Myocardial infarction: Stem cell transplantation for cardiac regeneration

Regenerative Medicine

Volumn 10, Issue 8, 2015, Pages 1025-1043

  Carvalho, Edmund ^a   Verma, Paul ^b,c   Hourigan, Kerry ^c   Banerjee, Rinti ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

^b SOUTH AUSTRALIAN RESEARCH AND DEVELOPMENT INSTITUTE   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

bench to clinic; cardiac regeneration; myocardial infarction

Indexed keywords

ALPHA ACTININ; ATAXIN 1; BONE MORPHOGENETIC PROTEIN 2; CD11B ANTIGEN; CD133 ANTIGEN; CD15 ANTIGEN; CD19 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; ENDOGLIN; FIBROBLAST GROWTH FACTOR 2; HLA DR1 ANTIGEN; HYALURONIC ACID; KRUPPEL LIKE FACTOR 4; MACROGOL; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; POLITEF; POLY(N ISOPROPYLACRYLAMIDE); POLYETHERURETHAN; POLYURETHAN; STEM CELL FACTOR; THY 1 ANTIGEN; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR PAX7; TRANSCRIPTION FACTOR SOX2; TRANSFORMING GROWTH FACTOR BETA; UNINDEXED DRUG; VASCULOTROPIN;

CARDIAC IMPLANT; CARDIOVASCULAR PARAMETERS; CARDIOVASCULAR STENT; CELL DIFFERENTIATION; CELL ENCAPSULATION; CELL EXPANSION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CELL SELECTION; CELL TRANSFER; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; HEART INFARCTION; HEART MUSCLE CELL; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HUMAN; LEFT VENTRICULAR ASSIST DEVICE; MESENCHYMAL STEM CELL; MUSCLE CELL; MYOBLAST; NONHUMAN; PACEMAKER; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SKELETAL MUSCLE; STEM CELL TRANSPLANTATION; TISSUE REGENERATION; TISSUE SCAFFOLD; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; METABOLISM; MYOCARDIAL INFARCTION; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; REGENERATION; STEM CELL;

ANIMALS; HUMANS; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; REGENERATION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84951279971     PISSN: 17460751     EISSN: 1746076X     Source Type: Journal    
DOI: 10.2217/rme.15.63     Document Type: Review

References (208)

1. World Health Organization. The top 10 causes of death. www.who.int/mediacentre
2. Gepstein L. Derivation and potential applications of human embryonic stem cells. Circ. Res. 91(10), 866-876 (2002).
3. Beltrami CA, Finato N, Rocco M et al. Structural basis of end-stage failure in ischemic cardiomyopathy in humans. Circulation 89(1), 151-163 (1994).
4. Pfeffer MA, Braunwald E. Ventricular remodeling after myocardial infarction. Experimental observations and clinical implications. Circulation 81(2138525), 1161-1172 (1990).
5. Silverman KJ, Bulkley BH, Hutchins GM. Anomalous left circumflex coronary artery: "normal" variant of uncertain clinical and pathologic significance. Am. J. Cardiol. 41(7), 1311-1314 (1978).
6. Von Harsdorf R. "Fas-ten" your seat belt: anti-apoptotic treatment in heart failure takes off. Circ. Res. 95(6), 554-556 (2004).
7. Seale P, Rudnicki MA. A new look at the origin, function, and "stem-cell" status of muscle satellite cells. Dev. Biol. 218(2), 115-124 (2000).
8. Winitsky SO, Gopal TV, Hassanzadeh S et al. Adult murine skeletal muscle contains cells that can differentiate into beating cardiomyocytes in vitro. PLoS Biol. 3(4), e87 (2005).
9. Wang QD, Sjoquist PO. Myocardial regeneration with stem cells: pharmacological possibilities for efficacy enhancement. Pharmacol. Res. 53(4), 331-340 (2006).
10. 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. Col. Cardiol. 41(5), 879-888 (2003).
11. Smits PC, Van Geuns R-JM, Poldermans D et al. Catheterbased intramyocardial injection of autologous skeletal myoblasts as a primary treatment of ischemic heart failure: clinical experience with six-month follow-up. J. Am. Col. Cardiol. 42(12), 2063-2069 (2003).
12. 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).
13. 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. 26(12), 1188-1195 (2005).
14. Bioheart I, NCT00054678. Myoheart™ (myogenesis heart efficiency and regeneration trial). http://clinicaltrials.gov/ct2/show/NCT00054678
15. Tedesco FS, Dellavalle A, Diaz-Manera J, Messina G, Cossu G. Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J. Clin. Invest. 120(1), 11-19 (2010).
16. Menasché P, Alfieri O, Janssens S et al. The myoblast autologous grafting in ischemic cardiomyopathy (MAGIC) trial. Circulation 117(9), 1189-1200 (2008).
17. Manginas A, Goussetis E, Koutelou M et al. Pilot study to evaluate the safety and feasibility of intracoronary CD133+ and CD133-CD34+ cell therapy in patients with nonviable anterior myocardial infarction. Catheter. Cardiovasc. Interv. 69(6), 773-781 (2007).
