Cardiac tissue engineering: Current state and perspectives

Frontiers in Bioscience

Volumn 17, Issue 4, 2012, Pages 1533-1550

  Chiu, Loraine L Y ^a   Iyer, Rohin K ^b   Reis, Lewis A ^b   Nunes, Sara S ^b,c   Radisic, Milica ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Bioreactors; Cardiac tissue engineering; Review; Scaffolds; Vascularization

Indexed keywords

ANIMAL; ARTICLE; BIOREACTOR; CYTOLOGY; HEART MUSCLE; HUMAN; STEM CELL; TISSUE ENGINEERING;

ANIMALS; BIOREACTORS; HUMANS; MYOCARDIUM; STEM CELLS; TISSUE ENGINEERING;

EID: 84859220157     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4002     Document Type: Review

References (143)

1. WH Zimmermann, I Melnychenko, T Eschenhagen, Engineered heart tissue for regeneration of diseased hearts. Biomaterials 25, 1639-1647 (2004). (Pubitemid 38091542)
2. M Radisic, H Park, H Shing, T Consi, FJ Schoen, R Langer, LE Freed, G Vunjak-Novakovic, Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci U S A 101, 18129-18134 (2004). (Pubitemid 40054085)
3. J Leor, S Aboulafia-Etzion, A Dar, L Shapiro, IM Barbash, A Battler, Y Granot, S Cohen, Bioengineered cardiac grafts: A new approach to repair the infarcted myocardium? Circulation 102, III56-III61 (2000).
4. F Rask, SM Dallabrida, NS Ismail, Z Amoozgar, Y Yeo, MA Rupnick, M Radisic, Photocrosslinkable chitosan modified with angiopoietin-1 peptide, QHREDGS, promotes survival of neonatal rat heart cells. J Biomed Mater Res A 95, 105-117 (2010).
5. Y Yeo, W Geng, T Ito, DS Kohane, JA Burdick, M Radisic, Photocrosslinkable hydrogel for myocyte cell culture and injection. J Biomed Mater Res B Appl Biomater 81, 312-322 (2007). (Pubitemid 46685097)
6. N Bursac, M Papadaki, JA White, SR Eisenberg, G Vunjak-Novakovic, LE Freed, Cultivation in rotating bioreactors promotes maintenance of cardiac myocyte electrophysiology and molecular properties. Tissue Eng 9, 1243-1253 (2003). (Pubitemid 37467672)
7. GC Engelmayr Jr., M Cheng, CJ Bettinger, JT Borenstein, R Langer, LE Freed, Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat Mater 7, 1003-1010 (2008).
8. M Radisic, H Park, F Chen, JE Salazar-Lazzaro, Y Wang, R Dennis, R Langer, LE Freed, G Vunjak- Novakovic, Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng 12, 2077-2091 (2006). (Pubitemid 44734968)
9. X Zong, H Bien, CY Chung, L Yin, D Fang, BS Hsiao, B Chu, E Entcheva, Electrospun fine-textured scaffolds for heart tissue constructs. Biomaterials 26, 5330-5338 (2005). (Pubitemid 40462348)
10. M Radisic, L Yang, J Boublik, RJ Cohen, R Langer, LE Freed, G Vunjak-Novakovic, Medium perfusion enables engineering of compact and contractile cardiac tissue. Am J Physiol Heart Circ Physiol 286, H507-516 (2004). (Pubitemid 38140330)
11. WH Zimmermann, K Schneiderbanger, P Schubert, M Didie, F Munzel, JF Heubach, S Kostin, WL Nehuber, T Eschenhagen, Tissue engineering of a differentiated cardiac muscle construct. Circulation Research 90, 223-230 (2002). (Pubitemid 34627092)
12. MH Soonpaa, LJ Field, Survey of studies examining mammalian cardiomyocyte DNA synthesis. Circulation Research 83, 15-26 (1998). (Pubitemid 28322095)
13. KL Laugwitz, A Moretti, J Lam, P Gruber, Y Chen, S Woodard, LZ Lin, CL Cai, MM Lu, M Reth, O Platoshyn, JX Yuan, S Evans, KR Chien, Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433, 647-653 (2005). (Pubitemid 40282999)
14. A Moretti, L Caron, A Nakano, JT Lam, A Bernshausen, Y Chen, Y Qyang, L Bu, M Sasaki, S Martin- Puig, Y Sun, SM Evans, KL Laugwitz, KR Chien, Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127, 1151-1165 (2006). (Pubitemid 44895618)
15. RR Smith, L Barile, HC Cho, MK Leppo, JM Hare, E Messina, A Giacomello, MR Abraham, E Marban, Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115, 896-908 (2007). (Pubitemid 46294730)
16. H Oh, SB Bradfute, TD Gallardo, T Nakamura, V Gaussin, Y Mishina, J Pocius, LH Michael, RR Behringer, DJ Garry, ML Entman, MD Schneider, Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100, 12313-12318 (2003). (Pubitemid 37271557)
17. AP Beltrami, L Barlucchi, D Torella, M Baker, F Limana, S Chimenti, H Kasahara, M Rota, E Musso, K Urbanek, A Leri, J Kajstura, B Nadal-Ginard, P Anversa, Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114, 763-776 (2003). (Pubitemid 37186770)
18. IJ Domian, M Chiravuri, P van der Meer, AW Feinberg, X Shi, Y Shao, SM Wu, KK Parker, KR Chien, Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science 326, 426-429 (2009).
