Cellular therapy for heart failure

Current Cardiology Reviews

Volumn 12, Issue 3, 2016, Pages 195-215

  Psaltis, Peter J ^a,b   Schwarz, Nisha ^a,b   Toledo Flores, Deborah ^a,b   Nicholls, Stephen J ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Angiogenesis; Cardiac stem cells; Heart failure; Mesenchymal stem cells; Pluripotent stem cells

Indexed keywords

BRAIN NATRIURETIC PEPTIDE;

ALLOTRANSPLANTATION; ARTICLE; BONE MARROW DERIVED MONONUCLEAR CELL; CARDIOMYOPATHY; CARDIOVASCULAR DISEASE; CELL REPROGRAMMING TECHNIQUE; CELL THERAPY; ELECTROPHYSIOLOGY; EMBRYONIC STEM CELL; EXCITATION CONTRACTION COUPLING; GENE OVEREXPRESSION; HEART FAILURE; HUMAN; INFLAMMATION; ISCHEMIC CARDIOMYOPATHY; ISCHEMIC PRECONDITIONING; MESENCHYMAL STROMA CELL; MORTALITY; NONHUMAN; OXIDATIVE STRESS; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); ADULT STEM CELL; BONE MARROW TRANSPLANTATION; CARDIAC MUSCLE CELL; CARDIOMYOPATHIES; DIASTOLE; HEART VENTRICLE REMODELING; MESENCHYMAL STEM CELL TRANSPLANTATION; PHYSIOLOGY; SKELETAL MYOBLAST; TRANSPLANTATION;

ADULT STEM CELLS; BONE MARROW TRANSPLANTATION; CARDIOMYOPATHIES; DIASTOLE; EMBRYONIC STEM CELLS; HEART FAILURE; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MYOBLASTS, SKELETAL; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS; VENTRICULAR REMODELING;

EID: 84981534897     PISSN: 1573403X     EISSN: 18756557     Source Type: Journal    
DOI: 10.2174/1573403X12666160606121858     Document Type: Article

References (189)

1. Go AS, Mozaffarian D, Roger VL, et al. Heart disease and stroke statistics--2014 update: a report from the American Heart Association. Circulation 2014; 129(3): e28-e292.
2. Lloyd-Jones DM, Larson MG, Leip EP, et al. Lifetime risk for developing congestive heart failure: the Framingham Heart Study. Circulation 2002; 106(24): 3068-72.
3. Stewart S, MacIntyre K, Capewell S, McMurray JJ. Heart failure and the aging population: an increasing burden in the 21st century? Heart 2003; 89(1): 49-53.
4. Felker GM, Thompson RE, Hare JM, et al. Underlying causes and long-term survival in patients with initially unexplained cardiomyopathy. N Engl J Med 2000; 342(15): 1077-84.
5. Leri A, Rota M, Hosoda T, Goichberg P, Anversa P. Cardiac stem cell niches. Stem Cell Res 2014; 13(3 Pt B): 631-46.
6. Leor J, Patterson M, Quinones MJ, Kedes LH, Kloner RA. Transplantation of fetal myocardial tissue into the infarcted myocardium of rat. A potential method for repair of infarcted myocardium? Circulation 1996; 94(9 Suppl): II332-6.
7. Taylor DA, Atkins BZ, Hungspreugs P, et al. Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat Med 1998; 4(8): 929-33.
8. Orlic D, Kajstura J, Chimenti S, et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001; 410(6829): 701-5.
9. Kocher AA, Schuster MD, Szabolcs MJ, et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 2001; 7(4): 430-6.
10. Menasche P, Hagege AA, Scorsin M, et al. Myoblast transplantation for heart failure. Lancet 2001; 357(9252): 279-80.
11. Assmus B, Schachinger V, Teupe C, et al. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation 2002; 106(24): 3009-17.
12. Psaltis PJ, Spoon DB, Wong DT, Gulati R. An update on stem cell therapies for acute coronary syndrome. Curr Cardiol Rep 2014; 16(9): 526.
13. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282(5391): 1145-7.
14. Mummery CL, Zhang J, Ng ES, Elliott DA, Elefanty AG, Kamp TJ. Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: a methods overview. Circ Res 2012; 111(3): 344-58.
15. Menard C, Hagege AA, Agbulut O, et al. Transplantation of cardiac- committed mouse embryonic stem cells to infarcted sheep myocardium: a preclinical study. Lancet 2005; 366(9490): 1005-12.
16. 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(1): 11-20.
17. Shiba Y, Fernandes S, Zhu WZ, et al. Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 2012; 489(7415): 322-5.
18. Fernandes S, Naumova AV, Zhu WZ, Laflamme MA, Gold J, Murry CE. Human embryonic stem cell-derived cardiomyocytes engraft but do not alter cardiac remodeling after chronic infarction in rats. J Mol Cell Cardiol 2010; 49(6): 941-9.
