Choice of cell-delivery route for successful cell transplantation therapy for the heart

Future Cardiology

Volumn 9, Issue 2, 2013, Pages 215-227

  Fukushima, Satsuki ^a   Sawa, Yoshiki ^a   Suzuki, Ken ^b  

^a OSAKA UNIVERSITY   (Japan)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

cell transplantation; cell delivery route; heart failure; intracoronary injection; intramyocardial injection; regenerative medicine; stem cells; tissue engineering

Indexed keywords

BIOMATERIAL; CASPASE INHIBITOR; CELL ADHESION MOLECULE; CHEMOKINE RECEPTOR CXCR4; CYCLOSPORIN A; INTERLEUKIN 1BETA; PINACIDIL; STROMAL CELL DERIVED FACTOR 1; SUPEROXIDE DISMUTASE;

AUTOLOGOUS STEM CELL TRANSPLANTATION; CARDIOVASCULAR CATHETER; CARDITIS; CELL ADHESION; CELL JUNCTION; CELL SURVIVAL; CELL TRANSPLANTATION; CELL TYPE; CORONARY ARTERY INJECTION; ENDOTHELIAL PROGENITOR CELL; EPICARDIAL CELL SHEET PLACEMENT; GENETIC MANIPULATION; GRAFT SURVIVAL; HEART DISEASE; HEART FAILURE; HEART MUSCLE; HEART VENTRICLE ARRHYTHMIA; HEAT SHOCK; HUMAN; HYDROGEL; INJECTION; INTERSTITIUM; INTRAMYOCARDIAL INJECTION; MESENCHYMAL STEM CELL; MYOBLAST; NONHUMAN; PERCUTANEOUS CORONARY INTERVENTION; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; REVIEW; STERNOTOMY; THORACOSCOPY; THORACOTOMY; TRANSESOPHAGEAL ECHOCARDIOGRAPHY;

ANIMALS; BALLOON OCCLUSION; CELL SURVIVAL; HEART DISEASES; HUMANS; INJECTIONS, INTRA-ARTERIAL; INJECTIONS, INTRAMUSCULAR; ISCHEMIC PRECONDITIONING, MYOCARDIAL; PERICARDIUM; RECOVERY OF FUNCTION; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TREATMENT OUTCOME;

EID: 84874691322     PISSN: 14796678     EISSN: 17448298     Source Type: Journal    
DOI: 10.2217/fca.12.85     Document Type: Review

References (104)