19. XM Guo, YS Zhao, HX Chang, CY Wang, LL E, XA Zhang, CM Duan, LZ Dong, H Jiang, J Li, Y Song, XJ Yang, Creation of engineered cardiac tissue in vitro from mouse embryonic stem cells. Circulation 113, 2229-2237 (2006).
20. A Lesman, L Gepstein, S Levenberg, Vascularization shaping the heart. Ann N Y Acad Sci 1188, 46-51 (2010).
21. O Caspi, A Lesman, Y Basevitch, A Gepstein, G Arbel, IH Habib, L Gepstein, S Levenberg, Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 100, 263-272 (2007). (Pubitemid 46208727)
22. A Lesman, M Habib, O Caspi, A Gepstein, G Arbel, S Levenberg, L Gepstein, Transplantation of a tissueengineered human vascularized cardiac muscle. Tissue Eng Part A 16, 115-125 (2010).
23. KR Stevens, L Pabon, V Muskheli, CE Murry, Scaffold-free human cardiac tissue patch created from embryonic stem cells. Tissue Eng Part A 15, 1211-1222 (2009).
24. KR Stevens, KL Kreutziger, SK Dupras, FS Korte, M Regnier, V Muskheli, MB Nourse, K Bendixen, H Reinecke, CE Murry, Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc Natl Acad Sci U S A 106, 16568-16573 (2009).
25. H Song, C Yoon, SJ Kattman, J Dengler, S Masse, T Thavaratnam, M Gewarges, K Nanthakumar, M Rubart, GM Keller, M Radisic, PW Zandstra, Interrogating functional integration between injected pluripotent stem cell-derived cells and surrogate cardiac tissue. Proc Natl Acad Sci U S A 107, 3329-3334 (2010).
26. RK Iyer, J Chui, M Radisic, Spatiotemporal tracking of cells in tissue-engineered cardiac organoids. J Tissue Eng Regen Med 3, 196-207 (2009).
27. KA Jackson, SM Majka, H Wang, J Pocius, CJ Hartley, MW Majesky, ML Entman, LH Michael, KK Hirschi, MA Goodell, Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107, 1395-1402 (2001). (Pubitemid 32522033)
28. A Deb, S Wang, KA Skelding, D Miller, D Simper, NM Caplice, Bone marrow-derived cardiomyocytes are present in adult human heart: A study of gendermismatched bone marrow transplantation patients. Circulation 107, 1247-1249 (2003). (Pubitemid 36314405)
29. D Orlic, J Kajstura, S Chimenti, DM Bodine, A Leri, P Anversa, Bone marrow stem cells regenerate infarcted myocardium. Pediatr Transplant 7 Suppl 3, 86-88 (2003). (Pubitemid 36314227)
30. D Orlic, J Kajstura, S Chimenti, F Limana, I Jakoniuk, F Quaini, B Nadal-Ginard, DM Bodine, A Leri, P Anversa, Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A 98, 10344-10349 (2001). (Pubitemid 32803022)
31. H Jawad, NN Ali, AR Lyon, QZ Chen, SE Harding, AR Boccaccini, Myocardial tissue engineering: a review. J Tissue Eng Regen Med 1, 327-342 (2007).
