Cardiac cell therapy: Where weve been, where we are, and where we should be headed

British Medical Bulletin

Volumn 98, Issue 1, 2011, Pages 161-185

  Malliaras, Konstantinos ^a   Marbán, Eduardo ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

cardiac stem cells; heart regeneration; stem cell therapy

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; STEM CELL ANTIGEN 1; STEM CELL FACTOR RECEPTOR;

ACUTE HEART INFARCTION; ALLOTRANSPLANTATION; ANGINA PECTORIS; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; BLOOD CLOT LYSIS; BONE MARROW TRANSPLANTATION; CARDIOMYOPLASTY; CELL DIFFERENTIATION; CLINICAL EFFECTIVENESS; CORONARY ARTERY BYPASS GRAFT; EMBRYONIC STEM CELL; ENGRAFTMENT; EXTRACELLULAR MATRIX; HEART FAILURE; HEART INFARCTION; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE; HEART MUSCLE CELL; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HYDROGEL; INTRACORONARY INFUSION; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MULTIPOTENT STEM CELL; MUSCLE REGENERATION; MYOBLAST; NERVE BLOCK; NONHUMAN; PARACRINE SIGNALING; PATIENT SAFETY; PERCUTANEOUS CORONARY INTERVENTION; PHASE 1 CLINICAL TRIAL (TOPIC); PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; STEM CELL TRANSPLANTATION; VASCULAR SMOOTH MUSCLE;

ADULT STEM CELLS; ANIMALS; BONE MARROW TRANSPLANTATION; EMBRYONIC STEM CELLS; HEART DISEASES; HUMANS; MYOBLASTS, SKELETAL; MYOCYTES, CARDIAC; STEM CELL TRANSPLANTATION;

EID: 79958782230     PISSN: 00071420     EISSN: 14718391     Source Type: Journal    
DOI: 10.1093/bmb/ldr018     Document Type: Article

References (144)

1. Heron M, Hoyert DL, Murphy SL et al. Deaths: final data for 2006. Natl Vital Stat Rep 2009;57:1-134.
2. Roger VL, Go AS, Lloyd-Jones DM et al. Heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation 2011;123:e18-e209.
3. Ford ES, Ajani UA, Croft JB et al. Explaining the decrease in U.S. deaths from coronary disease, 1980-2000. N Engl J Med 2007;356:2388-98. (Pubitemid 46883773)
4. Moss AJ, Zareba W, Hall WJ et al. Prophylactic implantation of a defibrillator in patients with myocardial infarction and reduced ejection fraction. N Engl J Med 2002;346:877-83. (Pubitemid 34984635)
5. 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;50:1884-93. (Pubitemid 350007960)
6. Dai W, Field LJ, Rubart M et al. Survival and maturation of human embryonic stem cellderived cardiomyocytes in rat hearts. J Mol Cell Cardiol 2007;43:504-16. (Pubitemid 47454736)
7. 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;25:1015-24. (Pubitemid 47517637)
8. 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;107:340-7.
