Injectable cardiac tissue engineering for the treatment of myocardial infarction

Journal of Cellular and Molecular Medicine

Volumn 14, Issue 5, 2010, Pages 1044-1055

  Wang, Haibin ^a   Zhou, Jin ^a   Liu, Zhiqiang ^a   Wang, Changyong ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

Biomaterials; Injectable cardiac tissue engineering; Myocardial infarction; Stem cells

Indexed keywords

BIOMATERIAL;

CYTOLOGY; EMBRYONIC STEM CELL; HEART INFARCTION; HEART MUSCLE; HUMAN; INJECTION; METHODOLOGY; PATHOLOGY; REVIEW; TISSUE ENGINEERING; MYOCARDIAL INFARCTION; PROCEDURES;

BIOCOMPATIBLE MATERIALS; EMBRYONIC STEM CELLS; HUMANS; INJECTIONS; MYOCARDIAL INFARCTION; MYOCARDIUM; TISSUE ENGINEERING;

EID: 77954741603     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2010.01046.x     Document Type: Review

References (120)

1. Tateishi K, Takehara N, Matsubara H. Stemming heart failure with cardiac- or reprogrammed-stem cells. J Cell Mol Med. 2008, 12:2217-32.
2. Virag JA, Rolle ML, Reece J. Fibroblast growth factor-2 regulates myocardial infarct repair: effects on cell proliferation, scar contraction, and ventricular function. Am J Pathol. 2007, 171:1431-40.
3. Zimmermann WH, Cesnjevar R. Cardiac tissue engineering: implications for pediatric heart surgery. Pediatr Cardiol. 2009, 30:716-23.
4. Murry CE, Field LJ, Menasché P. Cell-based cardiac repair: reflections at the 10-year point. Circulation 2005, 15:3174-83. 112
5. Murry CE, Wiseman RW, Schwartz SM. Skeletal myoblast transplantation for repair of myocardial necrosis. J Clin Invest. 1996, 98:2512-23.
6. Murry CE, Soonpaa MH, Reinecke H. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature. 2004, 428:664-8.
7. Mangi AA, Noiseux N, Kong D. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 2003, 9:1195-1201.
8. Beltrami AP, Barlucchi L, Torella D. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003, 114:763-76.
9. Doss MX, Koehler CI, Gissel C. Embryonic stem cells: a promising tool for cell replacement therapy. J Cell Mol Med. 2004, 8:465-73.
10. Smits AM, van Vliet P, Hassink RJ. The role of stem cells in cardiac regeneration. J Cell Mol Med. 2005, 9:25-36.
11. He Q, Trindade PT, Stumm M. Fate of undifferentiated mouse embryonic stem cells within the rat heart: role of myocardial infarction and immune suppression. J Cell Mol Med 2009, 13:188-201.
12. Nelson TJ, Martinez-Fernandez A, Yamada S. Repair of acute myocardial infarction by human stemness factors induced pluripotent stem cells. Circulation. 2009, 120:408-16.
13. Leor J, Aboulafia-Etzion S, Dar A. Bioengineered cardiac grafts: a new approach to repair the infarcted myocardium. Circulation 2000, 102:III56-61.
14. Reinecke H, Murry CE. Taking the death toll after cardiomyocyte grafting: a reminder of the importance of quantitative biology. J Mol Cell Cardiol 2002, 34:251-3.
15. Müller-Ehmsen J, Whittaker P, Kloner RA. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. J Mol Cell Cardiol 2002, 34:107-16.
16. Laflamme MA, Chen KY, Naumova AV. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol. 2007, 25:1015-24.
17. Langer R, Vacanti JP. Tissue engineering. Science. 1993, 260:920-6.
18. Leor J, Landa N, Cohen S. Renovation of the injured heart with myocardial tissue engineering. Expert Rev Cardiovasc Ther. 2006, 4:239-52.
19. Bleiziffer O, Eriksson E, Yao F. Gene transfer strategies in tissue engineering. J Cell Mol Med. 2007, 11:206-23.
20. Kneser U, Schaefer DJ, Polykandriotis E. Tissue engineering of bone: the reconstructive surgeon's point of view. J Cell Mol Med. 2006, 10:7-19.
21. Horch RE, Kopp J, Kneser U. Tissue engineering of cultured skin substitutes. J Cell Mol Med. 2005, 9:592-608.
22. Chalfoun CT, Wirth GA, Evans GR. Tissue engineered nerve constructs: where do we stand. J Cell Mol Med. 2006, 10:309-17.
