Ann Thorac Surg 2007;84:339-342
© 2007 The Society of Thoracic Surgeons
Key References
Cellular Therapy in Thoracic and Cardiovascular Disease
Philippe Menasche, MD, PhD*
Assistance Publique-Hopitaux de Paris, Hôpital Européen Georges Pompidou, Department of Cardiovascular Surgery; University Paris-Descartes, Faculty of Medicine, Paris, France
* Address correspondence to Dr Menasche, Hôpital Européen Georges Pompidou, Department of Cardiovascular Surgery, 20, rue Leblanc, Paris, 75015, France (Email: philippe.menasche{at}egp.aphp.fr).
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Reviews
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- 1 Melo LG, Pachori AS, Kong D, et al. Molecular and cell-based therapies for protection, rescue, and repair of ischemic myocardium: reasons for cautious optimism. Circulation 2004;109:2386–93.
- 2 Dimmeler S, Zeiher AM, Schneider MD. Unchain my heart: the scientific foundations of cardiac repair. Clin Invest 2005;115:572–83.
- 3 Murry CE, Field LJ, Menasche P. Cell-based cardiac repair: reflections at the 10-year point. Circulation 2005;112:3174–83.
- 4 Fazel S, Tang GH, Angoulvant D, et al. Current status of cellular therapy for ischemic heart disease. Ann Thorac Surg 2005;79:S2238–47.
- 5 Sanchez PL, San Roman JA, Villa A, et al. Contemplating the bright future of stem cell therapy for cardiovascular disease. Nat Clin Pract Cardiovasc Med 2006;(Suppl 1):S138–51.
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Adult Somatic Cells
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Skeletal Myoblasts
Experimental studies
- 6 Murry CE, Wiseman RW, Schwartz SM, et al. Skeletal myoblast transplantation for repair of myocardial necrosis. J Clin Invest 1996;98:2512–23.
- 7 Taylor DA, Atkins BZ, Hungspreugs P, et al. Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat Med 1998;4:929–33. Erratum in: Nat Med 1998;4:1200.
- 8 Reinecke H, Poppa V, Murry CE. Skeletal muscle stem cells do not transdifferentiate into cardiomyocytes after cardiac grafting. J Mol Cell Cardiol 2002;34:241–9.
- 9 Suzuki K, Murtuza B, Beauchamp JR, et al. Dynamics and mediators of acute graft attrition after myoblast transplantation to the heart. FASEB J 2004;18:1153–5.
- 10 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 Cardio-thorac Surg 2004;25:627–34.
- 11 Christman KL, Vardanian AJ, Fang Q, et al. Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J Am Coll Cardiol 2004;44:654–60.
- 12 Maurel A, Azarnoush K, Sabbah L, et al. Can cold or heat shock improve skeletal myoblast engraftment in infarcted myocardium? Transplantation 2005;5;80:660–5.
- 13 Yau TM, Kim C, Ng D, et al. Increasing transplanted cell survival with cell-based angiogenic gene therapy. Ann Thorac Surg 2005;80:1779–86.
- 14 McConnell PI, del Rio CL, Jacoby DB, et al. Correlation of autologous skeletal myoblast survival with changes in left ventricular remodeling in dilated ischemic heart failure. J Thorac Cardiovasc Surg 2005;130:1001.
- 15 Ott HC, Kroess R, Bonaros N, et al. Intramyocardial microdepot injection increases the efficacy of skeletal myoblast transplantation. Eur J Cardio-thorac Surg 2005;27:1017–21.
- 16 Tambara K, Premaratne GU, Sakaguchi G, et al. Administration of control-released hepatocyte growth factor enhances the efficacy of skeletal myoblast transplantation in rat infarcted hearts by greatly increasing both quantity and quality of the graft. Circulation 2005;112(Suppl I):I129–34.
- 17 Memon IA, Sawa Y, Fukushima N, et al. Repair of impaired myocardium by means of implantation of engineered autologous myoblast sheets. J Thorac Cardiovasc Surg 2005;130:1333–41.
- 18 Memon IA, Sawa Y, Miyagawa S, et al. Combined autologous cellular cardiomyoplasty with skeletal myoblasts and bone marrow cells in canine hearts for ischemic cardiomyopathy. J Thorac Cardiovasc Surg 2005;130:646–53.
- 19 Van den Bos EJ, Thompson RB, Wagner A, et al. Functional assessment of myoblast transplantation for cardiac repair with magnetic resonance imaging. Eur J Heart Fail 2005;7:435–43.
- 20 Kondoh H, Sawa Y, Miyagawa S, et al. Longer preservation of cardiac performance by sheet-shaped myoblast implantation in dilated cardiomyopathic hamsters. Cardiovasc Res 2006;69:466–75.