18. Orlic D, Kajstura J, Chimenti S et al. Bone marrow cells regenerate infarcted myocardium. Nature 410(6829), 701-705 (2001).
19. Valarmathi MT, Goodwin RL, Fuseler JW, Davis JM, Yost MJ, Potts JD. A 3D cardiac muscle construct for exploring adult marrow stem cell based myocardial regeneration. Biomaterials 31(12), 3185-3200 (2010).
20. Duran JM, Makarewich CA, Sharp TE et al. Bone-derived stem cells repair the heart after myocardial infarction through transdifferentiation and paracrine signaling mechanisms. Circ. Res. 113(5), 539-552 (2013).
21. Kajstura J, Rota M, Whang B et al. Bone marrow cells differentiate in cardiac cell lineages after infarction independently of cell fusion. Circ. Res. 96(1), 127-137 (2005).
22. 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. 51(3), 413-417 (2010).
23. Silva GV, Litovsky S, Assad JaR et al. Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 111(2), 150-156 (2005).
24. Chekanov V, Akhtar M, Tchekanov G et al. Transplantation of autologous endothelial cells induces angiogenesis. Pacing Clin. Electrophysiol. 26(1 Pt 2), 496-499 (2003).
25. Ménard C, Hagège AA, Agbulut O et al. Transplantation of cardiac-committed mouse embryonic stem cells to infarcted sheep myocardium: A preclinical study. Lancet 366(9490), 1005-1012 (2005).
26. 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. 87(3), 794-801 (2009).
27. Houtgraaf JH, De Jong R, Kazemi K et al. Intracoronary infusion of allogeneic mesenchymal precursor cells directly after experimental acute myocardial infarction reduces infarct size, abrogates adverse remodeling, and improves cardiac function. Circ. Res. 113(2), 153-166 (2013).
28. Zeng L, Hu Q, Wang X et al. Bioenergetic and functional consequences of bone marrow-derived multipotent progenitor cell transplantation in hearts with postinfarction left ventricular remodeling. Circulation 115(14), 1866-1875 (2007).
29. Zhang H, Song P, Tang Y et al. Injection of bone marrow mesenchymal stem cells in the borderline area of infarcted myocardium: heart status and cell distribution. J. Thorac. Cardiovasc. Surg. 134(5), 1234-1240 (2007).
30. 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. USA 102(32), 11474-11479 (2005).
31. Valina C, Pinkernell K, Song YH et al. Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur. Heart J. 28(21), 2667-2677 (2007).
32. Makkar RR, Price MJ, Lill M et al. Intramyocardial injection of allogenic bone marrow-derived mesenchymal stem cells without immunosuppression preserves cardiac function in a porcine model of myocardial infarction. J. Cardiovasc. Pharmacol. Ther. 10(4), 225-233 (2005).
33. Hatzistergos KE, Quevedo H, Oskouei BN et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ. Res. 107(7), 913-922 (2010).
34. Price MJ, Chou CC, Frantzen M et al. Intravenous mesenchymal stem cell therapy early after reperfused acute myocardial infarction improves left ventricular function and alters electrophysiologic properties. Int. J. Cardiol. 111(2), 231-239 (2006).
35. Hashemi SM, Ghods S, Kolodgie FD et al. A placebo controlled, dose-ranging, safety study of allogenic mesenchymal stem cells injected by endomyocardial delivery after an acute myocardial infarction. Eur. Heart J. 29(2), 251-259 (2008).
36. Qi CM, Ma GS, Liu NF et al. Transplantation of magnetically labeled mesenchymal stem cells improves cardiac function in a swine myocardial infarction model. Chin. Med. J. (Engl.) 121(6), 544-550 (2008).
37. De Jong R, Van Hout GPJ, Houtgraaf JH et al. Intracoronary infusion of encapsulated glucagon-like peptide-1-eluting mesenchymal stem cells preserves left ventricular function in a porcine model of acute myocardial infarction. Circ. Cardiovasc. Interv. 7(5), 673-683 (2014).
38. Suzuki G, Iyer V, Lee TC, Canty JM Jr. Autologous mesenchymal stem cells mobilize cKit+ and CD133+ bone marrow progenitor cells and improve regional function in hibernating myocardium. Circ. Res. 109(9), 1044-1054 (2011).
39. Rigol M, Solanes N, Farré J et al. Effects of adipose tissuederived stem cell therapy after myocardial infarction: impact of the route of administration. J. Card. Fail. 16(4), 357-366 (2010).
40. Rigol M, Solanes N, Roura S et al. Allogeneic adipose stem cell therapy in acute myocardial infarction. Eur. J. Clin. Invest. 44(1), 83-92 (2014).
41. Kanazawa H, Malliaras K, Yee K et al. Cardioprotective effect of allogeneic cardiosphere-derived cells: reduction of infarct size and attenuation of no-reflow when administered in the infarct-related artery after reperfusion in pigs with acute myocardial infarction. J. Am. Col. Cardiol. 61(10), E1818 (2013).
42. Yee K, Malliaras K, Kanazawa H et al. Pivotal trial of transendocardially-injected allogeneic cardiospheres in porcine ischemic cardiomyopathy reveals therapeutic regeneration and blunted adverse ventricular remodeling. J. Am. Col. Cardiol. 61(10), E1169-E1169 (2013).
