Engineering the heart piece by piece: State of the art in cardiac tissue engineering

Regenerative Medicine

Volumn 2, Issue 2, 2007, Pages 125-144

  Hecker, Louise ^a   Birla, Ravi K ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Active force; Artificial heart; Biomaterials; Bioreactors; Fibrin gel; Heart muscle; Perfusion; Scaffolds; Self organization; Tissue engineering

Indexed keywords

COLLAGEN; DACRON; FIBRIN; MATRIX METALLOPROTEINASE; POLITEF; POLYGLYCOLIC ACID;

ACUTE HEART INFARCTION; ARTERY INTIMA PROLIFERATION; BIODEGRADABLE IMPLANT; BIOREACTOR; CELL PROLIFERATION; CELL VIABILITY; CONGESTIVE HEART FAILURE; DEGRADATION KINETICS; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; HEART ASSIST DEVICE; HEART LEFT VENTRICLE; HEART MUSCLE; HEART MUSCLE INJURY; HEART TRANSPLANTATION; HEART VALVE PROSTHESIS; HEART VALVE REPLACEMENT; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HYDROGEL; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; MEDICAL TECHNOLOGY; NONHUMAN; PERIPHERAL BLOOD STEM CELL TRANSPLANTATION; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; SKELETAL MUSCLE; STEM CELL TRANSPLANTATION; THROMBOGENESIS; TISSUE ENGINEERING; TISSUE REGENERATION; TISSUE TRANSPLANTATION;

ANIMALS; BIOARTIFICIAL ORGANS; BIOREACTORS; CELL CULTURE TECHNIQUES; HUMANS; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS; REGENERATIVE MEDICINE; TISSUE ENGINEERING;

EID: 34249672809     PISSN: 17460751     EISSN: None     Source Type: Journal    
DOI: 10.2217/17460751.2.2.125     Document Type: Review

References (121)

1. Fuchs JR, Nasseri BA, Vacanti JP: Tissue engineering: a 21st century solution to surgical reconstruction. Ann. Thorac. Surg. 72(2), 577-591 (2001).
2. Langer R, Vacanti JP: Tissue engineering. Science 260(5110), 920-926 (1993).
3. Lysaght MJ, Reyes J: The growth of tissue engineering. Tissue Eng. 7(5), 485-493 (2001).
4. Nerem RM: Tissue engineering: the hope, the hype, and the future. Tissue Eng. 12(5). 1143-1150 (2006).
5. Vacanti CA: History of tissue engineering and a glimpse into its future. Tissue Eng. 12(5), 1137-1142 (2006).
6. Cleland JG, Khand A, Clark A: The heart failure epidemic: exactly how big is it? Eur Heart J. 22(8), 623-626 (2001).
7. Goldstein S: Heart failure therapy at the turn of the century. Heart Fail. Rev. 6(1), 7-14 (2001).
8. Miniati DN, Robbins RC: Heart transplantation: a thirty-year perspective. Ann. Rev. Med. 53, 189-205 (2002).
9. Akins RE: Can tissue engineering mend broken hearts? Cirr. Res. 90(2), 120-122 (2002).
10. Eschenhagen T, Didie M, Heubach J, Ravens U, Zimmermann WH: Cardiac tissue engineering. Transplant Immunol. 9(2-4), 315-321 (2002).
11. Fedak PW, Weisel RD, Verma S, Mickle DA, Li RK: Restoration and regeneration of failing myocardium with cell transplantation and tissue engineering. Semin. Thorac. Cardiovasc. Surg. 15(3), 277-286 (2003).
12. Mann BK, West JL: Tissue engineering in the cardiovascular system: progress toward a tissue engineered heart. Anatomical Record 263(4), 367-371 (2001).
13. Papadaki M: Cardiac muscle tissue engineering. IEEE Eng. Med. Biol. Mag. 22(3), 153-154 (2003).
14. Shimizu T, Yamato M, Kikuchi A, Okano T. Cell sheet engineering for myocardial tissue reconstruction. Biomaterials 24(13), 2309-2316 (2003).