32. E Messina, L De Angelis, G Frati, S Morrone, S Chimenti, F Fiordaliso, M Salio, M Battaglia, MV Latronico, M Coletta, E Vivarelli, L Frati, G Cossu, A Giacomello, Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95, 911-921 (2004). (Pubitemid 39435006)
33. PV Johnston, T Sasano, K Mills, R Evers, ST Lee, RR Smith, AC Lardo, S Lai, C Steenbergen, G Gerstenblith, R Lange, E Marban, Engraftment, differentiation, and functional benefits of autologous cardiosphere-derived cells in porcine ischemic cardiomyopathy. Circulation. 120, 1075-1083, 7 p following 1083 (2009).
34. I Chimenti, RR Smith, TS Li, G Gerstenblith, E Messina, A Giacomello, E Marban, Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res 106, 971-980 (2010).
35. K Cheng, TS Li, K Malliaras, DR Davis, Y Zhang, E Marban, Magnetic targeting enhances engraftment and functional benefit of iron-labeled cardiosphere-derived cells in myocardial infarction. Circ Res 106, 1570-1581 (2010).
36. JK Fraser, I Wulur, Z Alfonso, MH Hedrick, Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24, 150-154 (2006).
37. X Bai, E Alt, Myocardial regeneration potential of adipose tissue-derived stem cells. Biochem Biophys Res Commun 401, 321-326 (2010).
38. X Bai, Y Yan, YH Song, M Seidensticker, B Rabinovich, R Metzele, JA Bankson, D Vykoukal, E Alt, Both cultured and freshly isolated adipose tissue-derived stem cells enhance cardiac function after acute myocardial infarction. Eur Heart J 31, 489-501 (2009).
39. R Gaebel, D Furlani, H Sorg, B Polchow, J Frank, K Bieback, W Wang, C Klopsch, LL Ong, W Li, N Ma, G Steinhoff, Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration. PLoS One 6, e15652 (2011).
40. M Patel, JP Fisher, Biomaterial scaffolds in pediatric tissue engineering. Pediatr Res 63, 497-501 (2008). (Pubitemid 351572219)
41. J Leor, S Aboulafia-Etzion, A Dar, L Shapiro, IM Barbash, A Battler, Y Granot, S Cohen, Bioengineered cardiac grafts: A new approach to repair the infarcted myocardium? Circulation 102, III56-61 (2000).
42. M Shachar, O Tsur-Gang, T Dvir, J Leor, S Cohen, The effect of immobilized RGD peptide in alginate scaffolds on cardiac tissue engineering. Acta Biomater 7, 152-162 (2011).
43. E Rosellini, C Cristallini, N Barbani, G Vozzi, P Giusti, Preparation and characterization of alginate/gelatin blend films for cardiac tissue engineering. J Biomed Mater Res A 91, 447-453 (2009).
44. A Dar, M Shachar, J Leor, S Cohen, Optimization of cardiac cell seeding and distribution in 3D porous alginate scaffolds. Biotechnol Bioeng 80, 305-312 (2002). (Pubitemid 35221629)
45. C Deng, P Zhang, B Vulesevic, D Kuraitis, F Li, AF Yang, M Griffith, M Ruel, EJ Suuronen, A Collagen- Chitosan Hydrogel for Endothelial Differentiation and Angiogenesis. Tissue Eng Part A 16, 3099-3109 (2010).
46. NR Blan, RK Birla, Design and fabrication of heart muscle using scaffold-based tissue engineering. J Biomed Mater Res A 86, 195-208 (2008). (Pubitemid 351799500)
47. T Eschenhagen, C Fink, U Remmers, H Scholz, J Wattchow, J Weil, W Zimmermann, HH Dohmen, H Schafer, N Bishopric, T Wakatsuki, EL Elson, Threedimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J 11, 683-694 (1997). (Pubitemid 27318285)
48. H Park, M Radisic, JO Lim, BH Chang, G Vunjak-Novakovic, A novel composite scaffold for cardiac tissue engineering. In vitro Cell Dev Biol Anim 41, 188-196 (2005). (Pubitemid 41504522)
49. M Radisic, M Euloth, L Yang, R Langer, LE Freed, G Vunjak-Novakovic, High-density seeding of myocyte cells for cardiac tissue engineering. Biotechnol Bioeng 82, 403- 414 (2003). (Pubitemid 36505879)
50. TC Flanagan, B Wilkins, A Black, S Jockenhoevel, TJ Smith, AS Pandit, A collagen-glycosaminoglycan coculture model for heart valve tissue engineering applications. Biomaterials 27, 2233-2246 (2006). (Pubitemid 41774535)
51. V Chekanov, M Akhtar, G Tchekanov, G Dangas, MZ Shehzad, F Tio, M Adamian, A Colombo, G Roubin, MB Leon, JW Moses, NN Kipshidze, Transplantation of autologous endothelial cells induces angiogenesis. Pacing Clin Electrophysiol 26, 496-499 (2003). (Pubitemid 36399203)
52. KL Christman, AJ Vardanian, Q Fang, RE Sievers, HH Fok, RJ Lee, Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J Am Coll Cardiol 44, 654-660 (2004). (Pubitemid 39089073)
53. JH Ryu, IK Kim, SW Cho, MC Cho, KK Hwang, H Piao, S Piao, SH Lim, YS Hong, CY Choi, KJ Yoo, BS Kim, Implantation of bone marrow mononuclear cells using injectable fibrin matrix enhances neovascularization in infarcted myocardium. Biomaterials 26, 319-326 (2005). (Pubitemid 38950716)
54. W Bian, B Liau, N Badie, N Bursac, Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues. Nat Protoc 4, 1522-1534 (2009).
