, Brunskill SJ, Hyde CJ, et al. Autologous bone marrow stem cells to treat acute myocardial infarction: a systematic review. Eur Heart J 2008; 29: 1807-1818.
89. Price MJ, Chou CC, Frantzen M, et al. Intravenous mesenchymal stem cell therapy early after reperfused acute myocardial infarction improves left ventricular function and alters electrophysiologic properties. Int J Cardiol 2006; 111: 231-239. (Pubitemid 44107562)
90. Jeevanantham V, Butler M, Saad A, et al. Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters: a systematic review and meta-analysis. Circulation 2012; 126: 551-568.
91. Beitnes JO, Hopp E, Lunde K, et al. Long-term results after intracoronary injection of autologous mononuclear bone marrow cells in acute myocardial infarction: the ASTAMI randomised, controlled study. Heart 2009; 95: 1983-1989.
92. Meyer GP, Wollert KC, Lotz J, et al. Intracoronary bone marrow cell transfer after myocardial infarction: 5-year follow-up from the randomized-controlled BOOST trial. Eur Heart J 2009; 30: 2978-2984.
93. Traverse JH, Henry TD, Pepine CJ, et al. Effect of the use and timing of bone marrow mononuclear cell delivery on left ventricular function after acute myocardial infarction: the TIME randomized trial. JAMA 2012; 308: 2380-2389.
94. BAMI trial. http://clinicaltrials.gov/show/NCT01569178 (accessed Jan 22, 2013).
95. Williams AR, Hare JM. Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res 2011; 109: 923-940.
96. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-147. (Pubitemid 29282067)
97. Behfar A, Yamada S, Crespo-Diaz R, et al. Guided cardiopoiesis enhances therapeutic benefit of bone marrow human mesenchymal stem cells in chronic myocardial infarction. J Am Coll Cardiol 2010; 56: 721-734.
98. C-Cure Trial. http://clinicaltrials.gov/ct2/show/NCT00810238 (accessed Jan 22, 2013).
99. Quevedo HC, Hatzistergos KE, Oskouei BN, et al. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc Natl Acad Sci USA 2009; 106: 14022-14027.
100. Gnecchi M, Zhang Z, Ni A, et al. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008; 103: 1204-1219.
101. Toma C, Pittenger MF, Cahill KS, et al. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002; 105: 93-98. (Pubitemid 34049148)
102. Wang T, Xu Z, Jiang W, et al. Cell-to-cell contact induces mesenchymal stem cell to differentiate into cardiomyocyte and smooth muscle cell. Int J Cardiol 2006; 109: 74-81.
103. Xu W, Zhang X, Qian H, et al. Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp Biol Med (Maywood) 2004; 229: 623-631. (Pubitemid 38878907)
104. Gnecchi M, Danieli P, Cervio E. Mesenchymal stem cell therapy for heart disease. Vascul Pharmacol 2012; 57: 48-55.
105. Goumans MJ, de Boer TP, Smits AM, et al. TGF-beta1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res 2007; 1: 138-149.
106. Smits AM, van Laake LW, den Ouden K, et al. Human cardiomyocyte progenitor cell transplantation preserves long-term function of the infarcted mouse myocardium. Cardiovasc Res 2009; 83: 527-535.
107. Noort WA, Sluijter JP, Goumans MJ, et al. Stem cells from in- or outside of the heart: isolation, characterization, and potential for myocardial tissue regeneration. Pediatr Cardiol 2009; 30: 699-709.
108. Bolli R, Chugh AR, D'Amario D, et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 2011; 378: 1847-1857.
109. Makkar RR, Smith RR, Cheng K, et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 2012; 379: 895-904.
110. Hackam DG, Redelmeier DA. Translation of research evidence from animals to humans. JAMA 2006; 296: 1731-1732. (Pubitemid 44547792)
111. Bolli R, Becker L, Gross G, et al. Myocardial protection at a crossroads: the need for translation into clinical therapy. Circ Res 2004; 95: 125-134. (Pubitemid 38988678)
112. Dhein S, Garbade J, Rouabah D, et al. Effects of autologous bone marrow stem cell transplantation on beta-adrenoceptor density and electrical activation pattern in a rabbit model of non-ischemic heart failure. J Cardiothorac Surg 2006; 1: 17.
113. Nair M, Mukherjee S, Ahluwalia NS, et al. Feasibility and safety of autologous intracoronary stem cell transplantation in patients of non ischemic dilated cardiomyopathy. Indian Heart J 2007; 59: 511-514.
114. Vrtovec B, Poglajen G, Lezaic L, et al. Effects of Intracoronary CD34+ stem cell transplantation in nonischemic dilated cardiomyopathy patients: 5-year follow-up. Circ Res 2013; 112: 165-173.
115. Passier R, van Laake LW, Mummery CL. Stem-cell-based therapy and lessons from the heart. Nature 2008; 453: 322-329. (Pubitemid 351693138)
116. van der Spoel TI, Jansen of Lorkeers SJ, Agostoni P, et al. Human relevance of pre-clinical studies in stem cell therapy: systematic review and meta-analysis of large animal models of ischaemic heart disease. Cardiovasc Res 2011; 91: 649-658.