23. Fiegel HC, Lange C, Kneser U. Fetal and adult liver stem cells for liver regeneration and tissue engineering. J Cell Mol Med. 2006, 10:577-87.
24. Lü SH, Wang HB, Liu H. Reconstruction of engineered uterine tissues containing smooth muscle layer in collagen/matrigel scaffold in vitro. Tissue Eng Part A. 2009, 15:1611-8.
25. Zhang WJ, Liu W, Cui L. Tissue engineering of blood vessel. J Cell Mol Med. 2007, 11:945-57.
26. Guo XM, Zhao YS, Chang HX. Creation of engineered cardiac tissue in vitro from mouse embryonic stem cells. Circulation. 2006, 113:2229-37.
27. Zimmermann WH, Melnychenko I, Wasmeier G. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med. 2006, 12:452-8.
28. Hutmacher DW, Horch RE, Loessner D. Translating tissue engineering technology platforms into cancer research. J Cell Mol Med. 2009, 13:1417-27.
29. Shimizu T, Yamato M, Isoi Y. Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res 2002, 90:e40.
30. Ott HC, Matthiesen TS, Goh SK. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med. 2008, 14:213-21.
31. Christman KL, Lee RJ. Biomaterials for the treatment of myocardial infarction. J Am Coll Cardiol. 2006, 48:907-13.
32. Lu WN, Lü SH, Wang HB. Functional improvement of infarcted heart by co-injection of embryonic stem cells with temperature-responsive chitosan hydrogel. Tissue Eng Part A. 2009, 15:1437-47.
33. Gimble JM. Adipose tissue-derived therapeutics. Expert Opin Biol Ther. 2003, 3:705-13.
34. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res. 2007, 100:1249-60.
35. Li Z, Lee A, Huang M. Imaging survival and function of transplanted cardiac resident stem cells. J Am Coll Cardiol. 2009, 53:1229-40.
36. Joggerst SJ, Hatzopoulos AK. Stem cell therapy for cardiac repair: benefits and barriers. Expert Rev Mol Med 2009, 11:e20.
37. Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 2008, 132:661-80.
38. Kehat I, Kenyagin-Karsenti D, Snir M. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest. 2001, 108:407-14.
39. Laflamme MA, Gold J, Xu C. Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol. 2005, 167:663-71.
40. Behfar A, Perez-Terzic C, Faustino RS. Cardiopoietic programming of embryonic stem cells for tumor-free heart repair. J Exp Med. 2007, 204:405-20.
41. Segers VF, Lee RT. Stem-cell therapy for cardiac disease. Nature. 2008, 451:937-42.
42. Huber I, Itzhaki I, Caspi O. Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. FASEB J. 2007, 21:2551-63.
43. Tomescot A, Leschik J, Bellamy V. Differentiation in vivo of cardiac committed human embryonic stem cells in postmyocardial infarcted rats. Stem Cells. 2007, 25:2200-5.
44. Kang L, Wang J, Zhang Y. iPS cells can support full-term development of tetraploid blastocyst-complemented embryos. Cell Stem Cell. 2009, 5:135-8.
45. Wakayama T, Tabar V, Rodriguez I. Differentiation of embryonic stem cell lines generated from adult somatic cells by nuclear transfer. Science. 2001, 292:740-3.
46. Byrne JA, Pedersen DA, Clepper LL. Producing primate embryonic stem cells by somatic cell nuclear transfer. Nature. 2007, 450:497-502.
47. Koh CJ, Atala A. Therapeutic cloning applications for organ transplantation. Transpl Immunol. 2004, 12:193-201.
48. Kohda T, Inoue K, Ogonuki N. Variation in gene expression and aberrantly regulated chromosome regions in cloned mice. Biol Reprod. 2005, 73:1302-11.
49. Brambrink T, Hochedlinger K, Bell G. ES cells derived from cloned and fertilized blastocysts are transcriptionally and functionally indistinguishable. Proc Natl Acad Sci USA. 2006, 103:933-8.
50. Lü SH, Wang H, Lu WN. Both the transplantation of somatic cell nuclear transfer - and fertilization-derived-mouse embryonic stem cells with temperature-responsive chitosan hydrogel improve myocardial performance in infarcted rat hearts. Tissue Eng Part A. 2010, 16:1303-15.