55. W Bian, N Bursac, Engineered skeletal muscle tissue networks with controllable architecture. Biomaterials 30, 1401-1412 (2009).
56. LD Black 3rd, JD Meyers, JS Weinbaum, YA Shvelidze, RT Tranquillo, Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. Tissue Eng Part A 15, 3099-3108 (2009).
57. RK Li, ZQ Jia, RD Weisel, DA Mickle, A Choi, TM Yau, Survival and function of bioengineered cardiac grafts. Circulation 100, II63-69 (1999). (Pubitemid 29523511)
58. M Li, Y Guo, Y Wei, AG MacDiarmid, PI Lelkes, Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications. Biomaterials 27, 2705- 2715 (2006). (Pubitemid 43122074)
59. Z Xiang, R Liao, MS Kelly, M Spector, Collagen-GAG scaffolds grafted onto myocardial infarcts in a rat model: a delivery vehicle for mesenchymal stem cells. Tissue Eng 12, 2467-2478 (2006). (Pubitemid 46141270)
60. H Jawad, AR Lyon, SE Harding, NN Ali, AR Boccaccini, Myocardial tissue engineering. Br Med Bull 87, 31-47 (2008).
61. DN Rockwood, RE Akins Jr., IC Parrag, KA Woodhouse, JF Rabolt, Culture on electrospun polyurethane scaffolds decreases atrial natriuretic peptide expression by cardiomyocytes in vitro. Biomaterials 29, 4783-4791 (2008).
62. RG Heijkants, RV van Calck, TG van Tienen, JH de Groot, AJ Pennings, P Buma, RP Veth, AJ Schouten, Polyurethane scaffold formation via a combination of salt leaching and thermally induced phase separation. J Biomed Mater Res A 87, 921-932 (2008).
63. HJ Chun, GW Kim, CH Kim, Fabrication of porous chitosan scaffold in order to improve biocompatibility. Journal of Physics and Chemistry of Solids 69, 1573-1576 (2008).
64. RK. Li, ZQ Jia, RD Weisel, DAG Mickle, A Choi, TM Yau, Survival and function of bioengineered cardiac grafts. Circulation 100, II63-II69 (1999). (Pubitemid 29523511)
65. T Kofidis, P Akhyari, B Wachsmann, K Mueller-Stahl, J Boublik, A Ruhparwar, H Mertsching, L Balsam, R Robbins, A Haverich, Clinically established hemostatic scaffold (tissue fleece) as biomatrix in tissue- and organengineering research. Tissue Engineering 9, 517-523 (2003). (Pubitemid 36736134)
66. HC Ott, TS Matthiesen, SK Goh, LD Black, SM Kren, TI Netoff, DA Taylor, Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 14, 213-221 (2008). (Pubitemid 351214548)
67. SF Badylak, PV Kochupura, IS Cohen, SV Doronin, AE Saltman, TW Gilbert, DJ Kelly, RA Ignotz, GR Gaudette, The use of extracellular matrix as an inductive scaffold for the partial replacement of functional myocardium. Cell Transplant 15 Suppl 1, S29-S40 (2006).
68. JA DeQuach, V Mezzano, A Miglani, S Lange, GM Keller, F Sheikh, KL Christman, Simple and high yielding method for preparing tissue specific extracellular matrix coatings for cell culture. PLoS One 5, e13039 (2010).