1. Orlic D, Kajstura J, Chimenti S et al. Bone marrow cells regenerate infarcted myocardium. Nature 410(6829), 701-705 (2001).
2. Assmus B, Schachinger V, Teupe C et al. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation 106(24), 3009-3017 (2002).
3. Lunde K, Solheim S, Aakhus S et al. Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N. Engl. J. Med. 355(12), 1199-1209 (2006).
4. Schachinger V, Erbs S, Elsasser A et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N. Engl. J. Med. 355(12), 1210-1221 (2006).
5. 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 113(10), 1287-1294 (2006).
6. 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. 5(10), 663-670 (2008).
7. Beitnes JO, Hopp E, Lunde K et al. Long-term results after intracoronary injection of autologous mononuclear bone marrow cells in acute myocardial infarction: the ASTAMI randomised, controlled study. Heart 95(24), 1983-1989 (2009).
8. Grajek S, Popiel Mg, Gil L et al. Influence of bone marrow stem cells on left ventricle perfusion and ejection fraction in patients with acute myocardial infarction of anterior wall: randomized clinical trial. Eur. Heart. J. 31(6), 691-702 (2010).
9. Traverse JH, Henry TD, Ellis SG et al. Effect of intracoronary delivery of autologous bone marrow mononuclear cells 2 to 3 weeks following acute myocardial infarction on left ventricular function: the latetime randomized trial. JAMA 306(19), 2110-2119 (2011).
10. van Ramshorst J, Bax JJ, Beeres SL et al. Intramyocardial bone marrow cell injection for chronic myocardial ischemia: a randomized controlled trial. JAMA 301(19), 1997-2004 (2009).
11. 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 367(9505), 113-121 (2006).
12. 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 117(9), 1189-1200 (2008).
13. Yacoub M, Suzuki K, Rosenthal N. The future of regenerative therapy in patients with chronic heart failure. Nat. Clin. Pract. Cardiovasc. Med. 39(Suppl. 1), S133-S135 (2006).
14. Nadal-Ginard B, Fuster V. Myocardial cell therapy at the crossroads. Nat. Clin. Pract. Cardiovasc. Med. 4(1), 1 (2007).
15. Steering Committee of the National Heart, Lung, and Blood Institute Cardiovascular Cell Therapy Research Network. Cardiac cell therapy: bench or bedside? Nat. Clin. Pract. Cardiovasc. Med. 4(8), 403 (2007).
16. Campbell N, Suzuki K. Cell delivery routes for stem cell therapy to the heart: current and future approaches. J. Cardiovasc. Transl Res. 5(5), 713-726 (2012).
17. Dib N, McCarthy P, Campbell A et al. Feasibility and safety of autologous myoblast transplantation in patients with ischemic cardiomyopathy. Cell Transplant. 14(1), 11-19 (2005).
18. Menasche P. Myoblast-based cell transplantation. Heart Fail. Rev. 8(3), 221-227 (2003).
19. Ott HC, Kroess R, Bonaros N et al. Intramyocardial microdepot injection increases the efficacy of skeletal myoblast transplantation. Eur. J. Cardiothorac Surg. 27(6), 1017-1021 (2005).
20. Hattori F, Chen H, Yamashita H et al. Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat. Methods 7(1), 61-66 (2010).
21. 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 112(Suppl. 9), I150-I156 (2005).
22. Suzuki K, Murtuza B, Beauchamp JR et al. Dynamics and mediators of acute graft attrition after myoblast transplantation to the heart. FASEB J. 18(10), 1153-1155 (2004).
23. Suzuki K, Murtuza B, Beauchamp JR et al. Role of interleukin-1beta in acute inflammation and graft death after cell transplantation to the heart. Circulation 110(11 Suppl. 1), II219-II224 (2004).
24. Murtuza B, Suzuki K, Bou-Gharios G et al. Transplantation of skeletal myoblasts secreting an IL-1 inhibitor modulates adverse remodeling in infarcted murine myocardium. Proc. Natl Acad. Sci. USA 101(12), 4216-4221 (2004).
25. Reinecke H, Poppa V, Murry CE. Skeletal muscle stem cells do not transdifferentiate into cardiomyocytes after cardiac grafting. J. Mol. Cell. Cardiol. 34(2), 241-249 (2002).
26. Leobon B, Garcin I, Menasche P, Vilquin JT, Audinat E, Charpak S. Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc. Natl Acad. Sci. USA 100(13), 7808-7811 (2003).
27. Fukushima S, Varela-Carver A, Coppen SR et al. Direct intramyocardial but not intracoronary injection of bone marrow cells induces ventricular arrhythmias in a rat chronic ischemic heart failure model. Circulation 115(17), 2254-2261 (2007).
28. Fukushima S, Coppen SR, Lee J et al. Choice of cell-delivery route for skeletal myoblast transplantation for treating post-infarction chronic heart failure in rat. PLoS ONE 3(8), e3071 (2008).