15. Zimmermann WH, Eschenhagen T: Cardiac tissue engineering for replacement therapy. Heart Fail. Rev. 8(3), 259-269 (2003).
16. Weinberg CB, Bell E: A blood vessel model constructed from collagen and cultured vascular cells. Science 231(4736). 397-400 (1986).
17. L'Heureux N, Paquet S, Labbe R, Germain L, Auger FA: A completely biological tissue-engineered human blood vessel. FASEB J. 12(1), 47-56 (1998).
18. Thomas AC, Campbell GR, Campbell JH: Advances in vascular tissue engineering. Cardiovas. Pathol. 12(5), 271-276 (2003).
19. Nerem RM, Seliktar D: Vascular tissue engineering. Annu. Rev. Biomed. Eng. 3, 225-243 (2001).
20. Grassi ED, Oegema TR, Tranquillo RT: A fibrin-based arterial media equivalent. J. Biomed. Mater. Res. A 66(3), 550-561, (2003).
21. Stock UA, Vacanti JP, Mayer JE Jr, Wahlers T: Tissue engineering of heart valves - current aspects. Thorac. Cardiovasc. Surg. 50(3), 184-193 (2002).
22. Butany J, Ahluwalia MS, Munroe C et al.: Mechanical heart valve prostheses: identification and evaluation Cardiovasc. Pathol. 12(1), 1-22 (2003)
23. Butany J, Fayet C, Ahluwalia MS et al.: Biological replacement heart valves. Identification and evaluation. Cardiovasc. Pathol. 12(3), 119-139 (2003).
24. Sapirstein JS, Smith PK: The 'ideal' replacement heart valve. Am. Heart J. 141(5), 856-860 (2001).
25. Bader A, Schilling T, Teebken OE et al.: Tissue engineering of heart a valves - human endothelial cell seeding of detergent acellularized porcine valves. Eur. J. Cardiothorac. Surg. 14(3), 279-284 (1998).
26. Shinoka T, Breuer CK, Tanel RE et al.: Tissue engineering heart valves: valve leaflet replacement study in a lamb model. Ann. Thorac. Surg. 60(6 Suppl.), S513-S516 (1995).
27. Sodian R, Sperling JS, Martin DP, Stock U, Mayer JE Jr, Vacanti JP: Tissue engineering of a trileaflet heart valve early in vitro experiences with a combined polymer. Tissue Eng. 5(5), 489-494 (1999).
28. Stock UA, Nagashima M, Khalil PN et al.: Tissue-engineered valved condults in the pulmonary circulation. Ann. Thorac. Cardiovasc. Surg. 119(4 Pt 1), 732-740 (2000).
29. Zeltinger J, Landeen LK, Alexander HG, Kidd ID, Sibanda B: Development and characterization of tissue-engineered aortic valves. Tissue Eng. 7(1), 9-22 (2001).
30. Stevenson LW, Kormos RL: Mechanical cardiac support 2000: current applications and future trial design. J. Heart Lung Transplant. 20(1), 1-38 (2001).
31. Nag AC, Zak R: Dissociation of adult mammalian heart into single cell suspension: an ultrastructural study. J. Anatomy 129(Pt 3), 541-559 (1979).
32. Caspi O, Lesman A, Basevitch Y et al.: Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ. Res. 100(2), 263-272 (2007).
33. Li RK, Yau TM. Sakai T, Mickle DA, Weisel RD: Cell therapy to repair broken hearts. Can. J. Cardiol. 14(5), 735-744 (1998).
34. Laflamme MA, Murry CE: Regenerating the heart. Nat. Biotechnol. 23(7), 845-856 (2005).
35. Murry CE, Field LJ, Menasche P: Cell-based cardiac repair: reflections at the 10-year point. Circulation 112(20). 3174-3183 (2005).
36. Taylor DA, Silvestry SC, Bishop SP et al.: Delivery of primary autologous skeletal myoblasts into rabbit heart by coronary infusion: a potential approach to myocardial repair. Proc. Assoc. Am. Physicans 109(3), 245-253 (1997).