19. Chong JJ, Yang X, Don CW, et al. Human embryonic-stem-cellderived cardiomyocytes regenerate non-human primate hearts. Nature 2014; 510(7504): 273-7.
20. Cai J, Yi FF, Yang XC, et al. Transplantation of embryonic stem cell-derived cardiomyocytes improves cardiac function in infarcted rat hearts. Cytotherapy 2007; 9(3): 283-91.
21. Menasche P, Vanneaux V, Fabreguettes JR, et al. Towards a clinical use of human embryonic stem cell-derived cardiac progenitors: a translational experience. Eur Heart J 2014; 36(12): 743-50.
22. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663-76.
23. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318(5858): 1917-20.
24. Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, Woltjen K. Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 2009; 458(7239): 771-5.
25. Yu J, Hu K, Smuga-Otto K, et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009; 324(5928): 797-801.
26. Zhang J, Wilson GF, Soerens AG, et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 2009; 104(4): e30-41.
27. Nelson TJ, Martinez-Fernandez A, Yamada S, Perez-Terzic C, Ikeda Y, Terzic A. Repair of acute myocardial infarction by human stemness factors induced pluripotent stem cells. Circulation 2009; 120(5): 408-16.
28. Lalit PA, Hei DJ, Raval AN, Kamp TJ. Induced pluripotent stem cells for post-myocardial infarction repair: remarkable opportunities and challenges. Circ Res 2014; 114(8): 1328-45.
29. Aggarwal P, Turner A, Matter A, et al. RNA expression profiling of human iPSC-derived cardiomyocytes in a cardiac hypertrophy model. PLoS One 2014; 9(9): e108051.
30. Hashem SI, Perry CN, Bauer M, et al. Oxidative Stress Mediates Cardiomyocyte Apoptosis in a Human Model of Danon Disease and Heart Failure. Stem Cells 2015; 33(7): 2343-50.
31. Eschenhagen T, Mummery C, Knollmann BC. Modelling sarcomeric cardiomyopathies in the dish: from human heart samples to iPSC cardiomyocytes. Cardiovasc Res 2015; 105(4): 424-38.
32. Song K, Nam YJ, Luo X, et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 2012; 485(7400): 599-604.
33. Jayawardena TM, Egemnazarov B, Finch EA, et al. MicroRNAmediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ Res 2012; 110(11): 1465-73.
34. Wada R, Muraoka N, Inagawa K, et al. Induction of human cardiomyocyte- like cells from fibroblasts by defined factors. Proc Natl Acad Sci U S A 2013; 110(31): 12667-72.
35. Jayawardena TM, Finch EA, Zhang L, et al. MicroRNA induced cardiac reprogramming in vivo: evidence for mature cardiac myocytes and improved cardiac function. Circ Res 2015; 116(3): 418-24.
36. Hagege AA, Carrion C, Menasche P, et al. Viability and differentiation of autologous skeletal myoblast grafts in ischaemic cardiomyopathy. Lancet 2003; 361(9356): 491-2.
37. Suzuki K, Murtuza B, Suzuki N, Smolenski RT, Yacoub MH. Intracoronary infusion of skeletal myoblasts improves cardiac function in doxorubicin-induced heart failure. Circulation 2001; 104(12 Suppl 1): I213-7.
38. Steendijk P, Smits PC, Valgimigli M, van der Giessen WJ, Onderwater EE, Serruys PW. Intramyocardial injection of skeletal myoblasts: long-term follow-up with pressure-volume loops. Nat Clin Pract Cardiovasc Med 2006; 3(Suppl 1): S94-100.
39. Hagege AA, Marolleau JP, Vilquin JT, et al. Skeletal myoblast transplantation in ischemic heart failure: long-term follow-up of the first phase I cohort of patients. Circulation 2006; 114(1 Suppl): I108-13.
40. Reinecke H, Poppa V, Murry CE. Skeletal muscle stem cells do not transdifferentiate into cardiomyocytes after cardiac grafting. J Mol Cell Cardiol 2002; 34(2): 241-9.
41. Reinecke H, Minami E, Poppa V, Murry CE. Evidence for fusion between cardiac and skeletal muscle cells. Circ Res 2004; 94(6): e56-60.
42. Menasche P, Hagege AA, Vilquin JT, et al. Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J Am Coll Cardiol 2003; 41(7): 1078-83.
43. Chazaud B, Sonnet C, Lafuste P, et al. Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J Cell Biol 2003; 163(5): 1133-43.
44. Farahmand P, Lai TY, Weisel RD, et al. Skeletal myoblasts preserve remote matrix architecture and global function when im planted early or late after coronary ligation into infarcted or remote myocardium. Circulation 2008; 118(14 Suppl): S130-7.