43. 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 127(2), 213-223 (2013).
44. Strauer BE, Brehm M, Zeus T et al. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 106(15), 1913-1918 (2002).
45. 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).
46. Uemura R, Xu M, Ahmad N, Ashraf M. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ. Res. 98(11), 1414-1421 (2006).
47. Traverse JH, Mckenna DH, Harvey K et al. Results of a Phase 1, randomized, double-blind, placebo-controlled trial of bone marrow mononuclear stem cell administration in patients following ST-elevation myocardial infarction. Am. Heart J. 160(3), 428-434 (2010).
48. Kearns-Jonker M, Dai W, Kloner RA. Stem cells for the treatment of heart failure. Curr. Opin. Mol. Ther. 12(4), 432-441 (2010).
49. Sun L, Zhang T, Lan X, Du G. Effects of stem cell therapy on left ventricular remodeling after acute myocardial infarction: A meta-analysis. Clin. Cardiol. 33(5), 296-302 (2010).
50. Rangappa S, Makkar R, Forrester J. Current status of myocardial regeneration: new cell sources and new strategies. J. Cardiovasc. Pharmacol. Ther. 15(4), 338-343 (2010).
51. 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).
52. Trounson A, Thakar R, Lomax G, Gibbons D. Clinical trials for stem cell therapies. BMC Med. 9(1), 52 (2011).
53. Hopp E, Lunde K, Solheim S et al. Regional myocardial function after intracoronary bone marrow cell injection in reperfused anterior wall infarction: A cardiovascular magnetic resonance tagging study. J. Cardiovasc. Magn. Reson. 13(1), 22-22 (2011).
54. 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).
55. Murry CE, Soonpaa MH, Reinecke H et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428(6983), 664-668 (2004).
56. Breitbach M, Bostani T, Roell W et al. Potential risks of bone marrow cell transplantation into infarcted hearts. Blood 110(4), 1362-1369 (2007).
57. Ott I, Keller U, Knoedler M et al. Endothelial-like cells expanded from CD34+ blood cells improve left ventricular function after experimental myocardial infarction. FASEB J. 19(8), 992-994 (2005).
58. Klein HM, Ghodsizad A, Marktanner R et al. Intramyocardial implantation of CD133+ stem cells improved cardiac function without bypass surgery. Heart Surg. Forum 10(1), E66-E69 (2007).
59. Group T, NCT00984178. Trial of hematopoietic stem cells in acute myocardial infarction (TECAM2). http://clinicaltrials.gov/ct2/show/NCT00984178
60. All India Institute of Medical Sciences ND, NCT01625949. Stem cell therapy in patients with myocardial infarction and persistent total occlusion of infarct related artery (coat). http://clinicaltrials.gov/ct2/show/NCT01625949
61. 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 8(4), 315-317 (2006).
62. Koninckx R, Daniels A, Windmolders S et al. Mesenchymal stem cells or cardiac progenitors for cardiac repair? A comparative study. Cell Mol. Life Sci. 68(12), 2141-2156 (2011).
63. Lien CL, Wu C, Mercer B, Webb R, Richardson JA, Olson EN. Control of early cardiac-specific transcription of Nkx2-5 by a GATA-dependent enhancer. Development 126(1), 75-84 (1999).
64. Koninckx R, Hensen K, Daniels A et al. Human bone marrow stem cells co-cultured with neonatal rat cardiomyocytes display limited cardiomyogenic plasticity. Cytotherapy 11(6), 778-792 (2009).
65. Makino S, Fukuda K, Miyoshi S et al. Cardiomyocytes can be generated from marrow stromal cells in vitro. J. Clin. Invest. 103(5), 697-705 (1999).
66. Yoon J, Min BG, Kim YH, Shim WJ, Ro YM, Lim DS. Differentiation, engraftment and functional effects of pretreated mesenchymal stem cells in a rat myocardial infarct model. Acta Cardiol. 60(3), 277-284 (2005).
67. Lei Y, Gojgini S, Lam J, Segura T. The spreading, migration and proliferation of mouse mesenchymal stem cells cultured inside hyaluronic acid hydrogels. Biomaterials 32(1), 39-47 (2011).
68. Ho W, Tawil B, Dunn JC, Wu BM. The behavior of human mesenchymal stem cells in 3D fibrin clots: dependence on fibrinogen concentration and clot structure. Tissue Eng. 12(6), 1587-1595 (2006).
69. Zhou Y, Wang S, Yu Z et al. Direct injection of autologous mesenchymal stromal cells improves myocardial function. Biochem. Biophys. Res. Commun. 390(3), 902-907 (2009).
70. Nascimento DS, Mosqueira D, Sousa LM et al. Human umbilical cord tissue-derived mesenchymal stromal cells attenuate remodeling after myocardial infarction by proangiogenic, antiapoptotic, and endogenous cell-activation mechanisms. Stem Cell Res. Ther. 5(1), 5 (2014).
71. Hattan N, Kawaguchi H, Ando K et al. Purified cardiomyocytes from bone marrow mesenchymal stem cells produce stable intracardiac grafts in mice. Cardiovasc. Res. 65(2), 334-344 (2005).