9. Muller-Ehmsen J, Peterson KL, Kedes L et al. Rebuilding a damaged heart: long-term survival of transplanted neonatal rat cardiomyocytes after myocardial infarction and effect on cardiac function. Circulation 2002;105:1720-6. (Pubitemid 34298618)
10. Reffelmann T, Dow JS, Dai W et al. Transplantation of neonatal cardiomyocytes after permanent coronary artery occlusion increases regional blood flow of infarcted myocardium. J Mol Cell Cardiol 2003;35:607-13. (Pubitemid 36677444)
11. Menasche P, Alfieri O, Janssens S et al. The Myoblast Autologous Grafting in Ischemic Cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 2008;117:1189-200. (Pubitemid 351552018)
12. Katritsis DG, Sotiropoulou PA, Karvouni E et al. Transcoronary transplantation of autologous mesenchymal stem cells and endothelial progenitors into infarcted human myocardium. Catheter Cardiovasc Interv 2005;65:321-9. (Pubitemid 40898172)
13. Schachinger V, Erbs S, Elsä sser A et al. Improved clinical outcome after intracoronary administration of bone-marrow-derived progenitor cells in acute myocardial infarction: final 1-year results of the REPAIR-AMI trial. Eur Heart J 2006;27:2775-83. (Pubitemid 44871463)
14. Wollert KC, Meyer GP, Lotz J et al. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 2004;364:141-8. (Pubitemid 38891685)
15. Lunde K, Solheim S, Aakhus S et al. Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N Engl J Med 2006;355:1199-209. (Pubitemid 44427444)
16. Chen SL, Fang WW, Ye F et al. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol 2004;94:92-5. (Pubitemid 38813459)
17. Smith RR, Barile L, Cho HC et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007;115:896-908. (Pubitemid 46294730)
18. Beltrami AP, Barlucchi L, Torella D et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003;114:763-76. (Pubitemid 37186770)
19. Nussbaum J, Minami E, Laflamme MA et al. Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. Faseb J 2007;21:1345-57. (Pubitemid 46684837)
20. Menasche P, Hagege AA, Vilquin JT et al. Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J Am Coll Cardiol 2003;41:1078-83. (Pubitemid 36384891)
21. Siminiak T, Kalawski R, Fiszer D et al. Autologous skeletal myoblast transplantation for the treatment of postinfarction myocardial injury: phase I clinical study with 12 months of follow-up. Am Heart J 2004;148:531-37. (Pubitemid 39265130)
22. Smits PC, van Geuns RJ, Poldermans D et al. Catheter-based intramyocardial injection of autologous skeletal myoblasts as a primary treatment of ischemic heart failure: clinical experience with six-month follow-up. J Am Coll Cardiol 2003;42:2063-69. (Pubitemid 37549885)
23. Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 2008;132:661-80. (Pubitemid 351260059)
24. Nelson TJ, Martinez-Fernandez A, Terzic A. Induced pluripotent stem cells: developmental biology to regenerative medicine. Nat Rev Cardiol 2010;7:700-710.
25. Huber I, Itzhaki I, Caspi O et al. Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. FASEB J 2007;21:2551-63. (Pubitemid 47230684)
26. Passier R, van Laake LW, Mummery CL. Stem-cell-based therapy and lessons from the heart. Nature 2008;453:322-29. (Pubitemid 351693138)
27. Safety Study of GRNOPC1 in Spinal Cord Injury (NCT01217008). www.clinicaltrials.gov.
28. Takahashi K, Tanabe K, Ohnuki M et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-72. (Pubitemid 350138099)
29. Narazaki G, Uosaki H, Teranishi M et al. Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation 2008;118:498-506.
30. Zhang J, Wilson GF, Soerens AG et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 2009;104:e30-e41.
31. Freund C, Mummery CL. Prospects for pluripotent stem cell-derived cardiomyocytes in cardiac cell therapy and as disease models. J Cell Biochem 2009;107:592-9.
32. Gore A, Li Z, Fung HL et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 2011;471:63-67.
33. Ieda M, Fu JD, Delgado-Olguin P et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010;142:375-86.
34. Efe JA, Hilcove S, Kim J et al. Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat Cell Biol 2011;13:215-22.
35. Jain M, DerSimonian H, Brenner DA et al. Cell therapy attenuates deleterious ventricular remodeling and improves cardiac performance after myocardial infarction. Circulation 2001;103:1920-7. (Pubitemid 32328408)
36. He KL, Yi GH, Sherman W et al. Autologous skeletal myoblast transplantation improved hemodynamics and left ventricular function in chronic heart failure dogs. J Heart Lung Transplant 2005;24:1940-9. (Pubitemid 41641872)
37. Leobon B, Garcin I, Menasche P et al. Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc Natl Acad Sci USA 2003;100:7808-11. (Pubitemid 36760051)
38. Menasché P, Hagège AA, Scorsin M et al. Myoblast transplantation for heart failure. Lancet 2001;357:279-80. (Pubitemid 32120862)