45. Azarnoush K, Maurel A, Sebbah L, et al. Enhancement of the functional benefits of skeletal myoblast transplantation by means of coadministration of hypoxia-inducible factor 1alpha. J Thorac Cardiovasc Surg 2005; 130(1): 173-9.
46. 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(9): 1189-200.
47. Dib N, Dinsmore J, Lababidi Z, et al. One-year follow-up of feasibility and safety of the first U.S., randomized, controlled study using 3-dimensional guided catheter-based delivery of autologous skeletal myoblasts for ischemic cardiomyopathy (CAuSMIC study). JACC 2009; 2(1): 9-16.
48. 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(12): 1748-55.
49. Duckers HJ, Houtgraaf J, Hehrlein C, et al. Final results of a phase IIa, randomised, open-label trial to evaluate the percutaneous intramyocardial transplantation of autologous skeletal myoblasts in congestive heart failure patients: the SEISMIC trial. Eurointervention 2011; 6(7): 805-12.
50. Povsic TJ, O’Connor CM, Henry T, et al. A double-blind, randomized, controlled, multicenter study to assess the safety and cardiovascular effects of skeletal myoblast implantation by catheter delivery in patients with chronic heart failure after myocardial infarction. Am Heart J 2011; 162(4): 654-62 e1.
51. 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(6983): 668-73.
52. Kinnaird T, Stabile E, Burnett MS, Epstein SE. Bone-marrowderived cells for enhancing collateral development: mechanisms, animal data, and initial clinical experiences. Circ Res 2004; 95(4): 354-63.
53. Schachinger V, Erbs S, Elsasser 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(23): 2775-83.
54. 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(22): 2380-9.
55. Gyongyosi M, Wojakowski W, Lemarchand P, et al. Meta-Analysis of Cell-based CaRdiac stUdiEs (ACCRUE) in Patients With Acute Myocardial Infarction Based on Individual Patient Data. Circ Res 2015; 116(8): 1346-60.
56. Michelis KC, Boehm M, Kovacic JC. New vessel formation in the context of cardiomyocyte regeneration--the role and importance of an adequate perfusing vasculature. Stem Cell Res 2014; 13(3 Pt B): 666-82.
57. Bel A, Messas E, Agbulut O, et al. Transplantation of autologous fresh bone marrow into infarcted myocardium: a word of caution. Circulation 2003; 108(Suppl 1): II247-52.
58. Mathieu M, Bartunek J, El Oumeiri B, et al. Cell therapy with autologous bone marrow mononuclear stem cells is associated with superior cardiac recovery compared with use of nonmodified mesenchymal stem cells in a canine model of chronic myocardial infarction. J Thorac Cardiovasc Surg 2009; 138(3): 646-53.
59. Perin EC, Dohmann HF, Borojevic R, et al. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 2003; 107(18): 2294-302.
60. Perin EC, Dohmann HF, Borojevic R, et al. Improved exercise capacity and ischemia 6 and 12 months after transendocardial injection of autologous bone marrow mononuclear cells for ischemic cardiomyopathy. Circulation 2004; 110(11 Suppl 1): II213-8.
61. Beeres SL, Bax JJ, Dibbets-Schneider P, et al. Intramyocardial injection of autologous bone marrow mononuclear cells in patients with chronic myocardial infarction and severe left ventricular dysfunction. Am J Cardiol 2007; 100(7): 1094-8.
62. 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(1 Suppl): I101-7.
63. Assmus B, Honold J, Schachinger V, et al. Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med 2006; 355(12): 1222-32.
64. Assmus B, Fischer-Rasokat U, Honold J, et al. 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(8): 1234-41.
65. Honold J, Fischer-Rasokat U, Seeger FH, et al. Impact of intracoronary reinfusion of bone marrow-derived mononuclear progenitor cells on cardiopulmonary exercise capacity in patients with chronic postinfarction heart failure. Clin Res Cardiol 2013; 102(9): 619-25.
66. Assmus B, Walter DH, Seeger FH, et al. Effect of shock wavefacilitated intracoronary cell therapy on LVEF in patients with chronic heart failure: the CELLWAVE randomized clinical trial. JAMA 2013; 309(15): 1622-31.
67. Perin EC, Willerson JT, Pepine CJ, et al. Effect of transendocardial delivery of autologous bone marrow mononuclear cells on functional capacity, left ventricular function, and perfusion in chronic heart failure: the FOCUS-CCTRN trial. JAMA 2012; 307(16): 1717-26.
68. Seth S, Narang R, Bhargava B, et al. Percutaneous intracoronary cellular cardiomyoplasty for nonischemic cardiomyopathy: clinical and histopathological results: the first-in-man ABCD (Autologous Bone Marrow Cells in Dilated Cardiomyopathy) trial. J Am Coll Cardiol 2006; 48(11): 2350-1.