51. Takahashi K, Tanabe K, Ohnuki M. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007, 131:861-72.
52. Yu J, Vodyanik MA, Smuga-Otto K. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007, 318:1917-20.
53. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature. 2007, 448:313-7.
54. Zhang J, Wilson GF, Soerens AG. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 2009, 104:e30-41.
55. Menasché P. Stem cells for clinical use in cardiovascular medicine: current limitations and future perspectives. Thromb Haemost. 2005, 94:697-701.
56. Menasché P. Skeletal myoblasts and cardiac repair. J Mol Cell Cardiol. 2008, 45:545-53.
57. Marelli D, Ma F, Chiu RC. Satellite cell implantation for neomyocardial regeneration. Transplant Proc 1992, 24:2995.
58. Yoon PD, Kao RL, Magovern GJ. Transplanting satellite cells into damaged myocardium. Tex Heart Inst J. 1995, 22:119-25.
59. Taylor DA, Atkins BZ, Hungspreugs P. Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat Med. 1998, 4:929-33.
60. Tambara K, Sakakibara Y, Sakaguchi G. Transplanted skeletal myoblasts can fully replace the infarcted myocardium when they survive in the host in large numbers. Circulation 2003, 108:II-259-63.
61. Christman KL, Vardanian AJ, Fang Q. 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.
62. van den Bos EJ, Thompson RB, Wagner A. Functional assessment of myoblast transplantation for cardiac repair with magnetic resonance imaging. Eur J Heart Fail. 2005, 7:435-43.
63. Menasché P, Hagége AA, Scorsin M. Myoblast transplantation for heart failure. Lancet. 2001, 357:279-80.
64. Reinecke H, Minami E, Poppa V. Evidence for fusion between cardiac and skeletal muscle cells. Circ Res 2004, 94:e56-60.
65. Reinecke H, MacDonald GH, Hauschka SD. Electromechanical coupling between skeletal and cardiac muscle. Implications for infarct repair. J Cell Biol 2000, 149:731-40.
66. Tomita S, Li RK, Weisel RD. Autologous transplantation of bone marrow cells improves damaged heart function. Circulation 1999, 100:II247-56.
67. Orlic D, Kajstura J, Chimenti S. Bone marrow cells regenerate infarcted myocardium. Nature. 2001, 410:701-5.
68. Murry CE, Soonpaa MH, Reinecke H. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature. 2004, 428:664-8.
69. Toma C, Pittenger MF, Cahill KS. Human mesenchymal stem cells differentiate to a cardiomyocytes phenotype in the adult murine heart. Circulation. 2002, 105:93-8.
70. Dai W, Hale SL, Martin BJ. Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium: short- and long-term effects. Circulation. 2005, 112:214-23.
71. Jin J, Jeong SI, Shin YM. Transplantation of mesenchymal stem cells within a poly(lactide-co-epsilon-caprolactone) scaffold improves cardiac function in a rat myocardial infarction model. Eur J Heart Fail. 2009, 11:147-53.
72. Beltrami AP, Barlucchi L, Torella D. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003, 114:763-76.
73. Barile L, Chimenti I, Gaetani R. Cardiac stem cells: isolation, expansion and experimental use for myocardial regeneration. Nat Clin Pract Cardiovasc Med 2007, 4(Suppl 1):S9-14.
74. Smits AM, van Vliet P, Metz CH. Human cardiomyocyte progenitor cells differentiate into functional mature cardiomyocytes: an in vitro model for studying human cardiac physiology and pathophysiology. Nat Protoc. 2009, 4:232-43.
75. Pompilio G, Cannata A, Peccatori F. Autologous peripheral blood stem cell transplantation for myocardial regeneration: a novel strategy for cell collection and surgical injection. Ann Thorac Surg. 2004, 78:1808-12.
76. Ma N, Stamm C, Kaminski A. Human cord blood cells induce angiogenesis following myocardial infarction in NOD/scid-mice. Cardiovasc Res. 2005, 66:45-54.
77. Schuh A, Liehn EA, Sasse A. Transplantation of endothelial progenitor cells improves neovascularization and left ventricular function after myocardial infarction in a rat model. Basic Res Cardiol. 2008, 103:69-77.