39. Hagège AA, Marolleau JP, Vilquin JT et al. Circulation 2006;114(1 Suppl.):108-13.
40. Abraham MR, Henrikson CA, Tung L et al. Antiarrhythmic engineering of skeletal myoblasts for cardiac transplantation. Circ Res 2005;97:159-67. (Pubitemid 41033472)
41. Duckers HJ, Houtgraaf J, Hehrlein C et al. Final results of a phase IIa, randomised, openlabel trial to evaluate the percutaneous intramyocardial transplantation of autologous skeletal myoblasts in congestive heart failure patients: the SEISMIC trial. EuroIntervention 2011;6:805-812.
42. Strauer BE, Brehm M, Zeus T et al. Intracoronary, human autologous stem cell transplantation for myocardial regeneration following myocardial infarction. Dtsch Med Wochenschr 2001;126:932-8. (Pubitemid 32844014)
43. Orlic D, Kajstura J, Chimenti S et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001;410:701-5. (Pubitemid 32290358)
44. Murry CE, Soonpaa MH, Reinecke H et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature (2004);428:664-8. (Pubitemid 38524810)
45. Balsam LB, Wagers AJ, Christensen JL et al. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 2004;428:668-73. (Pubitemid 38524811)
46. Civin CI, Gore SD. Antigenic analysis of hematopoiesis: a review. J Hematother 1993;2:137-44. (Pubitemid 24090509)
47. Sussman MA, Murry CE. Bones of contention: marrow-derived cells in myocardial regeneration. J Mol Cell Cardiol 2008;44:950-3.
48. Crosby JR, Kaminski WE, Schatteman G et al. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res 2000;87:728-30.
49. Rehman J, Li J, Orschell CM et al. Peripheral blood 'endothelial progenitor cells' are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 2003;107:1164-9. (Pubitemid 36297209)
50. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-7. (Pubitemid 44269669)
51. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-22. (Pubitemid 40223708)
52. Dimmeler S, Zeiher AM. Cell therapy of acute myocardial infarction: open questions. Cardiology 2009;113:155-60.
53. Zhang S, Sun A, Xu D et al. Impact of timing on efficacy and safety of intracoronary autologous bone marrow stem cells transplantation in acute myocardial infarction: a pooled subgroup analysis of randomized controlled trials. Clin Cardiol 2009;32:458-66.
54. 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;29:1807-18.
55. Losordo DW, Schatz RA, White CJ et al. Intramyocardial transplantation of autologous CD34\+ stem cells for intractable angina: a phase I/IIa double-blind, randomized controlled trial. Circulation 2007;115:3165-3172. (Pubitemid 47018140)
56. van Ramshorst J, Bax JJ, Jeroen J et al. Intramyocardial bone marrow cell injection for chronic myocardial ischemia: a randomized controlled trial. JAMA 2009;301:1997-2004.
57. Mocini D, Staibano M, Mele L et al. Autologous bone marrow mononuclear cell transplantation in patients undergoing coronary artery bypass grafting. Am Heart J 2006;151:192-207.
58. Hendrikx M, Hensen K, Clijsters C et al. Recovery of regional but not global contractile function by the direct intramyocardial autologous bone marrow transplantation: results from a randomized controlled clinical trial. Circulation 2006;114(Suppl. 1):I101-I107. (Pubitemid 44297136)
59. Stamm C, Kleine HD, Choi YH. et al. Intramyocardial delivery of CD133\+ bone marrow cells and coronary artery bypass grafting for chronic ischemic heart disease: safety and efficacy studies. J Thorac Cardiovasc Surg 2007;133:717-725.
60. Bergmann O, Bhardwaj RD, Bernard S et al. Evidence for cardiomyocyte renewal in humans. Science 2009;324:98-102.
61. Mercola M, Ruiz-Lozano P, Schneider MD. Cardiac muscle regeneration: lessons from development. Genes Dev 2011;25:299-309.
62. Zhang Y, Li TS, Lee ST et al. Dedifferentiation and proliferation of mammalian cardiomyocytes. PLoS One 2010;5:e12559.