69. Fischer-Rasokat U, Assmus B, Seeger FH, et al. A pilot trial to assess potential effects of selective intracoronary bone marrowderived progenitor cell infusion in patients with nonischemic dilated cardiomyopathy: final 1-year results of the transplantation of progenitor cells and functional regeneration enhancement pilot trial in patients with nonischemic dilated cardiomyopathy. Circ Heart Fail 2009; 2(5): 417-23.
70. Cogle CR, Wise E, Meacham AM, et al. A Detailed Analysis of Bone Marrow from Patients with Ischemic Heart Disease and Left Ventricular Dysfunction: BM CD34, CD11b and Clonogenic Capacity as Biomarkers for Clinical Outcomes. Circ Res 2014; 115(10): 867-74.
71. Heeschen C, Lehmann R, Honold J, et al. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation 2004; 109(13): 1615-22.
72. Seeger FH, Tonn T, Krzossok N, Zeiher AM, Dimmeler S. 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(6): 766-72.
73. Seeger FH, Rasper T, Fischer A, et al. Heparin disrupts the CXCR4/SDF-1 axis and impairs the functional capacity of bone marrow-derived mononuclear cells used for cardiovascular repair. Circ Res 2012; 111(7): 854-62.
74. Henry TD, Traverse JH, Hammon BL, et al. Safety and efficacy of ixmyelocel-T: an expanded, autologous multi-cellular therapy, in dilated cardiomyopathy. Circ Res 2014; 115(8): 730-7.
75. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275(5302): 964-7.
76. Psaltis PJ, Simari RD. Vascular Wall Progenitor Cells in Health and Disease. Circ Res 2015; 116(8): 1392-412.
77. Kawamoto A, Tkebuchava T, Yamaguchi J, et al. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 2003; 107(3): 461-8.
78. Nasseri BA, Ebell W, Dandel M, et al. Autologous CD133+ bone marrow cells and bypass grafting for regeneration of ischaemic myocardium: the Cardio133 trial. Eur Heart J 2014; 35(19): 1263-74.
79. Poglajen G, Sever M, Cukjati M, et al. Effects of Transendocardial CD34+ Cell Transplantation in Patients With Ischemic Cardiomyopathy. Circ Cardiovasc Interv 2014; 7(4): 552-9.
80. Vrtovec B, Poglajen G, Sever M, et al. Effects of intracoronary stem cell transplantation in patients with dilated cardiomyopathy. J Card Fail 2011; 17(4): 272-81.
81. 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(1): 165-73.
82. Vrtovec B, Poglajen G, Lezaic L, et al. Comparison of transendocardial and intracoronary CD34+ cell transplantation in patients with nonischemic dilated cardiomyopathy. Circulation 2013; 128(11 Suppl 1): S42-9.
83. Psaltis PJ, Spoon DB, Wong DT. Utility of mesenchymal stromal cells for myocardial infarction. Transitioning from bench to bedside. Minerva Cardioangiol 2013; 61(6): 639-63.
84. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284(5411): 143-7.
85. Psaltis PJ, Paton S, See F, et al. Enrichment for STRO-1 expression enhances the cardiovascular paracrine activity of human bone marrow- derived mesenchymal cell populations. J Cell Physiol 2010; 223(2): 530-40.
86. See F, Seki T, Psaltis PJ, et al. Therapeutic effects of human STRO-3-selected mesenchymal precursor cells and their soluble factors in experimental myocardial ischemia. J Cell Mol Med 2011; 15(10): 2117-29.
87. Richardson JD, Nelson AJ, Zannettino AC, Gronthos S, Worthley SG, Psaltis PJ. Optimization of the cardiovascular therapeutic properties of mesenchymal stromal/stem cells-taking the next step. Stem Cell Rev 2013; 9(3): 281-302.
88. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006; 98(5): 1076-84.
89. 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 U S A 2009; 106(33): 14022-7.
90. Silva GV, Litovsky S, Assad JA, et al. Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 2005; 111(2): 150-6.
91. Psaltis PJ, Carbone A, Nelson AJ, et al. Reparative effects of allogeneic mesenchymal precursor cells delivered transendocardially in experimental nonischemic cardiomyopathy. JACC 2010; 3(9): 974-83.
92. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008; 103(11): 1204-19.
93. Hatzistergos KE, Quevedo H, Oskouei BN, et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res 2010; 107(7): 913-22.
94. Heldman AW, DiFede DL, Fishman JE, et al. Transendocardial mesenchymal stem cells and mononuclear bone marrow cells for ischemic cardiomyopathy: the TAC-HFT randomized trial. JAMA 2014; 311(1): 62-73.
95. Hare JM, Fishman JE, Gerstenblith G, et al. Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA 2012; 308(22): 2369-79.