78. Zuk PA, Zhu M, Mizuno H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001, 7:211-28.
79. Zuk PA, Zhu M, Ashjian P. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002, 13:4279-95.
80. Wang L, Deng J, Tian W. Adipose-derived stem cells are an effective cell candidate for treatment of heart failure: an MR imaging study of rat hearts. Am J Physiol Heart Circ Physiol 2009, 297:H1020-31.
81. van der Bogt KE, Schrepfer S, Yu J. Comparison of transplantation of adipose tissue- and bone marrow-derived mesenchymal stem cells in the infarcted heart. Transplantation 2009, 87:642-52.
82. Ahmed TA, Dare EV, Hincke M. Fibrin: a versatile scaffold for tissue engineering applications. Tissue Eng Part B Rev. 2008, 14:199-215.
83. Chekanov V, Akhtar M, Tchekanov G. Transplantation of autologous endothelial cells induces angiogenesis. Pacing Clin Electrophysiol. 2003, 26:496-9.
84. Christman KL, Fok HH, Sievers RE. Fibrin glue alone and skeletal myoblasts in a fibrin scaffold preserve cardiac function after myocardial infarction. Tissue Eng. 2004, 10:403-9.
85. Ryu JH, Kim IK, Cho SW. Implantation of bone marrow mononuclear cells using injectable fibrin matrix enhances neovascularization in infarcted myocardium. Biomaterials. 2005, 26:319-26.
86. Huang NF, Yu J, Sievers R. Injectable biopolymers enhance angiogenesis after myocardial infarction. Tissue Eng. 2005, 11:1860-6.
87. Martens TP, Godier AF, Parks JJ. Percutaneous cell delivery into the heart using hydrogels polymerizing in situ. Cell Transplant. 2009, 18:297-304.
88. Christman KL, Fang Q, Yee MS. Enhanced neovasculature formation in ischemic myocardium following delivery of pleiotrophin plasmid in a biopolymer. Biomaterials. 2005, 26:1139-44.
89. Koh CJ, Atala A. Tissue engineering, stem cells, and cloning: opportunities for regenerative medicine. J Am Soc Nephrol. 2004, 15:1113-25.
90. Leor J, Amsalem Y, Cohen S. Cells, scaffolds, and molecules for myocardial tissue engineering. Pharmacol Ther. 2005, 105:151-63.
91. Landa N, Miller L, Feinberg MS. Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat. Circulation. 2008, 117:1388-96.
92. Tsur-Gang O, Ruvinov E, Landa N. The effects of peptide-based modification of alginate on left ventricular remodeling and function after myocardial infarction. Biomaterials. 2009, 30:189-95.
93. Leor J, Tuvia S, Guetta V. Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in swine. J Am Coll Cardiol. 2009, 54:1014-23.
94. Yu J, Christman KL, Chin E. Restoration of left ventricular geometry and improvement of left ventricular function in a rodent model of chronic ischemic cardiomyopathy. J Thorac Cardiovasc Surg. 2009, 137:180-7.
95. Kofidis T, de Bruin JL, Hoyt G. Injectable bioartificial myocardial tissue for large-scale intramural cell transfer and functional recovery of injured heart muscle. J Thorac Cardiovasc Surg. 2004, 128:571-8.
96. Kofidis T, Lebl DR, Martinez EC. Novel injectable bioartificial tissue facilitates targeted, less invasive, large-scale tissue restoration on the beating heart after myocardial injury. Circulation 2005, 112:I173-7.
97. Zhang P, Zhang H, Wang H. Artificial matrix helps neonatal cardiomyocytes restore injured myocardium in rats. Artif Organs. 2006, 30:86-93.
98. Dai W, Wold LE, Dow JS. Thickening of the infracted wall by collagen injection improves left ventricular function in rats: a novel approach to preserve cardiac function after myocardial infarction. J Am Coll Cardiol. 2005, 46:714-9.
99. Suuronen EJ, Veinot JP, Wong S. Tissue-engineered injectable collagen-based matrices for improved cell delivery and vascularization of ischemic tissue using CD1331 progenitors expanded from the peripheral blood. Circulation. 2006, 114:138-44.