37. Chiu RC, Zibaitis A, Kao RL: Cellular cardiomyoplasty: myocardial regeneration with satellite cell implantation. Ann. Thorac. Surg. 60(1), 12-18 (1995).
38. Zibattis A, Greentree D, Ma F, Marelli D, Duong M, Chiu RC: Myocardial regeneration with satellite cell implantation. Transplant. Proc. 26(6), 3294 (1994).
39. Murry CE, Wiseman RW, Schwartz SM, Hauschka SD: Skeletal myoblast transplantation for repair of myocardial necrosis. J. Clin. Invest. 98(11), 2512-2523 (1996).
40. 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).
41. Atkins BZ, Lewis CW, Kraus WE, Hutcheson KA, Glower DD, Taylor DA: Intracardiac transplantation of skeletal myoblasts yields two populations of striated cells in situ. Ann. Thorac. Surg. 67(1), 124-129 (1999).
42. Dawn B. Bolli R: Bone marrow cells for cardiac regeneration: the quest for the protagonist continues. Cardiovasc. Res. 65(2), 293-295 (2005).
43. Vanelli P, Beltrami S, Cesana E et al.: Cardiac precursors in human bone marrow and card blood: in vitro cell cardiogenesis. Ital. Heart J. 5(5), 384-388 (2004).
44. Shim WS, Jiang S, Wong P et al.: Ex vivo differentiation of human adult bone marrow stem cells into cardiomyocyte-like cells. Biochem. Biophys. Res. Commun. 324(2), 481-488 (2004).
45. 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).
46. Fernandez-Aviles F, San Roman JA, Garcia-Frade J et al.: Experimental and clinical regenerative capability of human bone marrow cells after myocardial infarction. Cir. Res. 95(7), 742-748 (2004).
47. Rehman J, Li J, Orschell CM, March KL: Peripheral blood 'endothelial progenitor cells' are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107(8), 1164-1169 (2003).
48. 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. 7(4), 430-436 (2001).
49. Laflamme MA, Gold J, Xu C et al.: Formation of human myocardium in the rat heart from human embryonic stem cells. Am. J Pathol. 67(3). 663-671 (2005).
50. 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).
51. 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).
52. Mummery C, Ward-van Oostwaard D, Doevendans P et al.: Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107(21), 2733-2740 (2003).
53. 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).
54. Amit M, Itskovitz-Eldor J: Derivation and spontaneous diffierentiation of human embryonic stem cells. J. Anatomy 200(Pt 3), 225-232 (2002).
55. 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).
56. Sachinidis A, Fleischmann BK, Kolossov E, Wartenberg M, Sauer H, Hescheler J: Cardiac specific differentiation of mouse embryonic stem cells. Cardiovasc. Res. 58(2), 278-291 (2003).
57. Zandstra PW, Bauwens C, Yin T et al.: Scalable production of embryonic stem cell-derived cardiomyocytes. Tissue Eng. 9(4), 767-778 (2003). Erratum appears in Tissue Eng 9(6), 1331 (2003).
58. Zweigerdt R, Burg M, Willbold E, Abts H, Ruediger M: Generation of confluent cardiomyocyte monolayers derived from embryonic stem cells in suspension: a cell source for new therapies and screening strategies. Cytotherapy 5(5), 399-413 (2003).
59. Schroeder M, Niebruegge S, Werner A et al.: Differentiation and lineage selection of mouse embryonic stem cells in a stirred bench scale bioreactor with automated process control. Biotechnol. Bioeng. 92(7), 920-933 (2005).
60. van Vliet P, Sluijter JP, Doevendans PA, Goumans MJ: Isolation and expansion of resident cardiac progenitor cells. Expert Rev. Cardiovasc. Ther. 5(1), 33-43 (2007).
61. Davis ME, Hsieh PC, Grodzinsky AJ, Lee RT: Custom design of the cardiac microenvironment with biomaterials. Circ. Res. 97(1), 8-15 (2005).
62. Hollister SJ: Porous scaffold design for tissue engineering. Nat. Matter. 4(7), 518-524 (2005).
63. Lutolf MP, Hubbell JA: Synthetic biomaterials as instructive extacellular microenvironments far morphogenesis in tissue engineering. Nat. Biotechnol. 23(1), 47-55 (2005).