72. Wang JS, Shum-Tim D, Chedrawy E, Chiu RC. The coronary delivery of marrow stromal cells for myocardial regeneration: pathophysiologic and therapeutic implications. J. Thorac. Cardiovasc. Surg. 122(4), 699-705 (2001).
73. Miyahara Y, Nagaya N, Kataoka M et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat. Med. 12(4), 459-465 (2006).
74. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105(1), 93-98 (2002).
75. Tan J, Weil BR, Abarbanell AM et al. Ablation of TNF-alpha receptors influences mesenchymal stem cell-mediated cardiac protection against ischemia. Shock 34(3), 236-242 (2010).
76. Heldman AW, Difede DL, Fishman JE et al. Transendocardial mesenchymal stem cells and mononuclear bone marrow cells for ischemic cardiomyopathy: The TACHFT randomized trial. JAMA 311(1), 62-73 (2014).
77. 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. Col. Cardiol. 54(24), 2277-2286 (2009).
78. Miami UO, NCT00768066. The transendocardial autologous cells (hMSC or hBMC) in ischemic heart failure trial (TAC-HFT). https://clinicaltrials.gov/ct2/show/NCT00768066
79. Hare JM, NCT01392625. Percutaneous stem cell injection delivery effects on neomyogenesis in dilated cardiomyopathy (the POSEIDON-DCM study) (PoseidonDCM). https://clinicaltrials.gov/ct2/show/NCT01392625
80. 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. USA 102(25), 8966-8971 (2005).
81. 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 100(21), 12313-12318 (2003).
82. Bergmann O, Bhardwaj RD, Bernard S et al. Evidence for cardiomyocyte renewal in humans. Science 324(5923), 98-102 (2009).
83. Bearzi C, Rota M, Hosoda T et al. Human cardiac stem cells. Proc. Natl Acad. Sci. USA 104(35), 14068-14073 (2007).
84. Wu SM, Chien KR, Mummery C. Origins and fates of cardiovascular progenitor cells. Cell 132(4), 537-543 (2008).
85. Messina E, De Angelis L, Frati G et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ. Res. 95(9), 911-921 (2004).
86. Barile L, Messina E, Giacomello A, Marban E. Endogenous cardiac stem cells. Prog. Cardiovasc. Dis. 50(1), 31-48 (2007).
87. Matsuura K, Nagai T, Nishigaki N et al. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J. Biol. Chem. 279(12), 11384-11391 (2004).
88. Li Z, Guo X, Matsushita S, Guan J. Differentiation of cardiosphere-derived cells into a mature cardiac lineage using biodegradable poly(N-isopropylacrylamide) hydrogels. Biomaterials 32(12), 3220-3232 (2011).
89. Rosenblatt-Velin N, Lepore MG, Cartoni C, Beermann F, Pedrazzini T. FGF-2 controls the differentiation of resident cardiac precursors into functional cardiomyocytes. J. Clin. Invest. 115(7), 1724-1733 (2005).
90. Ellison GM, Vicinanza C, Smith AJ et al. Adult c-kit(POS) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell 154(4), 827-842 (2013).
91. Tateishi K, Ashihara E, Takehara N et al. Clonally amplified cardiac stem cells are regulated by Sca-1 signaling for efficient cardiovascular regeneration. J. Cell Sci. 120(Pt 10), 1791-1800 (2007).
92. Liang SX, Tan TYL, Gaudry L, Chong B. Differentiation and migration of Sca1+/CD31-cardiac side population cells in a murine myocardial ischemic model. Int. J. Cardiol. 138(1), 40-49 (2010).
93. Tillmanns J, Rota M, Hosoda T et al. Formation of large coronary arteries by cardiac progenitor cells. Proc. Natl Acad. Sci. USA 105(5), 1668-1673 (2008).
94. 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. Col. Cardiol. 52(23), 1858-1865 (2008).
95. Smith RR, Barile L, Cho HC et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115(7), 896-908 (2007).
96. 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. Col. Cardiol. 61(10), 1108-1119 (2013).
97. 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).
98. Stamm C, Nasseri B, Hetzer R. Cardiac stem cells in patients with ischaemic cardiomyopathy. Lancet 379(9819), 891 (2012).
99. 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 (2012).
100. Malliaras K, Cheng K, Smith RR et al. Intracoronary cardiosphere-derived cells after myocardial infarction: magnetic resonance imaging analysis of regeneration and determinants of efficacy in the final 1-year results of the CADUCEUS trial. J. Am. Col. Cardiol. 61(10-S), (2013).
101. 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. J. Am. Col. Cardiol. 63(2), 110-122 (2014).
102. Van Berlo JH, Kanisicak O, Maillet M et al. c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature 509(7500), 337-341 (2014).
103. Nadal-Ginard B, Ellison GM, Torella D. Absence of evidence is not evidence of absence: pitfalls of Cre knock-ins in the c-kit locus. Circ. Res. 115(4), 415-418 (2014).
104. Kehat I, Kenyagin-Karsenti D, Snir M et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J. Clin. Invest. 108(3), 407-414 (2001).