63. Deisher TA. Cardiac-derived stem cells. IDrugs 2000;3:649-53.
64. Oh H, Bradfute SB, Gallardo TD et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 2003;100:12313-8. (Pubitemid 37271557)
65. Messina E, De Angelis L, Frati G et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 2004;95:911-21. (Pubitemid 39435006)
66. Feigl EO. Coronary physiology. Physiol Rev 1983;63:1-205. (Pubitemid 13188482)
67. Davis DR, Zhang Y, Smith RR et al. Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue. PLoS One 2009;4:e7195.
68. Johnston PV, Sasano T, Mills K et al. Engraftment, differentiation, and functional benefits of autologous cardiosphere-derived cells in porcine ischemic cardiomyopathy. Circulation 2009;120:1075-83.
69. Li TS, Cheng K, Lee ST et al. Cardiospheres recapitulate a niche-like microenvironment rich in stemness and cell-matrix interactions, rationalizing their enhanced functional potency for myocardial repair. Stem Cells 2010;28:2088-98.
70. Chimenti I, Smith RR, Li TS et al. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res 2010;106:971-80.
71. Cheng K, Li TS, Malliaras K et al. Magnetic targeting enhances engraftment and functional benefit of iron-labeled cardiosphere-derived cells in myocardial infarction. Circ Res 2010;106:1570-81.
72. Davis DR, Kizana E, Terrovitis J et al. Isolation and expansion of functionally competent cardiac progenitor cells directly from heartbiopsies. J Mol Cell Cardiol 2010;49:312-21.
73. Terrovitis J, Lautamäki R, Bonios M et al. Noninvasive quantification and optimization of acute cell retention by in vivo positron emission tomography after intramyocardial cardiacderived stem cell delivery. J Am Coll Cardiol 2009;54:1619-26.
74. Lee ST, White AJ, Matsushita S et al. Intramyocardial injection of autologous cardiospheres or cardiosphere-derived cells preserves function and minimizes adverse ventricular remodeling in pigs with heart failure post-myocardial infarction. J Am Coll Cardiol 2011;57:455-65.
75. Aghila Rani KG, Kartha CC. Effects of epidermal growth factor on proliferation and migration of cardiosphere-derived cells expanded from adult human heart. Growth Factors 2010;28:157-65.
76. Gaetani R, Ledda M, Barile L et al. Differentiation of human adult cardiac stem cells exposed to extremely low-frequency electromagnetic fields. Cardiovasc Res 2009;82:411-20.
77. Mishra R, Vijayan K, Colletti EJ et al. Characterization and functionality of cardiac progenitor cells in congenital heart patients. Circulation 2011;123:364-73.
78. Takehara N, Tsutsumi Y, Tateishi K et al. Controlled delivery of basic fibroblast growth factor promotes human cardiosphere-derived cell engraftment to enhance cardiac repair for chronic myocardial infarction. J Am Coll Cardiol 2008;52:1858-65.
79. Tang YL, Zhu W, Cheng M et al. Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression. Circ Res 2009;104:1209-16.
80. Zakharova L, Mastroeni D, Mutlu N et al. Transplantation of cardiac progenitor cell sheet onto infarcted heart promotes cardiogenesis and improves function. Cardiovasc Res 2010;87:40-9.
81. Koninckx R, Danië ls A, Windmolders S et al. Mesenchymal stem cells or cardiac progenitors for cardiac repair? A comparative study. Cell Mol Life Sci 2010. DOI: 10.1007/s00018- 010-0560-y.
82. Hodgkiss-Geere HM, Argyle DJ, Corcoran BM et al. Characterisation and cardiac directed differentiation of canine adult cardiac stem cells. Vet J 2011; doi:10.1016/ j.tvjl.2010.12.033.
83. Andersen DC, Andersen P, Schneider M et al. Murine 'cardiospheres' are not a source of stem cells with cardiomyogenic potential. Stem Cells 2009;27:1571-81.