64. Ratner BD, Bryant SJ: Biomaterials: where we have been and where we are going. Annu. Rev. Biomed. Eng. 6, 41-75 (2004).
65. Christman KL, Lee RJ: Biomaterials for the treatment of myocardial infarction. J. Am. Coll. Cardiol. 48(5), 907-913 (2006).
66. Bursac N, Papadaki M, Cohen RJ et al.: Cardiac muscle tissue engineering toward an in vitro model for electrophysiological studies. Am. J. Physiol. 277 (2 Pt 2), H433-H444 (1999).
67. Carrier RL, Papadaki M, Rupnick M et al.: Cardiac tissue engineering: cell seeding, cultivation parameters, and tissue construct characterization. Biotechnol. Bioeng. 64(5), 580-589 (1999).
68. Papadaki M, Bursac N, Langer R, Merok J, Vunjak-Novakovic G, Freed LE: Tissue engineering of functional cardiac muscle: molecular structural, and electrophysiological studies. Am. J. Physiol. Heart Circ. Physiol. 280(1), H168-H178 (2001).
69. Radisic M, Euloth M, Yang L, Langer R, Freed LE, Vunjak-Novakovic G: High-density seeding of myocyte cells for cardiac tissue engineering. Biotechnol. Bioeng. 82(4), 403-414 (2003).
70. Eschenhagen T, Fink C, Remmers U et al.: Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J. 11(8), 683-694 (1997).
71. Eschenhagen T, Didie M, Munzel F, Schubert P, Schneiderbanger K, Zimmermann WH: 3D engineered heart tissue for replacement therapy. Basic Res. Cardiol. 97(Suppl. 1), I146-I152 (2002).
72. Zimmermann WH, Fink C, Kralisch D, Remmers U, Well J, Eschenhagen T. Three-dimensional engineered head tissue from neonatal rat cardiac myocytes. Biotechnol. Bioeng. 68(1), 106-114 (2000).
73. Zimmermann WH, Schnelderbanger K, Schubert P et al.: Tissue engineering of a differentiated cardiac muscle construct. Circ. Res. 90(2), 223-230 (2002).
74. Dar A, Shachar M, Leor J, Cohen S: Optimization of cardiac cell seeding and distribution in 3D porous alginate scaffolds. Biotechnol. Bioeng. 80(3), 305-312 (2002).
75. Davis ME, Hsieh PC, Grodzinsky AJ, Lee RT: Custom design of the cardiac microenvironment with biomaterials. Circ. Res. 97(1), 8-15 (2005).
76. Rosso F, Marino G, Giordano A, Barbarisi M, Parmeggiani D, Barbarisi A: Smart materials as scaffolds for tissue engineering. J. Cell. Physiol. 203(3), 465-470 (2005).
77. Zisch AH, Lutolf MP, Ehrbar M et al.: Cell-demanded release of VEGF from synthetic, biointeractive cell ingrowth matrices for vascularized tissue growth. FASEB J. 17(15), 2260-2262 (2003).
78. Ehrbar M, Djonov VG, Schnell C et al.: Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Cicr. Res. 94(8), 1124-1132 (2004).
79. Seliktar D, Zisch AH, Lutolf MP, Wrana JL, Hubbell JA: MMP-2 sensitive, VEGF-bearing bioactive hydrogels for promotion of vascular healing. J. Biomed. Mater. Res. A 68(4), 704-16 (2004).
80. Kusonwiriyawong C, van de WP, Hubbell JA, Merkle HP, Walter E: Evaluation of pH-dependent membrane-disruptive properties of poly(acrylic acid) derived polymers. Eur J. Pharm. Biopharm. 56(2), 237-246 (2003).
81. Napoli A, Valentini M, Tirelli N, Muller M, Hubbell JA: Oxidation-responsive polymeric vesicles. Nature Materials 3(3), 183-189 (2004).
82. Napoli A, Boerakker MJ, Tirelli N, Nolte RJ, Sommerdijk NA, Hubbell JA: Glucose-oxidase based self-destructing polymeric vesicles. Langmuir 9, 3487-3491 (1920).