96. Suncion VY, Ghersin E, Fishman JE, et al. Does transendocardial injection of mesenchymal stem cells improve myocardial function locally or globally?: An analysis from the Percutaneous Stem Cell Injection Delivery Effects on Neomyogenesis (POSEIDON) randomized trial. Circ Res 2014; 114(8): 1292-301.
97. Karantalis V, DiFede DL, Gerstenblith G, et al. Autologous mesenchymal stem cells produce concordant improvements in regional function, tissue perfusion, and fibrotic burden when administered to patients undergoing coronary artery bypass grafting: The Prospective Randomized Study of Mesenchymal Stem Cell Therapy in Patients Undergoing Cardiac Surgery (PROMETHEUS) trial. Circ Res 2014; 114(8): 1302-10.
98. Miyahara Y, Nagaya N, Kataoka M, et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 2006; 12(4): 459-65.
99. Perin EC, Sanz-Ruiz R, Sanchez PL, et al. Adipose-derived regenerative cells in patients with ischemic cardiomyopathy: The PRECISE Trial. Am Heart J 2014; 168(1): 88-95 e2.
100. Behfar A, Terzic A. Derivation of a cardiopoietic population from human mesenchymal stem cells yields cardiac progeny. Nat Clin Pract Cardiovasc Med 2006; 3 Suppl 1: S78-82.
101. 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(9): 721-34.
102. Bartunek J, Behfar A, Dolatabadi D, et al. Cardiopoietic stem cell therapy in heart failure The C-CURE multicenter randomized trial with lineage-specified biologics. J Am Coll Cardiol 2013; 61(23): 2329-38.
103. 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(9806): 1847-57.
104. Makkar RR, Smith RR, Cheng K, et al. Intracoronary cardiospherederived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 2012; 379(9819): 895-904.
105. Laugwitz KL, Moretti A, Lam J, et al. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005; 433(7026): 647-53.
106. Linke A, Muller P, Nurzynska D, et al. Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc Natl Acad Sci U S A 2005; 102(25): 8966-71.
107. Bearzi C, Rota M, Hosoda T, et al. Human cardiac stem cells. Proc Natl Acad Sci U S A 2007; 104(35): 14068-73.
108. Oh H, Bradfute SB, Gallardo TD, et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 2003; 100(21): 12313-8.
109. Chong JJ, Chandrakanthan V, Xaymardan M, et al. Adult cardiacresident MSC-like stem cells with a proepicardial origin. Cell Stem Cell 2011; 9(6): 527-40.
110. Sereti KI, Oikonomopoulos A, Unno K, Cao X, Qiu Y, Liao R. ATP-binding cassette G-subfamily transporter 2 regulates cell cycle progression and asymmetric division in mouse cardiac side population progenitor cells. Circ Res 2012; 112(1): 27-34.
111. Smart N, Risebro CA, Melville AA, et al. Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 2007; 445(7124): 177-82.
112. 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(9): 911-21.
113. 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(4): 455-65.
114. Urbanek K, Torella D, Sheikh F, et al. Myocardial regeneration by activation of multipotent cardiac stem cells in ischemic heart failure. Proc Natl Acad Sci U S A 2005; 102(24): 8692-7.
115. 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(2): 293-305.
116. Bolli R, Tang XL, Sanganalmath SK, et al. Intracoronary delivery of autologous cardiac stem cells improves cardiac function in a porcine model of chronic ischemic cardiomyopathy. Circulation 2013; 128(2): 122-31.
117. Zaruba MM, Soonpaa M, Reuter S, Field LJ. Cardiomyogenic potential of C-kit(+)-expressing cells derived from neonatal and adult mouse hearts. Circulation 2010; 121(18): 1992-2000.
118. van Berlo JH, Kanisicak O, Maillet M, et al. c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature 2014; 509(7500): 337-41.
119. Chugh AR, Beache GM, Loughran JH, et al. Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation 2012; 126(11 Suppl 1): S54-64.
120. Nowbar AN, Mielewczik M, Karavassilis M, et al. Discrepancies in autologous bone marrow stem cell trials and enhancement of ejection fraction (DAMASCENE): weighted regression and metaanalysis. BMJ 2014; 348: g2688.
121. Smith RR, Barile L, Cho HC, et al. Regenerative potential of cardiosphere- derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007; 115(7): 896-908.
122. 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(12): 1075-83, 7 p following 83.
123. Aminzadeh MA, Tseliou E, Sun B, et al. Therapeutic efficacy of cardiosphere-derived cells in a transgenic mouse model of nonischaemic dilated cardiomyopathy. Eur Heart J 2014; 36(12): 751-62.
124. Malliaras K, Ibrahim A, Tseliou E, et al. Stimulation of endogenous cardioblasts by exogenous cell therapy after myocardial infarction. EMBO Mol Med 2014; 6(6): 760-77.