84. Shenje LT, Field LJ, Pritchard CA et al. Lineage tracing of cardiac explant derived cells. PLoS ONE. 2008;3:e1929.
85. Davis DR, Ruckdeschel Smith R, Marbán E. Human cardiospheres are a source of stem cells with cardiomyogenic potential. Stem Cells 2010;28:903-4.
86. Cheng K, Li T-S, Malliaras K et al. Paracrine and functional superiority of human cardiosphere-derived cells as compared to mesenchymal stem cells, adipose-derived stem cells or bone marrow mononuclear cells. Circulation 2010;122:A20957.
87. Smith RR, Chimenti I, Marbán E. Unselected human cardiosphere-derived cells are functionally superior to c-Kit- or CD90-purified cardiosphere-derived cells. Circulation 2008;118:S420.
88. CADUCEUS. CArdiosphere-Derived aUtologous stem CElls to reverse ventricUlar dysfunction (NCT00893360). www.clinicaltrials.gov.
89. SCIPIO. Cardiac stem cell infusion in patients with ischemic cardiOmyopathy (NCT00474461). www.clinicaltrials.gov.
90. Ragosta M, Beller GA, Watson DD et al. Quantitative planar rest-redistribution 201Tl imaging in detection of myocardial viability and prediction of improvement in left ventricular function after coronary bypass surgery in patients with severely depressed left ventricular function. Circulation 1993;87(5):1630.
91. Ugander M, Cain PA, Johnsson P et al. Chronic non-transmural infarction has a delayed recovery of function following revascularization. BMC Cardiovasc Disord 2010;10:4.
92. Silvestre JS, Gojova A, Brun V et al. Transplantation of bone marrow derived mononuclear cells in ischemic apolipoprotein E-knockout mice accelerates atherosclerosis without altering plaque composition. Circulation 2003;108:2839-42. (Pubitemid 37517809)
93. Mansour S, Vanderheyden M, De Bruyne B et al. Intracoronary delivery of hematopoietic bone marrow stem cells and luminal loss of the infarct-related artery in patients with recent myocardial infarction. J Am Coll Cardiol 2006;474:1727-30.
94. Fernandez-Aviles F, San Roman JA, Garcia-Frade J et al. Experimental and clinical regenerative capability of human bone marrow cells after myocardial infarction. Circ Res 2004;95:742-8. (Pubitemid 39331935)
95. Bartunek J, Vanderheyden M, Vandekerckhove B et al. Intracoronary injection of CD133-positive enriched bone marrow progenitor cells promotes cardiac recovery after recent myocardial infarction: feasibility and safety. Circulation 2005;112(Suppl. 9):I178-83. (Pubitemid 41266671)
96. Schächinger V, Erbs S, Elsä sser A et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 2006;355:1210-21.
97. Seeger FH, Tonn T, Krzossok N et al. Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction. Eur Heart J 2007;28:766-72. (Pubitemid 46439231)
98. Meyer GP, Wollert KC, Lotz J et al. Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months' follow-up data from the randomized, controlled BOOST trial. Circulation 2006;113:1287-94. (Pubitemid 43739450)
99. Huikuri HV, Kervinen K, Niemelä M et al. Effects of intracoronary injection of mononuclear bone marrow cells on left ventricular function, arrhythmia risk profile, and restenosis after thrombolytic therapy of acute myocardial infarction. Eur Heart J 2008;29:2723-32.
100. Tendera M, Wojakowski W, Ruzyłło W et al. Intracoronary infusion of bone marrowderived selected CD34\+CXCR4\+ cells and non-selected mononuclear cells in patients with acute STEMI and reduced left ventricular ejection fraction: results of randomized, multicentre Myocardial Regeneration by Intracoronary Infusion of Selected Population of Stem Cells in Acute Myocardial Infarction (REGENT) Trial. Eur Heart J 2009;30:1313-21.
101. Janssens S, Dubois C, Bogaert J et al. Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 2006;367:113-21. (Pubitemid 43077127)
102. Roncalli J, Mouquet F, Piot C et al. Intracoronary autologous mononucleated bone marrow cell infusion for acute myocardial infarction: results of the randomized multicenter BONAMI trial. Eur Heart J 2010. doi:10.1093/eurheartj/ehq455.