105. Xu C, Police S, Rao N, Carpenter MK. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ. Res. 91(6), 501-508 (2002).
106. Mummery C, Ward D, Van Den Brink CE et al. Cardiomyocyte differentiation of mouse and human embryonic stem cells. J. Anat. 200(Pt 3), 233-242 (2002).
107. Wobus AM, Kaomei G, Shan J et al. Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J. Mol. Cell Cardiol. 29(6), 1525-1539 (1997).
108. Wobus AM, Wallukat G, Hescheler J. Pluripotent mouse embryonic stem cells are able to differentiate into cardiomyocytes expressing chronotropic responses to adrenergic and cholinergic agents and Ca2 + channel blockers. Differentiation 48(3), 173-182 (1991).
109. Kehat I, Khimovich L, Caspi O et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat. Biotechnol. 22(10), 1282-1289 (2004).
110. 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 111(1), 11-20 (2005).
111. Fijnvandraat AC, Van Ginneken ACG, Schumacher CA et al. Cardiomyocytes purified from differentiated embryonic stem cells exhibit characteristics of early chamber myocardium. J. Mol. Cell Cardiol. 35(12), 1461-1472 (2003).
112. Snir M, Kehat I, Gepstein A et al. Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 285(6), 2355-2363 (2003).
113. Burridge PW, Anderson D, Priddle H et al. Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel v-96 plate aggregation system highlights interline variability. Stem Cells 25(4), 929-938 (2007).
114. Bratt-Leal AM, Carpenedo RL, Ungrin MD, Zandstra PW, McDevitt TC. Incorporation of biomaterials in multicellular aggregates modulates pluripotent stem cell differentiation. Biomaterials 32(1), 48-56 (2011).
115. 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).
116. Mummery C, Ward-Van Oostwaard D, Doevendans P et al. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endodermlike cells. Circulation 107(21), 2733-2740 (2003).
117. Duan Y, Liu Z, O'neill J, Wan LQ, Freytes DO, Vunjak-Novakovic G. Hybrid gel composed of native heart matrix and collagen induces cardiac differentiation of human embryonic stem cells without supplemental growth factors. J. Cardiovasc. Transl Res. 4(5), 605-615 (2011).
118. Young JL, Engler AJ. Hydrogels with time-dependent material properties enhance cardiomyocyte differentiation in vitro. Biomaterials 32(4), 1002-1009 (2011).
119. Chan CK, Rolle MW, Potter-Perigo S et al. Differentiation of cardiomyocytes from human embryonic stem cells is accompanied by changes in the extracellular matrix production of versican and hyaluronan. J. Cell. Biochem. 111(3), 585-596 (2010).
120. Moyes KW, Sip CG, Obenza W et al. Human embryonic stem cell-derived cardiomyocytes migrate in response to gradients of fibronectin and Wnt5a. Stem Cells Dev. 22(16), 2315-2325 (2013).
121. Zhu W-Z, Van Biber B, Laflamme MA. Methods for the derivation and use of cardiomyocytes from human pluripotent stem cells. Methods Mol. Biol. 767, 419-431 (2011).
122. Laflamme MA, Gold J, Xu C et al. Formation of human myocardium in the rat heart from human embryonic stem cells. Am. J. Pathol. 167(3), 663-671 (2005).
123. Zhu W-Z, Filice D, Palpant NJ, Laflamme MA. Methods for assessing the electromechanical integration of human pluripotent stem cell-derived cardiomyocyte grafts. Methods Mol. Biol. 1181, 229-247 (2014).
124. Chong JJ, Yang X, Don CW et al. Human embryonic-stemcell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510(7504), 273-277 (2014).
125. Madden LR, Mortisen DJ, Sussman EM et al. Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc. Natl Acad. Sci. USA 107(34), 15211-15216 (2010).
126. Paris AP-HD, NCT02057900. Transplantation of human embryonic stem cell-derived progenitors in severe heart failure (ESCORT). http://clinicaltrials.gov/ct2/show/NCT02057900
127. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4), 663-676 (2006).
128. Robinton DA, Daley GQ. The promise of induced pluripotent stem cells in research and therapy. Nature 481(7381), 295-305 (2012).
129. Narazaki G, Uosaki H, Teranishi M et al. Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation 118(5), 498-506 (2008).
130. Mauritz C, Schwanke K, Reppel M et al. Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 118(5), 507-517 (2008).
131. Schenke-Layland K, Rhodes KE, Angelis E et al. Reprogrammed mouse fibroblasts differentiate into cells of the cardiovascular and hematopoietic lineages. Stem Cells 26(6), 1537-1546 (2008).
132. Zhang J, Wilson GF, Soerens AG et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ. Res. 104(4), e30-e41 (2009).
133. Sarvi F, Jain K, Arbatan T et al. Cardiogenesis of embryonic stem cells with liquid marble micro-bioreactor. Adv. Healthc. Mater. 4(1), 77-86 (2014).
134. Heng BC, Haider HK, Sim EK-W, Cao T, Ng SC. Strategies for directing the differentiation of stem cells into the cardiomyogenic lineage in vitro. Cardiovasc. Res. 62(1), 34-42 (2004).