100. Kutschka I, Chen IY, Kofidis T. Collagen matrices enhance survival of transplanted cardiomyoblasts and contribute to functional improvement of ischemic rat hearts. Circulation. 2006, 114:167-73.
101. Kutschka I, Chen IY, Kofidis T. In vivo optical bioluminescence imaging of collagen-supported cardiac cell grafts. J Heart Lung Transplant. 2007, 3:273-80.
102. Zhang Y, Thorn S, DaSilva JN. Collagen-based matrices improve the delivery of transplanted circulating progenitor cells: development and demonstration by ex vivo radionuclide cell labeling and in vivo tracking with positron-emission tomography. Circ Cardiovasc Imaging. 2008, 3:197-204.
103. Kim IY, Seo SJ, Moon HS. Chitosan and its derivatives for tissue engineering applications. Biotechnol Adv. 2008, 26:1-21.
104. Hoemann CD, Chenite A, Sun J. Cytocompatible gel formation of chitosan-glycerol phosphate solutions supplemented with hydroxyl ethyl cellulose is due to the presence of glyoxal. J Biomed Mater Res A. 2007, 83:521-9.
105. Chenite A, Chaput C, Wang D. Novel injectable neutral solutions of chitosan form biodegradable gels in situ. Biomaterials. 2000, 21:2155-61.
106. Li J, Xu Z. Physical characterization of a chitosan-based hydrogel delivery system. J Pharm Sci. 2002, 91:1669-77.
107. Chupa JM, Foster AM, Sumner SR. Vascular cell responses to polysaccharide materials: in vitro and in vivo evaluations. Biomaterials. 2000, 21:2315-22.
108. Ishihara M, Nakanishi K, Ono K. Photocrosslinkable chitosan as a dressing for wound occlusion and accelerator in healing process. Biomaterials. 2002, 23:833-40.
109. Davis ME, Motion JP, Narmoneva DA. Injectable self-assembling peptide nanofibers create intramyocardial microenvironments for endothelial cells. Circulation. 2005, 111:442-50.
110. Takehara N, Tsutsumi Y, Tateishi K. Controlled delivery of basic fibroblast growth factor promotes human cardiosphere-derived cell engraftment to enhance cardiac repair for chronic myocardial infarction. J Am Coll Cardiol. 2008, 52:1858-65.
111. Singelyn JM, DeQuach JA, Seif-Naraghi SB. Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials. 2009, 30:5409-16.
112. Shapira-Schweitzer K, Seliktar D. Matrix stiffness affects spontaneous contraction of cardiomyocytes cultured within a PEGylated fibrinogen biomaterial. Acta Biomater. 2007, 3:33-41.
113. Jiang XJ, Wang T, Li XY. Injection of a novel synthetic hydrogel preserves left ventricle function after myocardial infarction. J Biomed Mater Res A. 2009, 90:472-7.
114. Wang T, Wu DQ, Jiang XJ. Novel thermosensitive hydrogel injection inhibits post-infarct ventricle remodelling. Eur J Heart Fail. 2009, 11:14-9.
115. Teng CJ, Luo J, Chiu RC. Massive mechanical loss of microspheres with direct intramyocardial injection in the beating heart: implications for cellular cardiomyoplasty. J Thorac Cardiovasc Surg. 2006, 132:628-32.
116. Murata H, Masuo M, Yoshimoto H. Oozing type cardiac rupture repaired with percutaneous injection of fibrin-glue into the pericardial space, case report. Jpn Circ J. 2000, 64:312-5.
117. Joho S, Asanoi H, Sakabe M. Long-term usefulness of percutaneous intrapericardial fibrin-glue fixation therapy for oozing type of left ventricular free wall rupture, a case report. Circ J. 2002, 66:705-6.
118. Terashima M, Fujiwara S, Yaginuma GY. Outcome of percutaneous intrapericardial fibrin-glue injection therapy for left ventricular free wall rupture secondary to acute myocardial infarction. Am J Cardiol. 2008, 101:419-21.
119. Chachques JC, Trainini JC, Lago N. Myocardial Assistance by Grafting a New Bioartificial Upgraded Myocardium (MAGNUM Trial): Clinical feasibility study. Ann Thorac Surg. 2008, 85:901-8.
120. Chachques JC. Cellular cardiac regenerative therapy in which patients. Expert Rev Cardiovasc Ther. 2009, 7:911-9.