Arrhythmias
- 21 Reinecke H, MacDonald GH, Hauschka SD, et al. Electromechanical coupling between skeletal and cardiac muscle. Implications for infarct repair. J Cell Biol 2000;149:731–40.
- 22 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;114:775–83.
- 23 Abraham MR, Henrikson CA, Tung L, et al. Antiarrhythmic engineering of skeletal myoblasts for cardiac transplantation. Circ Res 2005;97:159–67.
- 24 Itabashi Y, Miyoshi S, Yuasa S, et al. Analysis of the electrophysiological properties and arrhythmias in directly contacted skeletal and cardiac muscle cell sheets. Cardiovasc Res 2005;67:561–70.
- 25 Fernandes S, Amirault JC, Lande G, et al. Autologous myoblast transplantation after myocardial infarction increases the inducibility of ventricular arrhythmias. Cardiovasc Res 2006;6:348–58.
- 26 Fouts K, Fernandes B, Mal N, Liu J, et al. Electrophysiological consequence of skeletal myoblast transplantation in normal and infarcted canine myocardium. Heart Rhythm 2006;3:452–61.
Clinical studies
- 27 Pagani FD, DerSimonian H, Zawadzka A, et al. Autologous skeletal myoblasts transplanted to ischemia-damaged myocardium in humans. Histological analysis of cell survival and differentiation. J Am Coll Cardiol 2003;41:879–88.
- 28 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.
- 29 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;148:531–7.
- 30 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;26:1188–95.
- 31 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;112:1748–55.
- 32 Gavira JJ, Herreros J, Perez A, et al. Autologous skeletal myoblast transplantation in patients with nonacute myocardial infarction: 1-year follow-up. J Thorac Cardiovasc Surg 2006;131:799–804.
Bone Marrow Cells
Experimental studies
- 33 Shake JG, Gruber PJ, Baumgartner WA, et al. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann Thorac Surg 2002;73:1919–25; discussion 1926.
- 34 Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41–9.
- 35 Rangappa S, Entwistle JW, Wechsler AS, et al. Cardiomyocyte-mediated contact programs human mesenchymal stem cells to express cardiogenic phenotype. J Thorac Cardiovasc Surg 2003;126:124–32.
- 36 Medvinsky A, Smith A. Stem cells: fusion brings down barriers. Nature 2003;422:823–5.
- 37 Skowasch D, Jabs A, Andrie R, et al. Presence of bone-marrow- and neural-crest-derived cells in intimal hyperplasia at the time of clinical in-stent restenosis. Cardiovasc Res 2003;60:684–91.
- 38 Nygren JM, Jovinge S, Breitbach M, et al. Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat Med 2004;10:494–501.
- 39 Yoon YS, Park JS, Tkebuchava T, et al. Unexpected severe calcification after transplantation of bone marrow cells in acute myocardial infarction. Circulation 2004;109:3154–7.
- 40 Yau TM, Kim C, Li G, Zhang Y, et al. Maximizing ventricular function with multimodal cell-based gene therapy. Circulation 2005;112(Suppl I):I123–8.
- 41 Amado LC, Saliaris AP, Schuleri KH, et al. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc Natl Acad Sci U S A 2005;102:11474–9.
- 42 Dai W, Hale SL, Martin BJ, et al. Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium: short- and long-term effects. Circulation 2005;112:214–23.
- 43 Rubio D, Garcia-Castro J, Martin MC, et al. Spontaneous human adult stem cell transformation. Cancer Res 2005;65:3035–9. Erratum in: Cancer Res 2005;65:4969.
- 44 Yoon YS, Wecker A, Heyd L, et al. Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J Clin Invest 2005;115:326–38.
- 45 Ryan JM, Barry FP, Murphy JM, et al. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm (Lond) 2005;2:8.
- 46 Nagaya N, Kangawa K, Itoh T, et al. Transplantation of mesenchymal stem cells improves cardiac function in a rat model of dilated cardiomyopathy. Circulation 2005;112:1128–35.
- 47 Chang MG, Tung L, Sekar RB, et al. Proarrhythmic potential of mesenchymal stem cell transplantation revealed in an in vitro coculture model. Circulation 2006;113:1832–41.
- 48 Miyahara Y, Nagaya N, Kataoka M, et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 2006;12:459–65.
Hematopoietic progenitors
- 49 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;7:430–6.
- 50 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.
- 51 Balsam LB, Wagers AJ, Christensen JL, et al. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 2004;428:668–73.
- 52 Limbourg FP, Ringes-Lichtenberg S, Schaefer A, et al. Haematopoietic stem cells improve cardiac function after infarction without permanent cardiac engraftment. Eur J Heart Fail 2005;7:722–9.