135. Herzenberg LA, Parks D, Sahaf B, Perez O, Roederer M. The history and future of the fluorescence activated cell sorter and flow cytometry: A view from Stanford. Clin. Chem. 48(10), 1819-1827 (2002).
136. Zhao T, Zhang ZN, Rong Z, Xu Y. Immunogenicity of induced pluripotent stem cells. Nature 474(7350), 212-215 (2011).
137. Araki R, Uda M, Hoki Y et al. Negligible immunogenicity of terminally differentiated cells derived from induced pluripotent or embryonic stem cells. Nature 494(7435), 100-104 (2013).
138. Ye L, Chang Y-H, Xiong Q et al. Cardiac repair in a porcine model of acute myocardial infarction with human induced pluripotent stem cell-derived cardiovascular cells. Cell Stem Cell 15(6), 750-761 (2014).
139. Jezierska-Woźniak K, Mystkowska D, Tutas A, Jurkowski MK. Stem cells as therapy for cardiac disease-A review. Folia Histochem. Cytobiol. 49(1), 13-25 (2011).
140. Lundy SD, Zhu W-Z, Regnier M, Laflamme MA. Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev. 22(14), 1991-2002 (2013).
141. Chen JX, Krane M, Deutsch M-A et al. Inefficient reprogramming of fibroblasts into cardiomyocytes using GATA4, MEF2C, and TBX5. Circ. Res. 111(1), 50-55 (2012).
142. Cyranoski D. Stem cells cruise to clinic. Nature 494(7438), 413 (2013).
143. Didie M, Christalla P, Schwoerer AP et al. Derivation of functional cardiomyocytes from parthenogenetic stem cells. Circulation 118(18), S428-S428 (2008).
144. 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. 25(4), 627-634 (2004).
145. Barbash IM, Chouraqui P, Baron J et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation 108(7), 863-868 (2003).
146. 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).
147. Perin EC, Lopez J. Methods of stem cell delivery in cardiac diseases. Nat. Clin. Pract. Cardiovasc. Med. 3(Suppl. 1), S110-S113 (2006).
148. Gyongyosi M, Lang I, Dettke M et al. Combined delivery approach of bone marrow mononuclear stem cells early and late after myocardial infarction: The MYSTAR prospective, randomized study. Nat. Clin. Pract. Cardiovasc. Med. 6(1), 70-81 (2009).
149. Sherman W, Martens TP, Viles-Gonzalez JF, Siminiak T. Catheter-based delivery of cells to the heart. Nat. Clin. Pract. Cardiovasc. Med. 3 (Suppl. 1), 57-64 (2006).
150. 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 Cardiovasc. Interv. 2(1), 9-16 (2009).
151. Pozzobon M, Bollini S, Iop L et al. Human bone marrow-derived CD133+ cells delivered to a collagen patch on cryoinjured rat heart promote angiogenesis and arteriogenesis. Cell Transplant 19(10), 1247-1260 (2010).
152. Alperin C, Zandstra PW, Woodhouse KA. Polyurethane films seeded with embryonic stem cell-derived cardiomyocytes for use in cardiac tissue engineering applications. Biomaterials 26(35), 7377-7386 (2005).
153. Mcdevitt TC, Woodhouse KA, Hauschka SD, Murry CE, Stayton PS. Spatially organized layers of cardiomyocytes on biodegradable polyurethane films for myocardial repair. J. Biomed. Mater. Res. A 66(3), 586-595 (2003).
154. Fujimoto KL, Tobita K, Merryman WD et al. An elastic, biodegradable cardiac patch induces contractile smooth muscle and improves cardiac remodeling and function in subacute myocardial infarction. J. Am. Col. Cardiol. 49(23), 2292-2300 (2007).
155. Ravichandran R, Seitz V, Reddy Venugopal J et al. Mimicking native extracellular matrix with phytic acidcrosslinked protein nanofibers for cardiac tissue engineering. Macromol. Biosci. 13(3), 366-375 (2013).
156. Miki K, Uenaka H, Saito A et al. Bioengineered myocardium derived from induced pluripotent stem cells improves cardiac function and attenuates cardiac remodeling following chronic myocardial infarction in rats. Stem cells Transl. Med. 1(5), 430-437 (2012).
157. Chen Q-Z, Bismarck A, Hansen U et al. Characterisation of a soft elastomer poly(glycerol sebacate) designed to match the mechanical properties of myocardial tissue. Biomaterials 29(1), 47-57 (2008).
158. Krupnick AS, Kreisel D, Engels FH et al. A novel small animal model of left ventricular tissue engineering. J. Heart Lung Transplant. 21(2), 233-243 (2002).
159. Urech L, Bittermann AG, Hubbell JA, Hall H. Mechanical properties, proteolytic degradability and biological modifications affect angiogenic process extension into native and modified fibrin matrices in vitro. Biomaterials 26(12), 1369-1379 (2005).
160. Semler EJ, Ranucci CS, Moghe PV. Mechanochemical manipulation of hepatocyte aggregation can selectively induce or repress liver-specific function. Biotechnol. Bioeng. 69(4), 359-369 (2000).