29. Menasche P, Hagege AA, Vilquin JT et al. Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J. Am. Coll. Cardiol. 41(7), 1078-1083 (2003).
30. Murry CE, Wiseman RW, Schwartz SM, Hauschka SD. Skeletal myoblast transplantation for repair of myocardial necrosis. J. Clin. Invest. 98(11), 2512-2523 (1996).
31. Taylor DA, Atkins BZ, Hungspreugs P et al. Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat. Med. 4(8), 929-933 (1998).
32. 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. 115(2), 326-338 (2005).
33. Kimura T, Miyoshi S, Takatsuki S et al. Safety and efficacy of pericardial endoscopy by percutaneous subxyphoid approach in swine heart in vivo. J. Thorac Cardiovasc. Surg. 142(1), 181-190 (2011).
34. Losordo DW, Schatz RA, White CJ et al. Intramyocardial transplantation of autologous CD34+ stem cells for intractable angina. Circulation 115(25), 3165-3172 (2007).
35. Kumar A, Haralampus CA, Hughes M et al. Assessment of safety, accuracy, and human CD34+ cell retention after intramyocardial injections with a helical needle catheter in a porcine model. Cathet. Cardiovasc. Intervent. doi:10.1002/ccd.24476 (2012) (Epub ahead of print).
36. Trachtenberg B, Velazquez DL, Williams AR et al. Rationale and design of the Transendocardial Injection of Autologous Human Cells (bone marrow or mesenchymal) in Chronic Ischemic Left Ventricular Dysfunction and Heart Failure Secondary to Myocardial Infarction (TACHFT) trial: a randomized, double-blind, placebo-controlled study of safety and efficacy. Am. Heart J. 161(3), 487-493 (2011).
37. Siminiak T, Fiszer D, Jerzykowska O et al. Percutaneous trans-coronary-venous transplantation of autologous skeletal myoblasts in the treatment of postinfarction myocardial contractility impairment: the POZNAN trial. Eur. Heart. J. 26(12), 1188-1195 (2005).
38. Brasselet C, Morichetti MC, Messas E et al. Skeletal myoblast transplantation through a catheter-based coronary sinus approach: an effective means of improving function of infarcted myocardium. Eur. Heart J. 26(15), 1551-1556 (2005).
39. Penn MS, Ellis S, Gandhi S et al. Adventitial delivery of an allogeneic bone marrow derived adherent stem cell in acute myocardial infarction/novelty and significance. Circ. Res. 110(2), 304-311 (2012).
40. 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. 148(3), 531-537 (2004).
41. 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. 133(3), 717-725 (2007).
42. Patel AN, Geffner L, Vina RF et al. Surgical treatment for congestive heart failure with autologous adult stem cell transplantation: a prospective randomized study. J. Thorac Cardiovasc. Surg. 130(6), 1631-1638 (2005).
43. 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. 86(6), 1833-1840 (2008).
44. Agbulut O, Mazo M, Bressolle C et al. Can bone marrow-derived multipotent adult progenitor cells regenerate infarcted myocardium? Cardiovasc. Res. 72(1), 175-183 (2006).
45. Menasche P, Hagege AA, Scorsin M et al. Myoblast transplantation for heart failure. Lancet 357(9252), 279-280 (2001).
46. 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 115(25), 3165-3172 (2007).
47. 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 307(16), 1717-1726 (2012).
48. 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 (FOCUS-HF). Am. Heart J. 161(6), 1078-1087 (2011).
49. Arom KV, Ruengsakulrach P, Jotisakulratana V. Intramyocardial angiogenic cell precursor injection for cardiomyopathy. Asian Cardiovasc. Thorac Ann. 16(2), 143-148 (2008).
50. 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. 25(9), 1015-1024 (2007).
51. Suzuki K, Smolenski RT, Jayakumar J, Murtuza B, Brand NJ, Yacoub MH. Heat shock treatment enhances graft cell survival in skeletal myoblast transplantation to the heart. Circulation 102(19 Suppl. 3), III216-III221 (2000).
52. Lee WY, Wei HJ, Lin WW et al. Enhancement of cell retention and functional benefits in myocardial infarction using human amniotic-fluid stem-cell bodies enriched with endogenous ECM. Biomaterials 32(24), 5558-5567 (2011).
53. Huang NF, Yu J, Sievers R, Li S, Lee RJ. Injectable biopolymers enhance angiogenesis after myocardial infarction. Tissue Eng. 11(11-12), 1860-1866 (2005).
54. Christman KL, Vardanian AJ, Fang Q, Sievers RE, Fok HH, Lee RJ. Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J. Am. Coll. Cardiol. 44(3), 654-660 (2004).