69. PV Kochupura, EU Azeloglu, DJ Kelly, SV Doronin, SF Badylak, IB Krukenkamp, IS Cohen, GR Gaudette, Tissue-engineered myocardial patch derived from extracellular matrix provides regional mechanical function. Circulation 112, I144-149 (2005). (Pubitemid 41266666)
70. M Di Donato, M Sabatier, V Dor, GF Gensini, A Toso, M Maioli, AWH Stanley, C Athanasuleas, G Buckberg, Effects of the Dor procedure on left ventricular dimension and shape and geometric correlates of mitral regurgitation one year after surgery. Journal of Thoracic and Cardiovascular Surgery 121, 91-96 (2001). (Pubitemid 32105328)
71. J.M. Wainwright, C.A. Czajka, U.B. Patel, D.O. Freytes, K. Tobita, T.W. Gilbert, S.F. Badylak, Preparation of cardiac extracellular matrix from an intact porcine heart, Tissue Eng Part C Methods. 16 (2010) 525-532.
72. DA Taylor, From stem cells and cadaveric matrix to engineered organs. Curr Opin Biotechnol 20, 598-605 (2009).
73. A Furuta, S Miyoshi, Y Itabashi, T Shimizu, S Kira, K Hayakawa, N Nishiyama, K Tanimoto, Y Hagiwara, T Satoh, K Fukuda, T Okano, S Ogawa, Pulsatile cardiac tissue grafts using a novel three-dimensional cell sheet manipulation technique functionally integrates with the host heart, in vivo. Circ Res 98, 705-712 (2006).
74. S Miyagawa, Y Sawa, S Sakakida, S Taketani, H Kondoh, IA Memon, Y Imanishi, T Shimizu, T Okano, H Matsuda, Tissue Cardiomyoplasty Using Bioengineered Contractile Cardiomyocyte Sheets to Repair Damaged Myocardium: Their Integration with Recipient Myocardium. Transplantation 80, 1586-1595 (2005). (Pubitemid 43005870)
75. IA Memon, Y Sawa, N Fukushima, G Matsumiya, S Miyagawa, S Taketani, SK Sakakida, H Kondoh, AN Aleshin, T Shimizu, T Okano, H Matsuda, Repair of impaired myocardium by means of implantation of engineered autologous myoblast sheets. J Thorac Cardiovasc Surg 130, 1333-1341 (2005). (Pubitemid 41543202)
76. T Shimizu, H Sekine, J Yang, Y Isoi, M Yamato, A Kikuchi, E Kobayashi, T Okano, Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. Faseb J 20, 708-710 (2006). (Pubitemid 46671189)
77. A Bel, V Planat-Bernard, A Saito, L Bonnevie, V Bellamy, L Sabbah, L Bellabas, B Brinon, V Vanneaux, P Pradeau, S Peyrard, J Larghero, J Pouly, P Binder, S Garcia, T Shimizu, Y Sawa, T Okano, P Bruneval, M Desnos, AA Hagège, L Casteilla, M Pucéat, P Menasché, Composite cell sheets: a further step toward safe and effective myocardial regeneration by cardiac progenitors derived from embryonic stem cells. Circulation 122, S118- 123 (2010).
78. K Matsuura, A Honda, T Nagai, N Fukushima, K Iwanaga, M Tokunaga, T Shimizu, T Okano, H Kasanuki, N Hagiwara, I Komuro, Transplantation of cardiac progenitor cells ameliorates cardiac dysfunction after myocardial infarction in mice. The Journal of clinical investigation 119, 2204-2217 (2009).
79. Y Sawa, (Myocardial regeneration for heart failure) Nippon Rinsho 68, 719-725 (2010).
80. M Radisic, J Malda, E Epping, W Geng, R Langer, G Vunjak-Novakovic, Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol Bioeng 93, 332-343 (2006).
81. M Radisic, W Deen, R Langer, G Vunjak-Novakovic, Mathematical model of oxygen distribution in engineered cardiac tissue with parallel channel array perfused with culture medium containing oxygen carriers. Am J Physiol Heart Circ Physiol 288, H1278-1289 (2005). (Pubitemid 40270035)
82. Y Barash, T Dvir, P Tandeitnik, E Ruvinov, H Guterman, S Cohen, Electric Field Stimulation Integrated into Perfusion Bioreactor for Cardiac Tissue Engineering. Tissue Eng Part C Methods 16, 1417-1426 (2010).