- 53 Lagostena L, Avitabile D, De Falco E, et al. Electrophysiological properties of mouse bone marrow c-kit+ cells co-cultured onto neonatal cardiac myocytes. Cardiovasc Res 2005;66:482–92.
- 54 Yoshioka T, Ageyama N, Shibata H, et al. Repair of infarcted myocardium mediated by transplanted bone marrow-derived CD34+ stem cells in a nonhuman primate model. Stem Cells 2005;23:355–64.
Endothelial progenitors
- 55 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.
- 56 Szmitko PE, Fedak PW, Weisel RD, et al. Endothelial progenitor cells: new hope for a broken heart. Circulation 2003;107:3093–100 (review).
- 57 Zimmermann WH, Eschenhagen T. Questioning the relevance of circulating cardiac progenitor cells in cardiac regeneration. Cardiovasc Res 2005;68:344–6.
- 58 Schmidt-Lucke C, Rossig L, Fichtlscherer S, et al. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation 2005;111:2981–7.
Clinical studies
- 59 Strauer BE, Brehm M, Zeus T, Kostering M, et al. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 2002;106:1913–8.
- 60 Stamm C, Westphal B, Kleine HD, et al. Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 2003;361:45–6.
- 61 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;109:1615–22.
- 62 Schachinger V, Assmus B, Britten MB, et al. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: final one-year results of the TOPCARE-AMI Trial. J Am Coll Cardiol 2004;44:1690–9.
- 63 Galinanes M, Loubani M, Davies J, et al. Autotransplantation of unmanipulated bone marrow into scarred myocardium is safe and enhances cardiac function in humans. Cell Transplant 2004;13:7–13.
- 64 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(Suppl II):II213–8.
- 65 Hofmann M, Wollert KC, Meyer GP, et al. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 2005;111:2198–202.
- 66 Strauer BE, Brehm M, Zeus T, et al. Regeneration of human infarcted heart muscle by intracoronary autologous bone marrow cell transplantation in chronic coronary artery disease: the IACT Study. J Am Coll Cardiol 2005;46:1651–8.
- 67 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 (Bone marrow transfer to enhance ST-elevation infarct regeneration) trial. Circulation 2006;113:1287–94.
- 68 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.
Mobilization and Homing
- 69 Orlic D, Kajstura J, Chimenti S, et al. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A 2001;98:10344–9.
- 70 Deten A, Volz HC, Clamors S, et al. Hematopoietic stem cells do not repair the infarcted mouse heart. Cardiovasc Res 2005;65:52–63.
- 71 Harada M, Qin Y, Takano H, et al. G-CSF prevents cardiac remodeling after myocardial infarction by activating the Jak-Stat pathway in cardiomyocytes. Nat Med 2005;11:305–11.
- 72 Ripa RS, Jorgensen E, Wang Y, et al. Stem cell mobilization induced by subcutaneous granulocyte-colony stimulating factor to improve cardiac regeneration after acute ST-elevation myocardial infarction: result of the double-blind, randomized, placebo-controlled stem cells in myocardial infarction (STEMMI) trial. Circulation 2006;113:1983–92.
- 73 Zohlnhöfer D, Ott I, Mehilli J, et al. Stem cell mobilization by granulocyte colony-stimulating factor in patients with acute myocardial infarction: a randomized controlled trial. JAMA 2006;295:1003–100.
Cord Blood Cells
- 74 Ma N, Stamm C, Kaminski A, et al. Human cord blood cells induce angiogenesis following myocardial infarction in NOD/scid-mice. Cardiovasc Res 2005;66:45–54.
- 75 Kim BO, Tian H, Prasongsukarn K, et al. Cell transplantation improves ventricular function after a myocardial infarction: a preclinical study of human unrestricted somatic stem cells in a porcine model. Circulation 2005;112(Suppl I):I96–104.
- 76 Leor J, Guetta E, Feinberg MS, et al. Human umbilical cord blood-derived CD133+ cells enhance function and repair of the infarcted myocardium. Stem Cells 2006;24:772–80.
Adipose Cells
- 77 Planat-Benard V, Silvestre JS, Cousin B, et al. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 2004;109:656–63.
Cardiomyocytes
- 78 Leor J, Patterson M, Quinones MJ, et al. Transplantation of fetal myocardial tissue into the infarcted myocardium of rat. A potential method for repair of infarcted myocardium? Circulation 1996;94(Suppl II):II332–6.
- 79 Scorsin M, Hagege AA, Marotte F, et al. Does transplantation of cardiomyocytes improve function of infracted myocardium? Circulation 1997;96(Suppl II):II188–93.