55. Nakamuta JS, Danoviz ME, Marques FLN et al. Cell therapy attenuates cardiac dysfunction post myocardial infarction: effect of timing, routes of injection and a fibrin scaffold. PLoS ONE 4(6), e6005 (2009).
56. Ren J, Samson WK, Sowers Jr. Insulin-like growth factor I as a cardiac hormone: physiological and pathophysiological implications in heart disease. J. Mol. Cell. Cardiol. 31(11), 2049-2061 (1999).
57. Davis ME, Hsieh PC, Takahashi T et al. Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc. Natl Acad. Sci. USA 103(21), 8155-8160 (2006).
58. Yau TM, Kim C, Li G, Zhang Y, Weisel RD, Li RK. Maximizing ventricular function with multimodal cell-based gene therapy. Circulation 112(Suppl. 9), I123-I128 (2005).
59. Yau TM, Kim C, Ng D et al. Increasing transplanted cell survival with cell-based angiogenic gene therapy. Ann. Thorac Surg. 80(5), 1779-1786 (2005).
60. Mangi AA, Noiseux N, Kong D et al. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat. Med. 9(9), 1195-1201 (2003).
61. 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 114(Suppl. 1), I108-I113 (2006).
62. Strauer BE, Brehm M, Zeus T et al. [Intracoronary, human autologous stem cell transplantation for myocardial regeneration following myocardial infarction]. Dtsch Med. Wochenschr. 126(34-35), 932-938 (2001).
63. Fukushima S, Campbell NG, Coppen SR et al. Quantitative assessment of initial retention of bone marrow mononuclear cells injected into the coronary arteries. J. Heart Lung Transplant. 30(2), 227-233 (2011).
64. 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. 44(8), 1690-1699 (2004).
65. Hirsch A, Nijveldt R, van der Vleuten PA et al. Intracoronary infusion of autologous mononuclear bone marrow cells or peripheral mononuclear blood cells after primary percutaneous coronary intervention: rationale and design of the HEBE trial -a prospective, multicenter, randomized trial. Am. Heart J. 152(3), 434-441 (2006).
66. Suzuki K, Brand NJ, Smolenski RT, Jayakumar J, Murtuza B, Yacoub MH. Development of a novel method for cell transplantation through the coronary artery. Circulation 102(19), 359-364 (2000).
67. Vulliet PR, Greeley M, Halloran SM, MacDonald KA, Kittleson MD. Intracoronary arterial injection of mesenchymal stromal cells and microinfarction in dogs. Lancet 363(9411), 783-784 (2004).
68. Suzuki K, Murtuza B, Smolenski RT, Yacoub MH. Selective cell dissemination into the heart by retrograde intracoronary infusion in the rat. Transplantation 77(5), 757-759 (2004).
69. Suzuki K, Murtuza B, Fukushima S et al. Targeted cell delivery into infarcted rat hearts by retrograde intracoronary infusion: distribution, dynamics, and influence on cardiac function. Circulation 110(11 Suppl. 1), II225-II230 (2004).
70. Clifford DM, Fisher SA, Brunskill SJ et al. Stem cell treatment for acute myocardial infarction. Cochrane. Database. Syst. Rev. 2, CD006536 (2012).
71. Jeevanantham V, Butler M, Saad A, Bdel-Latif A, Zuba-Surma EK, Dawn B. Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters/clinical perspective. Circulation 126(5), 551-568 (2012).
72. 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 378(9806), 1847-1857 (2011).
73. Makkar RR, Smith RR, Cheng K et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised Phase 1 trial. Lancet 379(9819), 895-904 (2010).
74. Segers VF, Van R, I, Andries LJ et al. Mesenchymal stem cell adhesion to cardiac microvascular endothelium: activators and mechanisms. Am. J. Physiol. Heart Circ. Physiol. 290(4), H1370-H1377 (2006).
75. Wu Y, Ip JE, Huang J et al. Essential role of ICAM-1/CD18 in mediating EPC recruitment, angiogenesis, and repair to the infarcted myocardium. Circ. Res. 99(3), 315-322 (2006).
76. Tossios P, Krausgrill B, Schmidt M et al. Role of balloon occlusion for mononuclear bone marrow cell deposition after intracoronary injection in pigs with reperfused myocardial infarction. Eur. Heart. J. 29, 1911-1921 (2008).
77. Zhao ZQ, Corvera JS, Halkos ME et al. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am. J. Physiol. Heart Circ. Physiol. 285(2), H579-H588 (2003).
78. Assmus B, Honold J, Schachinger V et al. Transcoronary transplantation of progenitor cells after myocardial infarction. N. Engl. J. Med. 355(12), 1222-1232 (2006).
79. Doyle B, Kemp BJ, Chareonthaitawee P et al. Dynamic tracking during intracoronary injection of 18F-FDG-labeled progenitor cell therapy for acute myocardial infarction. J. Nucl. Med. 48(10), 1708-1714 (2007).
80. 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/novelty and significance. Circ. Res. 111(7), 854-862 (2012).