161. Barocas VH, Moon AG, Tranquillo RT. The fibroblastpopulated collagen microsphere assay of cell traction force-part 2: measurement of the cell traction parameter. J. Biomech. Eng. 117(2), 161-170 (1995).
162. Stile RA, Chung E, Burghardt WR, Healy KE. Poly(Nisopropylacrylamide)-based semi-interpenetrating polymer networks for tissue engineering applications. Effects of linear poly(acrylic acid) chains on rheology. J. Biomater. Sci. Polym. Ed. 15(7), 865-878 (2004).
163. Kim S, Healy KE. Synthesis and characterization of injectable poly(N-isopropylacrylamide-co-acrylic acid) hydrogels with proteolytically degradable cross-links. Biomacromolecules 4(5), 1214-1223 (2003).
164. Stokke BT, Draget KI, Smidsrød O, Yuguchi Y, Urakawa H, Kajiwara K. Small-angle x-ray scattering and rheological characterization of alginate gels. 1. Ca-alginate gels. Macromolecules 33(5), 1853-1863 (2000).
165. Rizzi SC, Ehrbar M, Halstenberg S et al. Recombinant protein-co-peg networks as cell-adhesive and proteolytically degradable hydrogel matrixes. Part II: biofunctional characteristics. Biomacromolecules 7(11), 3019-3029 (2006).
166. Nagueh SF, Shah G, Wu Y et al. Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 110(2), 155-162 (2004).
167. Weis SM, Emery JL, Becker KD, Mcbride DJ Jr., Omens JH, Mcculloch AD. Myocardial mechanics and collagen structure in the osteogenesis imperfecta murine (OIM). Circ. Res. 87(8), 663-669 (2000).
168. Coirault C, Samuel JL, Chemla D et al. Increased compliance in diaphragm muscle of the cardiomyopathic Syrian hamster. J. Appl. Physiol. (1985) 85(5), 1762-1769 (1998).
169. Omens JH, Vaplon SM, Fazeli B, Mcculloch AD. Left ventricular geometric remodeling and residual stress in the rat heart. J. Biomech. Eng. 120(6), 715-719 (1998).
170. Verheggen R, Schulte-Baumann WJ, Hahm G et al. A new technique of dural closure-experience with a vicryl mesh. Acta Neurochir (Wien) 139(11), 1074-1079 (1997).
171. Dai W, Wold LE, Dow JS, Kloner RA. Thickening of the infarcted wall by collagen injection improves left ventricular function in rats: A novel approach to preserve cardiac function after myocardial infarction. J. Am. Col. Cardiol. 46(4), 714-719 (2005).
172. Li Z, Guo X, Guan J. A thermosensitive hydrogel capable of releasing bFGF for enhanced differentiation of mesenchymal stem cell into cardiomyocyte-like cells under ischemic conditions. Biomacromolecules 13(6), 1956-1964 (2012).
173. Iwakura A, Fujita M, Kataoka K et al. Intramyocardial sustained delivery of basic fibroblast growth factor improves angiogenesis and ventricular function in a rat infarct model. Heart Vessels 18(2), 93-99 (2003).
174. Leor J, Aboulafia-Etzion S, Dar A et al. Bioengineered cardiac grafts: A new approach to repair the infarcted myocardium? Circulation 102(Suppl. 3), III-56-III-61 (2000).
175. Zimmermann WH, Didie M, Wasmeier GH et al. Cardiac grafting of engineered heart tissue in syngenic rats. Circulation 106(12 Suppl. 1), I151-157 (2002).
176. Naito H, Melnychenko I, Didié M et al. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114(1 Suppl.), I-72-I-78 (2006).
177. Soong PL, Tiburcy M, Zimmermann WH. Cardiac differentiation of human embryonic stem cells and their assembly into engineered heart muscle. Curr. Protoc. Cell Biol. doi:10.1002/0471143030.cb2308s55 (2012) (Epub ahead of print).
178. Christman KL, Fok HH, Sievers RE, Fang Q, Lee RJ. Fibrin glue alone and skeletal myoblasts in a fibrin scaffold preserve cardiac function after myocardial infarction. Tissue Eng. 10(3-4), 403-409 (2004).
179. 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. Col. Cardiol. 44(3), 654-660 (2004).
180. Ou L, Li W, Zhang Y et al. Intracardiac injection of matrigel induces stem cell recruitment and improves cardiac functions in a rat myocardial infarction model. J. Cell Mol. Med. 15(6), 1310-1318 (2011).
181. Ifkovits JL, Tous E, Minakawa M et al. Injectable hydrogel properties influence infarct expansion and extent of postinfarction left ventricular remodeling in an ovine model. Proc. Natl Acad. Sci. USA 107(25), 11507-11512 (2010).
182. Shen D, Wang X, Zhang L et al. The amelioration of cardiac dysfunction after myocardial infarction by the injection of keratin biomaterials derived from human hair. Biomaterials 32(35), 9290-9299 (2011).
183. Singelyn JM, Dequach JA, Seif-Naraghi SB, Littlefield RB, Schup-Magoffin PJ, Christman KL. Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials 30(29), 5409-5416 (2009).
184. Singelyn JM, Sundaramurthy P, Johnson TD et al. Catheterdeliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. J. Am. Col. Cardiol. 59(8), 751-763 (2012).