- 80 Zhang M, Methot D, Poppa V, et al. Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J Mol Cell Cardiol 2001;33:907–21.
- 81 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.
- 82 Rubart M, Pasumarthi KB, Nakajima H, et al. Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ Res 2003;92:1217–24.
- 83 Retuerto MA, Schalch P, Patejunas G, et al. Angiogenic pretreatment improves the efficacy of cellular cardiomyoplasty performed with fetal cardiomyocyte implantation. J Thorac Cardiovasc Surg. 2004;127:1041–9; discussion 1049–51.
- 84 Dow J, Simkhovich BZ, Kedes L, et al. Washout of transplanted cells from the heart: a potential new hurdle for cell transplantation therapy. Cardiovasc Res 2005;67:301–7.
Paracrine Effects
- 85 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;94:678–85. Erratum in: Circ Res 2005;97:e51.
- 86 Rehman J, Traktuev D, Li J, et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 2004;109:1292–8.
- 87 Agbulut O, Vandervelde S, Al Attar N, et al. Comparison of human skeletal myoblasts and bone marrow-derived CD133+ progenitors for the repair of infarcted myocardium. J Am Coll Cardiol 2004;44:458–63.
- 88 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;11:367–8.
- 89 Tang YL, Zhao Q, Qin X, et al. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg 2005;80:229–36; discussion 236–7.
- 90 Misao Y, Takemura G, Arai M, et al. Bone marrow-derived myocyte-like cells and regulation of repair-related cytokines after bone marrow cell transplantation. Cardiovasc Res 2006;69:476–90.
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Cardiac Stem Cells
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- 91 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.
- 92 Hocht-Zeisberg E, Kahnert H, Guan K, et al. Cellular repopulation of myocardial infarction in patients with sex-mismatched heart transplantation. Eur Heart J 2004;25:749–58.
- 93 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;102:8966–71.
- 94 Laugwitz KL, Moretti A, Lam J, et al. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005;433:647–53.
- 95 Minami E, Laflamme MA, Saffitz JE, et al. Extracardiac progenitor cells repopulate most major cell types in the transplanted human heart. Circulation 2005;112:2951–8.
- 96 Parmacek MS, Epstein JA. Pursuing cardiac progenitors: regeneration redux. Cell 2005;120:295–8 (review).
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Embryonic Stem Cells
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Reviews
- 97 Nir SG, David R, Zaruba M, et al. Human embryonic stem cells for cardiovascular repair. Cardiovasc Res 2003;58:313–23.
- 98 Lerou PH, Daley GQ. Therapeutic potential of embryonic stem cells. Blood Rev 2005;19:321–31.
Transplantation
- 99 Min JY, Yang Y, Sullivan MF, et al. Long-term improvement of cardiac function in rats after infarction by transplantation of embryonic stem cells. J Thorac Cardiovasc Surg 2003;125:361–9.
- 100 Kehat I, Khimovich L, Caspi O, et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 2004;22:1282–9.
- 101 Hodgson DM, Behfar A, Zingman LV, et al. Stable benefit of embryonic stem cell therapy in myocardial infarction. Am J Physiol Heart Circ Physiol 2004;287:H471–9.
- 102 Laflamme MA, Gold J, Xu C, et al. Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol 2005;167:663–71.
- 103 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.
- 104 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;366:1005–12.
- 105 Kofidis T, Lebl DR, Swijnenburg RJ, et al. Allopurinol/uricase and ibuprofen enhance engraftment of cardiomyocyte-enriched human embryonic stem cells and improve cardiac function following myocardial injury. Eur J Cardio-thorac Surg 2006;29:50–5.
- 106 Cao F, Lin S, Xie X, Ray P, et al. In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation 2006;113:1005–14.
Immunology
- 107 Taylor CJ, Bolton EM, Pocock S, et al. Banking on human embryonic stem cells: estimating the number of donor cell lines needed for HLA matching. Lancet 2005;366:2019–25.
- 108 Swijnenburg RJ, Tanaka M, Vogel H, et al. Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation 2005;112(Suppl I):I166–72.
- 109 Drukker M, Katchman H, Katz G, et al. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells 2006;24:221–9.
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Cell Tracking
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- 110 Frangioni JV, Hajjar RJ. In vivo tracking of stem cells for clinical trials in cardiovascular disease. Circulation 2004;110:3378–83.
- 111 Kraitchman DL, Tatsumi M, Gilson WD, et al. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation 2005;112:1451–61.
- 112 Cao F, Lin S, Xie X, et al. In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation 2006;113:1005–14.
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Reviews
Adult Somatic Cells