125. Xie Y, Ibrahim A, Cheng K, et al. Importance of cell-cell contact in the therapeutic benefits of cardiosphere-derived cells. Stem Cells 2014; 32(9): 2397-406.
126. Li TS, Cheng K, Malliaras K, et al. Direct comparison of different stem cell types and subpopulations reveals superior paracrine potency and myocardial repair efficacy with cardiosphere-derived cells. J Am Coll Cardiol 2012; 59(10): 942-53.
127. Cheng K, Malliaras K, Smith RR, et al. Human cardiospherederived cells from advanced heart failure patients exhibit augmented functional potency in myocardial repair. JACC Heart Fail 2014; 2(1): 49-61.
128. Tseliou E, Pollan S, Malliaras K, et al. Allogeneic cardiospheres safely boost cardiac function and attenuate adverse remodeling after myocardial infarction in immunologically mismatched rat strains. J Am Coll Cardiol 2013; 61(10): 1108-19.
129. Malliaras K, Li TS, Luthringer D, et al. Safety and efficacy of allogeneic cell therapy in infarcted rats transplanted with mismatched cardiosphere-derived cells. Circulation 2012; 125(1): 100-12.
130. Malliaras K, Makkar RR, Smith RR, et al. Intracoronary cardiosphere- derived cells after myocardial infarction: evidence of therapeutic regeneration in the final 1-year results of the CADUCEUS trial (CArdiosphere-Derived aUtologous stem CElls to reverse ventricUlar dySfunction). J Am Coll Cardiol 2013; 63(2): 110-22.
131. Fisher SA, Doree C, Mathur A, Martin-Rendon E. Meta-analysis of cell therapy trials for patients with heart failure. Circ Res 2015; 116(8): 1361-77.
132. Yao K, Huang R, Qian J, et al. Administration of intracoronary bone marrow mononuclear cells on chronic myocardial infarction improves diastolic function. Heart 2008; 94(9): 1147-53.
133. Ang KL, Chin D, Leyva F, et al. Randomized, controlled trial of intramuscular or intracoronary injection of autologous bone marrow cells into scarred myocardium during CABG versus CABG alone. Nat Clin Pract Cardiovasc Med 2008; 5(10): 663-70.
134. Zhao Q, Sun Y, Xia L, Chen A, Wang Z. Randomized study of mononuclear bone marrow cell transplantation in patients with coronary surgery. Ann Thorac Surg 2008; 86(6): 1833-40.
135. Pokushalov E, Romanov A, Chernyavsky A, et al. Efficiency of intramyocardial injections of autologous bone marrow mononuclear cells in patients with ischemic heart failure: a randomized study. J Cardiovasc Transl Res 2010; 3(2): 160-8.
136. Perin EC, Silva GV, Henry TD, et al. A randomized study of transendocardial injection of autologous bone marrow mononuclear cells and cell function analysis in ischemic heart failure (FOCUSHF). Am Heart J 2011; 161(6): 1078-87 e3.
137. Hu S, Liu S, Zheng Z, et al. Isolated coronary artery bypass graft combined with bone marrow mononuclear cells delivered through a graft vessel for patients with previous myocardial infarction and chronic heart failure: a single-center, randomized, double-blind, placebo-controlled clinical trial. J Am Coll Cardiol 2011; 57(24): 2409-15.
138. Turan RG, Bozdag TI, Ortak J, et al. Improved functional activity of bone marrow derived circulating progenitor cells after intra coronary freshly isolated bone marrow cells transplantation in patients with ischemic heart disease. Stem Cell Reviews 2011; 7(3): 646-56.
139. Patila T, Lehtinen M, Vento A, et al. Autologous bone marrow mononuclear cell transplantation in ischemic heart failure: a prospective, controlled, randomized, double-blind study of cell transplantation combined with coronary bypass. J Heart Lung Transplant 2014; 33(6): 567-74.
140. Perin EC, Silva GV, Zheng Y, et al. Randomized, double-blind pilot study of transendocardial injection of autologous aldehyde dehydrogenase-bright stem cells in patients with ischemic heart failure. Am Heart J. 2012; 163(3): 415-21, 21 e1.
141. Honold J, Fischer-Rasokat U, Lehmann R, et al. G-CSF stimulation and coronary reinfusion of mobilized circulating mononuclear proangiogenic cells in patients with chronic ischemic heart disease: five-year results of the TOPCARE-G-CSF trial. Cell Transplant 2012; 21(11): 2325-37.
142. Mozid A, Yeo C, Arnous S, et al. Safety and feasibility of intramyocardial versus intracoronary delivery of autologous cell therapy in advanced heart failure: the REGENERATE-IHD pilot study. Regen Med 2014; 9(3): 269-78.
143. Yeh ET, Zhang S, Wu HD, Korbling M, Willerson JT, Estrov Z. Transdifferentiation of human peripheral blood CD34+-enriched cell population into cardiomyocytes, endothelial cells, and smooth muscle cells in vivo. Circulation 2003; 108(17): 2070-3.