103. Hirsch A, Nijveldt R, van der Vleuten PA et al. Intracoronary infusion of mononuclear cells from bone marrow or peripheral blood compared with standard therapy in patients after acute myocardial infarction treated by primary percutaneous coronary intervention: results of the randomized controlled HEBE trial. Eur Heart J 2010. doi:10.1093/eurheartj/ehq449.
104. Wö hrle J, Merkle N, Mailänder V et al. Results of intracoronary stem cell therapy after acute myocardial infarction. Am J Cardiol 2010;105:804-12.
105. Hou D, Youssef EA-S, Brinton TJ et al. Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation 2005;112(9 Suppl.):I150-6. (Pubitemid 41266667)
106. Aicher A, Brenner W, Zuhayra M et al. Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling. Circulation 2003;107:2134-9. (Pubitemid 36532196)
107. Blocklet D, Toungouz M, Berkenboom G et al. Myocardial homing of nonmobilized peripheral-blood CD34\+ Cells after intracoronary injection. Stem Cells 2006;24:333-6. (Pubitemid 44464802)
108. Hofmann M, Wollert KC, Meyer GP et al. Monitoring of Bone Marrow Cell Homing Into the Infarcted Human Myocardium. Circulation 2005;111:2198-2202. (Pubitemid 40632435)
109. Mü ller-Ehmsen J, Whittaker P, Kloner RA et al. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. J Mol Cell Cardiol 2002;34:107-16.
110. Zeng L, Hu Q, Wang X et al. Bioenergetic and functional consequences of bone marrowderived multipotent progenitor cell transplantation in hearts with postinfarction left ventricular remodeling. Circulation 2007;115:1866-75. (Pubitemid 46598900)
111. 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;106:14022-7.
112. Tang XL, Rokosh G, Sanganalmath SK et al. Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation 2010;121:293-305.
113. Gnecchi M, Zhang Z, Ni A et al. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008;103:1204-19.
114. Perez-Ilzarbe M, Agbulut O, Pelacho B et al. Characterization of the paracrine effects of human skeletal myoblasts transplanted in infarcted myocardium. Eur J Heart Fail 2008;10:1065-72.
115. Korf-Klingebiel M, Kempf T, Sauer T et al. Bone marrow cells are a rich source of growth factors and cytokines: implications for cell therapy trials after myocardial infarction. Eur Heart J 2008;29:2851-8.
116. Gnecchi M, He H, Noiseux N et al. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 2006;20:661-9. (Pubitemid 44933310)
117. Cho HJ, Lee N, Lee JY et al. Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J Exp Med 2007;204:3257-69.
118. Quaini F, Urbanek K, Beltrami AP et al. Chimerism of the transplanted heart. N Engl J Med 2002;346:5-15. (Pubitemid 34438914)
119. Laflamme MA, Myerson D, Saffitz JE et al. Evidence for cardiomyocyte repopulation by extracardiac progenitors in transplanted human hearts. Circ Res 2002;90:634-40. (Pubitemid 34640880)
120. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM et al. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 2003;425:968-73. (Pubitemid 37376928)
121. Assmus B, Rolf A, Erbs S et al. Clinical outcome 2 years after intracoronary administration of bone marrow-derived progenitor cells in acute myocardial infarction. Circ Heart Fail 2010;3:89-96.
122. Yousef M, Schannwell CM, Kö stering 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;53:2262-9.
123. Williams AR, Trachtenberg B, Velazquez DL et al. Intramyocardial stem cell injection in patients with ischemic cardiomyopathy: functional recovery and reverse remodeling. Circ Res. 2011;108:792-796.
124. Reffelmann T, Könemann S, Kloner RA. Promise of blood- and bone marrow-derived stem cell transplantation for functional cardiac repair: putting it in perspective with existing therapy. J Am Coll Cardiol 2009;53:305-8.