83. Shimizu T, Yamato M, Akutsu T et al.: Electrically communicating three-dimensional cardiac tissue mimic fabricated by layered cultured cardiomyocyte sheets. J. Biomed. Mater. Res. 60(1), 110-117 (2002).
84. 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).
85. Shimizu T, Yamato M, Kikuchi A, Okano T: Two-dimensional manipulation of cardiac myocyte sheets utilizing temperature-responsive culture dishes augments the pulsatile amplitude. Tissue Eng. 7(2), 141-151 (2001).
86. Okano T, Yamada N, Okuhara M, Sakai H, Sakurai Y: Mechanism of cell detachment from temperature-modulated, hydrophilic-hydrophobic polymer surfaces. Biomaterials 16(4), 297-303 (1995).
87. Akins RE, Boyce RA, Madonna ML et al.: Cardiac organogenesis in vitro: reestablishment of three-dimensional tissue architecture by dissociated neonatal rat ventricular cells. Tissue Eng. 5(2), 103-118 (1999).
88. Li RK, Yau TM, Weisel RD et al.: Construction of a bioengineered cardiac graft. Ann. Thorac. Cardiovasc. Surg. 119(2), 368-375 (2000).
89. Ozawa T, Mickle DA, Weisel RD et al.: Histologic changes of nonbiodegradable and biodegradable biomaterials used to repair right ventricular heart defects in rats. Ann. Thorac. Cardiovasc. Surg. 124(6), 1157-1164 (2002).
90. Ozawa T, Mickle DA, Weisel RD, Koyama N. Ozawa S, Li RK: Optimal biomaterial for creation of autologous cardiac grafts. Circulation 106(12 Suppi. 1). I176-I182 (2002).
91. Li RK, Jia ZQ, Weisel RD, Mickie DA, Choi A, Yau TM: Survival and function of bioengineered cardiac grafts. Circulation 100(19 Suppl.), I163-I169 (1999).
92. Sakai T, Li RK, Weisel RD et al.: The fate of a tissue-engineered cardiac graft in the right ventricular outflow tract of the rat. Ann. Thorac. Cardiovasc. Surg. 121(5), 932-942 (2001).
93. Leor J, Aboulafta-Etzion S, Dar A et al.: Bioengineered cardiac grafts: a new approach to repair the infarcted myocardium? Circulation 102(19 Suppl. 3), III56-III61 (2000).
94. Dennis RG, Kosnik PE: Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In vitro Cell. Dev. Biol. 36(5), 327-335 (2000).
95. Hecker L, Baar K, Dennis RG, Bitar KN: Development of a three-dimensional physiological model of the internal anal sphincter bioengineered in vitro from isolated smooth muscle cells. Am. J. Physiol. Gastrointest. Liver Physiol. 289(2), G188-G196 (2005).
96. Huang YC, Dennis RG, Larkin L, Baar K: Rapid formation of functional muscle in vitro using fibrin gels. J. Appl. Physiol. 98(2), 706-713 (2005).
97. Kosnik PE, Faulkner JA, Dennis RG: Functional development of engineered skeletal muscle from adult and neonatal rats. Tissue Eng. 7(5), 573-584 (2001).
98. Baar K, Birla R, Boluyt MO. Borschel GH, Arruda EM, Dennis RG: Self-organization of rat cardiac cells into contractile 3-D cardiac tissue. FASEB J. 2, 275-277 (2005).
99. Birla RK, Borschel GH, Dennis RG, Brown DL: Myocardial engineering in vivo: formation and characterization of contractile, vascularized three-dimensional cardiac tissue. Tissue Eng. 1115-6), 803-813 (2005).
100. Birla RK, Borschel GH, Dennis RG: In vivo conditioning of tissue-engineered heart muscle improves contractile performance. Artif Organs 29(11), 866-875 (2005).
101. Portner R, Nagel-Heyer S, Goepfert C, Adamietz P, Meenen NM: Bioreactor design for tissue engineering. J. Biosci. Bioeng. 100(3), 235-245 (2005).