144. Zhang S, Wang D, Estrov Z, Raj S, Willerson JT, Yeh ET. Both cell fusion and transdifferentiation account for the transformation of human peripheral blood CD34-positive cells into cardiomyocytes in vivo. Circulation 2004; 110(25): 3803-7.
145. Dawn B, Stein AB, Urbanek K, et al. Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc Natl Acad Sci U S A 2005; 102(10): 3766-71.
146. Malliaras K, Zhang Y, Seinfeld J, et al. Cardiomyocyte proliferation and progenitor cell recruitment underlie therapeutic regeneration after myocardial infarction in the adult mouse heart. EMBO Mol Med 2013; 5(2): 191-209.
147. Sahoo S, Klychko E, Thorne T, et al. Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circ Res 2011; 109(7): 724-8.
148. Gnecchi M, He H, Liang OD, et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 2005; 11(4): 367-8.
149. Rota M, Padin-Iruegas ME, Misao Y, et al. Local activation or implantation of cardiac progenitor cells rescues scarred infarcted myocardium improving cardiac function. Circ Res 2008; 103(1): 107-16.
150. Ben-Mordechai T, Holbova R, Landa-Rouben N, et al. Macrophage subpopulations are essential for infarct repair with and without stem cell therapy. J Am Coll Cardiol 2013; 62(20): 1890-901.
151. Dixon JA, Gorman RC, Stroud RE, et al. Mesenchymal cell transplantation and myocardial remodeling after myocardial infarction. Circulation 2009; 120(11 Suppl): S220-9.
152. Gnecchi M, He H, Melo LG, et al. Early beneficial effects of bone marrow-derived mesenchymal stem cells overexpressing Akt on cardiac metabolism after myocardial infarction. Stem Cells 2009; 27(4): 971-9.
153. Mills WR, Mal N, Kiedrowski MJ, et al. Stem cell therapy enhances electrical viability in myocardial infarction. J Mol Cell Cardiol 2007; 42(2): 304-14.
154. Kinnaird T, Stabile E, Burnett MS, et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004; 94(5): 678-85.
155. Lai RC, Arslan F, Lee MM, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res 2010; 4(3): 214-22.
156. Mazo M, Gavira JJ, Abizanda G, et al. Transplantation of mesenchymal stem cells exerts a greater long-term effect than bone marrow mononuclear cells in a chronic myocardial infarction model in rat. Cell Transplant 2010; 19(3): 313-28.
157. Zhang S, Ge J, Sun A, et al. Comparison of various kinds of bone marrow stem cells for the repair of infarcted myocardium: Single clonally purified non-hematopoietic mesenchymal stem cells serve as a superior source. J Cell Biochem 2006.
158. Shintani Y, Fukushima S, Varela-Carver A, et al. Donor cell-type specific paracrine effects of cell transplantation for post-infarction heart failure. J Mol Cell Cardiol 2009; 47(2): 288-95.
159. van der Bogt KE, Sheikh AY, Schrepfer S, et al. Comparison of different adult stem cell types for treatment of myocardial ischemia. Circulation 2008; 118(14 Suppl): S121-9.
160. Gaebel R, Furlani D, Sorg H, et al. Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration. PLoS One 2011; 6(2): e15652.
161. Jansen Of Lorkeers SJ, Eding JE, Vesterinen HM, et al. Similar effect of autologous and allogeneic cell therapy for ischemic heart disease: systematic review and meta-analysis of large animal studies. Circ Res 2015; 116(1): 80-6.
162. Ott HC, Bonaros N, Marksteiner R, et al. Combined transplantation of skeletal myoblasts and bone marrow stem cells for myocardial repair in rats. Eur J Cardiothorac Surg 2004; 25(4): 627-34.
163. Williams AR, Hatzistergos KE, Addicott B, et al. Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction. Circulation 2012; 127(2): 213-23.
164. Hamamoto H, Gorman JH, 3rd, Ryan LP, et al. Allogeneic mesenchymal precursor cell therapy to limit remodeling after myocardial infarction: the effect of cell dosage. Ann Thorac Surg 2009; 87(3): 794-801.
165. Gavira JJ, Nasarre E, Abizanda G, et al. Repeated implantation of skeletal myoblast in a swine model of chronic myocardial infarction. Eur Heart J 2010; 31(8): 1013-21.
166. Richardson JD, Psaltis PJ, Frost L, et al. Incremental benefits of repeated mesenchymal stromal cell administration compared with solitary intervention after myocardial infarction. Cytotherapy 2014; 16(4): 460-70.
167. Diederichsen AC, Moller JE, Thayssen P, et al. Effect of repeated intracoronary injection of bone marrow cells in patients with ischaemic heart failure the Danish stem cell study--congestive heart failure trial (DanCell-CHF). Eur J Heart Fail 2008; 10(7): 661-7.