185. Landa N, Miller L, Feinberg MS et al. Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat. Circulation 117(11), 1388-1396 (2008).
186. Davis ME, Motion JPM, Narmoneva DA et al. Injectable self-assembling peptide nanofibers create intramyocardial microenvironments for endothelial cells. Circulation 111(4), 442-450 (2005).
187. Yu J, Christman KL, Chin E, Sievers RE, Saeed M, Lee RJ. Restoration of left ventricular geometry and improvement of left ventricular function in a rodent model of chronic ischemic cardiomyopathy. J. Thorac. Cardiovasc. Surg. 137(1), 180-187 (2009).
188. Ryu JH, Kim IK, Cho SW et al. Implantation of bone marrow mononuclear cells using injectable fibrin matrix enhances neovascularization in infarcted myocardium. Biomaterials 26(3), 319-326 (2005).
189. 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).
190. Thompson CA, Nasseri BA, Makower J et al. Percutaneous transvenous cellular cardiomyoplasty. A novel nonsurgical approach for myocardial cell transplantation. J. Am. Col. Cardiol. 41(11), 1964-1971 (2003).
191. Kofidis T, De Bruin JL, Hoyt G et al. Injectable bioartificial myocardial tissue for large-scale intramural cell transfer and functional recovery of injured heart muscle. J. Thorac. Cardiovasc. Surg. 128(4), 571-578 (2004).
192. Kofidis T, Lebl DR, Martinez EC, Hoyt G, Tanaka M, Robbins RC. Novel injectable bioartificial tissue facilitates targeted, less invasive, large-scale tissue restoration on the beating heart after myocardial injury. Circulation 112(9 Suppl.), I173-I177 (2005).
193. Wall ST, Walker JC, Healy KE, Ratcliffe MB, Guccione JM. Theoretical impact of the injection of material into the myocardium: A finite element model simulation. Circulation 114(24), 2627-2635 (2006).
194. Davis ME, Hsieh PCH, 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).
195. Ungerleider JL, Christman KL. Concise review: injectable biomaterials for the treatment of myocardial infarction and peripheral artery disease: translational challenges and progress. Stem Cells Transl. Med. 3(9), 1090-1099 (2014).
196. Bellerophon BCM LLC, NCT01226563. IK-5001 for the prevention of remodeling of the ventricle and congestive heart failure after acute myocardial infarction (PRESERVATION 1). http://clinicaltrials.gov/ct2/show/NCT01226563
197. Lonestar Heart I, NCT01311791. A randomized, controlled study to evaluate Algisyl-LVR™ as a method of left ventricular augmentation for heart failure (AUGMENT-HF). http://clinicaltrials.gov/show/NCT01311791
198. Lonestar Heart I, NCT00847964. Safety and feasibility of Algisyl-LVR™ as a method of left ventricular restoration in patients with DCM undergoing open-heart surgery. http://clinicaltrials.gov/show/NCT00847964
199. Radhakrishnan J, Krishnan UM, Sethuraman S. Hydrogel based injectable scaffolds for cardiac tissue regeneration. Biotechnol. Adv. 32(2), 449-461 (2014).
200. Rastogi S, Gupta RC, Mishra S, Morita H, Tanhehco EJ, Sabbah HN. Long-term therapy with the Acorn cardiac support device normalizes gene expression of growth factors and gelatinases in dogs with heart failure. J. Heart Lung Transplant. 24(10), 1619-1625 (2005).
201. Mann DL, Kubo SH, Sabbah HN et al. Beneficial effects of the CorCap cardiac support device: five-year results from the Acorn trial. J. Thorac. Cardiovasc. Surg. 143(5), 1036-1042 (2012).
202. Prat-Vidal C, Galvez-Monton C, Puig-Sanvicens V et al. Online monitoring of myocardial bioprosthesis for cardiac repair. Int. J. Cardiol. 174(3), 654-661 (2014).
203. Cameron CM, Hu W-S, Kaufman DS. Improved development of human embryonic stem cell-derived embryoid bodies by stirred vessel cultivation. Biotechnol. Bioeng. 94(5), 938-948 (2006).
204. Kofidis T, Lenz A, Boublik J, et al. Pulsatile perfusion and cardiomyocyte viability in a solid three-dimensional matrix. Biomaterials 24(23), 5009-5014 (2003).
205. Ting S, Lecina M, Reuveny S, Oh S. Differentiation of human embryonic stem cells to cardiomyocytes on microcarrier cultures. Curr. Protoc. Stem Cell Biol. doi:10.1002/9780470151808.sc01d07s21 (2012) (Epub ahead of print).
206. Dubois NC, Craft AM, Sharma P et al. SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat. Biotechnol. 29(11), 1011-1018 (2011).
207. Unger C, Skottman H, Blomberg P, Dilber MS, Hovatta O. Good manufacturing practice and clinical-grade human embryonic stem cell lines. Hum. Mol. Genet. 17(R1), R48-R53 (2008).
208. Yildirimer L, Seifalian AM. Three-dimensional biomaterial degradation-material choice, design and extrinsic factor considerations. Biotechnol. Adv. 32(5), 984-999 (2014).