102. Narita Y, Hata K, Kagami H, Usui A, Ueda M, Ueda Y: Novel pulse duplicating bioreactor system for tissue-engineered vascular construct. Tissue Eng. 10(7-8), 1224-1233 (2004).
103. Niklason LE, Gao J, Abbott WM et al.: Functional arteries gown in vitro. Science 284(5413), 489-493 (1999).
104. Sodian R, Lemke T, Fritsche C et al.: Tissue-engineering bioreactors: a new combined cell-seeding and perfusion system for vascular tissue engineering. Tissue Eng. 8(5), 863-870 (2002).
105. Solan A, Mitchell S, Moses M, Niklason L: Effect of pulse rate on collagen deposition in the tissue-engineered blood vessel. Tissue Eng. 9(4), 579-586 (2003).
106. Williams C, Wick TM: Perfusion bioreactor for small diameter tissue-engineered arteries. Tissue Eng. 10(5-6), 930-941 (2004).
107. Engelmayr GC Jr, Hildebrand DK, Sutherland FW, Mayer JE Jr, Sacks MS: A novel bioreactor for the dynamic flexural stimulation of tissue engineered heart valve biomaterials. Biomaterials 24(14), 2523-2532 (2003).
108. Hoerstrup SP, Sodian R, Daebritz S et al.: Functional living trileaflet heart valves grown in vitro Circulation 102(19 Suppl. 3), III44-III49 (2000).
109. Hoerstrup SP, Sodian R, Sperling JS, Vacanti JP, Mayer JE Jr: New pulsatile bioreactor for in vitro formation of tissue engineered heart valves. Tissue Eng. 6(1), 75-79 (2000).
110. Dumont K, Yperman J, Verbeken E et al.: Design of a new pulsatile bioreactor for tissue engineered aortic heart valve formation. Artif Organs 26(8), 710-714 (2002).
111. Engelmayr GC Jr, Hildebrand DK, Sutherland FW, Mayer JE Jr, Sacks MS: A novel bioreactor for the dynamic flexural stimulation of tissue engineered heart valve biormaterials. Biomaterials 24(14). 2523-2532 (2003).
112. Mol A, Driessen NJ, Rutten MC, Hoerstrup SP, Bouten CV, Baaijens FP: Tissue engineering of human heart valve leaflets: a novel bioreactor for a strain-based conditioning approach. Ann. Biomed. Eng. 33(12), 1778-1788 (2005).
113. Akhyari P, Fedak PW, Weisel RD et al.: Mechanical stretch regimen enhances the formation of bioengineered autologous cardiac muscle grafts. Circulation 106(12 Suppl. 1), I137-I142 (2002).
114. Carrier RL, Rupnick M, Langer R, Schoen FJ, Freed LE, Vunjak-Novakovic G: Perfusion improves tissue architecture of engineered cardiac muscle. Tissue Eng. 8(2), 175-488 (2002).
115. Fink C, Ergun S, Kralisch D, Remmers U, Weil J, Eschenhagen T: Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J. 14(5), 669-679 (2000).
116. Bottaro DP, Liebmann-Vinson A, Heidaran MA: Molecular signaling in bioengineered tissue microenvironments. Ann. N. Y. Acad. Sci. 961, 143-153 (2002).
117. Abbott A: Cell culture: biology's new dimension. Nature 424(6951), 870-872 (2003).
118. Engler AJ, Sen S, Sweeney HL, Discher DE: Matrix elasticity directs stem cell lineage specification. Cell 126(4), 677-689 (2006).
119. Zisch AH, Lutolf MP, Hubbell JA: Biopolymeric delivery matrices for angiogenic growth factors. Cardivas. Pathol. 12(6), 295-310 (2003).
120. Sakiyama-Elbert SE, Panitch A, Hubbell JA: Development of growth factor fusion proteins for cell-triggered drug delivery. FASEB J. 15(1), 1300-1302 (2001).
121. Zisch AH, Schenk U, Schense JC, Sakiyama-Elbert SE, Hubbell JA: Covalently conjugated VEGF - fibrin matrices for endothetialization. J. Control. Release 72(1-3), 101-113 (2001).