168. Hare JM, Traverse JH, Henry TD, et al. A randomized, doubleblind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 2009; 54(24): 2277-86.
169. De Rosa S, Seeger FH, Honold J, et al. Procedural safety and predictors of acute outcome of intracoronary administration of progenitor cells in 775 consecutive procedures performed for acute myocardial infarction or chronic heart failure. Circ Cardiovasc Interv 2013; 6(1): 44-51.
170. Kang HJ, Kim HS, Koo BK, et al. Intracoronary infusion of the mobilized peripheral blood stem cell by G-CSF is better than mobilization alone by G-CSF for improvement of cardiac function and remodeling: 2-year follow-up results of the Myocardial Regeneration and Angiogenesis in Myocardial Infarction with G-CSF and Intra-Coronary Stem Cell Infusion (MAGIC Cell) 1 trial. Am Heart J 2007; 153(2): 237 e1-8.
171. 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(9): 1114-22.
172. Perin EC, Silva GV, Assad JA, et al. Comparison of intracoronary and transendocardial delivery of allogeneic mesenchymal cells in a canine model of acute myocardial infarction. J Mol Cell Cardiol 2008; 44(3): 486-95.
173. Psaltis PJ, Carbone A, Leong DP, et al. Assessment of myocardial fibrosis by endoventricular electromechanical mapping in experimental nonischemic cardiomyopathy. Int J Cardiovasc Imaging 2011; 27(1): 25-37.
174. Hudson W, Collins MC, deFreitas D, Sun YS, Muller-Borer B, Kypson AP. Beating and arrested intramyocardial injections are associated with significant mechanical loss: implications for cardiac cell transplantation. J Surg Res 2007; 142(2): 263-7.
175. Mitchell AJ, Sabondjian E, Sykes J, et al. Comparison of initial cell retention and clearance kinetics after subendocardial or subepicardial injections of endothelial progenitor cells in a canine myocardial infarction model. J Nucl Med 2010; 51(3): 413-7.
176. Hou D, Youssef EA, 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.
177. Siminiak T, Fiszer D, Jerzykowska O, et al. Percutaneous transcoronary- venous transplantation of autologous skeletal myoblasts in the treatment of post-infarction myocardial contractility impairment: the POZNAN trial. Eur Heart J 2005; 26(12): 1188-95.
178. Tuma J, Fernandez-Vina R, Carrasco A, et al. Safety and feasibility of percutaneous retrograde coronary sinus delivery of autologous bone marrow mononuclear cell transplantation in patients with chronic refractory angina. J Transl Med 2011; 9: 183.
179. Psaltis PJ, Zannettino AC, Gronthos S, Worthley SG. Intramyocardial navigation and mapping for stem cell delivery. J Cardiovasc Transl Res 2010; 3(2): 135-46.
180. 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(1): 48-62.
181. Botker HE, Lassen JF, Hermansen F, et al. Electromechanical mapping for detection of myocardial viability in patients with ischemic cardiomyopathy. Circulation 2001; 103(12): 1631-7.
182. Dick AJ, Guttman MA, Raman VK, et al. Magnetic resonance fluoroscopy allows targeted delivery of mesenchymal stem cells to infarct borders in Swine. Circulation 2003; 108(23): 2899-904.
183. Baklanov DV, de Muinck ED, Simons M, et al. Live 3D echo guidance of catheter-based endomyocardial injection. Catheter Cardiovasc Interv 2005; 65(3): 340-5.
184. Hong KU, Li QH, Guo Y, et al. A highly sensitive and accurate method to quantify absolute numbers of c-kit+ cardiac stem cells following transplantation in mice. Basic Res Cardiol 2013; 108(3): 346.
185. Hofmann M, Wollert KC, Meyer GP, et al. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 2005; 111(17): 2198-202.
186. Godier-Furnemont AF, Martens TP, Koeckert MS, et al. Composite scaffold provides a cell delivery platform for cardiovascular repair. Proc Natl Acad Sci U S A 2011; 108(19): 7974-9.
187. Behfar A, Latere JP, Bartunek J, et al. Optimized delivery system achieves enhanced endomyocardial stem cell retention. Circ Cardiovasc Interv 2013; 6(6): 710-8.
188. Psaltis PJ, Simari RD, Rodriguez-Porcel M. Emerging roles for integrated imaging modalities in cardiovascular cell-based therapeutics: a clinical perspective. Eur J Nucl Med Mol Imaging 2011; 39(1): 165-81.
189. Ascheim DD, Gelijns AC, Goldstein D, et al. Mesenchymal precursor cells as adjunctive therapy in recipients of contemporary left ventricular assist devices. Circulation 2014; 129(22): 2287-96.