81. Kloner RA. No-reflow phenomenon: maintaining vascular integrity. J. Cardiovasc. Pharmacol. Ther. 16(3-4), 244-250 (2011).
82. Robinson SW, Cho PW, Levitsky HI et al. Arterial delivery of genetically labelled skeletal myoblasts to the murine heart: long-term survival and phenotypic modification of implanted myoblasts. Cell Transplant. 5(1), 77-91 (1996).
83. Hayashi M, Li TS, Ito H, Mikamo A, Hamano K. Comparison of intramyocardial and intravenous routes of delivering bone marrow cells for the treatment of ischemic heart disease: an experimental study. Cell Transplant. 13(6), 639-647 (2004).
84. Aicher A, Brenner W, Zuhayra M et al. Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling. Circulation 107(16), 2134-2139 (2003).
85. Forest V, Tirouvanziam A, Perigaud C et al. Cell distribution after intracoronary bone marrow stem cell delivery in damaged and undamaged myocardium: implications for clinical trials. Stem Cell Res. Ther. 1(1), 4 (2010).
86. Brenner W, Aicher A, Eckey T et al. 111In-labeled CD34+ hematopoietic progenitor cells in a rat myocardial infarction model. J. Nucl. Med. 45(3), 512-518 (2004).
87. Kraitchman DL, Tatsumi M, Gilson WD et al. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation 112(10), 1451-1461 (2005).
88. Schots R, De Keulenaer G, Schoors D et al. Evidence that intracoronary-injected CD133+ peripheral blood progenitor cells home to the myocardium in chronic postinfarction heart failure. Exp. Hematol. 35, 1884-1890 (2007).
89. Hare JM, Traverse JH, Henry TD et al. A randomized, double-blind, placebocontrolled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J. Am. Coll. Cardiol. 54(24), 2277-2286 (2009).
90. Okano T, Yamada N, Sakai H, Sakurai Y. A novel recovery system for cultured cells using plasma-treated polystyrene dishes grafted with poly (N-isopropylacrylamide). J. Biomed. Mater. Res. 27(10), 1243-1251 (1993).
91. Sawa Y, Miyagawa S, Sakaguchi T et al. Tissue engineered myoblast sheets improved cardiac function sufficiently to discontinue LVAS in a patient with DCM: report of a case. Surg. Today 42(2), 181-184 (2012).
92. Yang J, Yamato M, Kohno C et al. Cell sheet engineering: recreating tissues without biodegradable scaffolds. Biomaterials 26(33), 6415-6422 (2005).
93. Elloumi-Hannachi I, Yamato M, Okano T. Cell sheet engineering: a unique nanotechnology for scaffold-free tissue reconstruction with clinical applications in regenerative medicine. J. Int. Med. 267(1), 54-70 (2010).
94. Shimizu T, Yamato M, Isoi Y et al. Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperatureresponsive cell culture surfaces. Circ. Res. 90(3), e40-e48 (2002).
95. Miyagawa S, Saito A, Sakaguchi T et al. Impaired myocardium regeneration with skeletal cell sheets -a preclinical trial for tissue-engineered regeneration therapy. Transplantation 90(4), 364-372 (2010).
96. Imanishi Y, Miyagawa S, Maeda N et al. Induced adipocyte cell-sheet ameliorates cardiac dysfunction in a mouse myocardial infarction model. Circulation 124(11 Suppl. 1), S10-S17 (2011).
97. Kondoh H, Sawa Y, Miyagawa S et al. Longer preservation of cardiac performance by sheetshaped myoblast implantation in dilated cardiomyopathic hamsters. Cardiovasc. Res. 69(2), 466-475 (2006).
98. 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. 130(5), 1333-1341 (2005).
99. Sekine H, Shimizu T, Dobashi I et al. Cardiac cell sheet transplantation improves damaged heart function via superior cell survival in comparison with dissociated cell injection. Tissue Eng. Part A 17(23-24), 2973-2980 (2011).
100. Shudo Y, Miyagawa S, Fukushima S et al. Novel regenerative therapy using cell-sheet covered with omentum flap delivers a huge number of cells in a porcine myocardial infarction model. J. Thorac Cardiovasc. Surg. 142(5), 1188-1196 (2011).
101. Ptaszek LM, Mansour M, Ruskin JN, Chien KR. Towards regenerative therapy for cardiac disease. Lancet 379(9819), 933-942 (2012).
102. Dai W, Kloner RA. Bone marrow-derived cell transplantation therapy for myocardial infarction: lessons learned and future questions. Am. J. Transplant. 11(11), 2297-2301 (2011).
103. Sekiya N, Matsumiya G, Miyagawa S et al. Layered implantation of myoblast sheets attenuates adverse cardiac remodeling of the infarcted heart. J. Thorac Cardiovasc. Surg. 138(4), 985-993 (2009).
104. Zhou R, Acton PD, Ferrari VA. Imaging stem cells implanted in infarcted myocardium. J. Am. Coll. Cardiol. 48(10), 2094-2106 (2006).