125. Robey TE, Saiget MK, Reinecke H et al. Systems approaches to preventing transplanted cell death in cardiac repair. J Mol Cell Cardiol 2008;45:567-81.
126. Doyle B, Sorajja P, Hynes B et al. Progenitor cell therapy in a porcine acute myocardial infarction model induces cardiac hypertrophy, mediated by paracrine secretion of cardiotrophic factors including TGFbeta1. Stem Cells Dev 2008;17:941-51.
127. Beeres SL, Atsma DE, van Ramshorst J et al. Cell therapy for ischaemic heart disease. Heart 2008;94:1214-26.
128. Siminiak T, Fiszer D, Jerzykowska O et al. Percutaneous trans-coronary-venous transplantation of autologous skeletal myoblasts in the treatment of post-infarction myocardial contractility impairment: The POZNAN trial. Eur Heart J 2005;26:1188-1195. (Pubitemid 40863125)
129. Thompson CA, Nasseri BA, Makower J et al. Percutaneous transvenous cellular cardiomyoplasty: a novel nonsurgical approach for myocardial cell transplantation. J Am Col Cardiol 2003;41:1964-1971. (Pubitemid 36677117)
130. Azene N, Ehtiati T, Fu Y et al. Intrapericardial delivery of visible microcapsules containing stem cells using xfm (X-ray fused with magnetic resonance imaging). J Cardiovasc Magn Reson 2011;13(Suppl. 1):P26.
131. Freyman T, Polin G, Osman H et al. A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. Eur Heart J 2006;27:1114-22.
132. Murry CE, Field LJ, Menasché P. Cell-based cardiac repair reflections at the 10-year point. Circulation 2005;112:3174-3183. (Pubitemid 43113446)
133. Psaltis PJ, Worthley SG. Endoventricular electromechanical mapping-the diagnostic and therapeutic utility of the NOGA XP Cardiac Navigation System. J Cardiovasc Transl Res 2009;2:48-62.
134. Terrovitis JV, Smith RR, Marbán E. Assessment and optimization of cell engraftment after transplantation into the heart. Circ Res 2010;106:479-94.
135. Christman KL, Lee RJ. Biomaterials for the treatment of myocardial infarction. J Am Coll Cardiol. 2006;48:907-13. (Pubitemid 44292446)
136. Dimmeler S, Leri A. Aging and disease as modifiers of efficacy of cell therapy. Circ Res 2008;102:1319-30.
137. Dib N, Henry T, DeMaria A et al. The first US study to assess the feasibility and safety of endocardial delivery of allogeneic mesenchymal stem precursor cells in patient with heart failure: three month interim analysis (abstr). Circulation 2009;120(Suppl.):810.
138. 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;54:2277-86.
139. Zangi L, Margalit R, Reich-Zeliger S et al. Direct imaging of immune rejection and memory induction by allogeneic mesenchymalstromal cells. Stem Cells 2009;27:2865-74.
140. Badillo AT, Beggs KJ, Javazon EH et al. Murine bone marrow stromal progenitor cells elicit an in vivo cellular andhumoral alloimmune response. Biol Blood Marrow Transplant 2007;13:412-22. (Pubitemid 46421896)
141. Eliopoulos N, Stagg J, Lejeune L et al. Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood 2005;106:4057-65. (Pubitemid 41775910)
142. Poncelet AJ, Vercruysse J, Saliez A et al. Although pig allogeneic mesenchymal stem cells are not immunogenic in vitro,intracardiac injection elicits an immune response in vivo. Transplantation 2007;83:783-90. (Pubitemid 46569198)
143. Assmus B, Fischer-Rasokat U, Honold J et al. TOPCARE-CHD Registry: transcoronary transplantation of functionally competent BMCs is associated with a decrease in natriuretic peptide serum levels and improved survival of patients with chronic postinfarction heart failure: results of the TOPCARE-CHD Registry. Circ Res 2007;100:1234-41. (Pubitemid 46684137)
144. Yao K, Huang RC, Ge L et al. Observation on the safety: clinical trial on