83. MA Brown, RK Iyer, M Radisic, Pulsatile perfusion bioreactor for cardiac tissue engineering. Biotechnol Prog 24, 907-920 (2008).
84. T Dvir, O Levy, M Shachar, Y Granot, S Cohen, Activation of the ERK1/2 cascade via pulsatile interstitial fluid flow promotes cardiac tissue assembly. Tissue Eng 13, 2185-2193 (2007). (Pubitemid 47404434)
85. T Eschenhagen, C Fink, U Remmers, H Scholz, J Wattchow, J Weil, WH Zimmermann, HH Dohmen, H Schäfer, N Bishopric, T Wakatsuki, EL Elson, Threedimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. The FASEB journal 11, 683-694 (1997). (Pubitemid 27318285)
86. WH Zimmermann, C Fink, D Kralish, U Remmers, J Weil, T Eschenhagen, Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnology and Bioengineering 68, 106-114 (2000). (Pubitemid 30163499)
87. WH Zimmermann, I Melnychenko, G Wasmeier, M Didié, H Naito, U Nixdorff, A Hess, L Budinsky, K Brune, B Michaelis, S Dhein, A Schwoerer, H Ehmke, T Eschenhagen, Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nature medicine 12, 452-458 (2006).
88. N Tandon, C Cannizzaro, PHG Chao, R Maidhof, A Marsano, HTH Au, M Radisic, G Vunjak-Novakovic, Electrical stimulation systems for cardiac tissue engineering. Nature protocols 4, 155-173 (2009).
89. LL Chiu, RK Iyer, JP King, M Radisic, Biphasic Electrical Field Stimulation Aids in Tissue Engineering of Multicell-Type Cardiac Organoids. Tissue Eng Part A 17, 1465-1477 (2011).
90. DH Kim, EA Lipke, P Kim, R Cheong, S Thompson, M Delannoy, KY Suh, L Tung, A Levchenko, Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs. Proc Natl Acad Sci U S A 107, 565-570 (2010).
91. HT Au, I Cheng, MF Chowdhury, M Radisic, Interactive effects of surface topography and pulsatile electrical field stimulation on orientation and elongation of fibroblasts and cardiomyocytes. Biomaterials 28, 4277- 4293 (2007). (Pubitemid 47212400)
92. H Au, B Cui, Z Chu, T Veres, M Radisic, Cell culture chips for simultaneous application of topographical and electrical cues enhance phenotype of cardiomyocytes. Lab Chip 9, 564-575 (2009).
93. E Cimetta, S Pizzato, S Bollini, E Serena, P De Coppi, N Elvassore, Production of arrays of cardiac and skeletal muscle myofibers by micropatterning techniques on a soft substrate. Biomed Microdevices 11, 389-400 (2009).
94. N Badie, N Bursac, Novel micropatterned cardiac cell cultures with realistic ventricular microstructure. Biophys J 96, 3873-3885 (2009).
95. CY Chung, H Bien, EA Sobie, V Dasari, D McKinnon, B Rosati, E Entcheva, Hypertrophic phenotype in cardiac cell assemblies solely by structural cues and ensuing selforganization. FASEB J 25, 851-862 (2011).
96. MR Badrossamay, HA McIlwee, JA Goss, KK Parker, Nanofiber assembly by rotary jet-spinning. Nano Lett 10, 2257-2261 (2010).
97. PW Alford, AW Feinberg, SP Sheehy, KK Parker, Biohybrid thin films for measuring contractility in engineered cardiovascular muscle. Biomaterials 31, 3613- 3621 (2010).
98. AW Feinberg, A Feigel, SS Shevkoplyas, S Sheehy, GM Whitesides, KK Parker, Muscular thin films for building actuators and powering devices. Science 317, 1366-1370 (2007). (Pubitemid 47417472)
99. MR Badrossamay, HA McIlwee, JA Goss, KK Parker, Nanofiber assembly by rotary jet-spinning. Nano Lett 10, 2257-2261 (2010).
100. Z Liu, JL Tan, DM Cohen, MT Yang, NJ Sniadecki, SA Ruiz, CM Nelson, CS Chen, Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci U S A 107, 9944-9949 (2010).
101. WR Legant, A Pathak, MT Yang, VS Deshpande, RM McMeeking, CS Chen, Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues. Proc Natl Acad Sci U S A 106, 10097-10102 (2009).
102. YC Huang, L Khait, RK Birla, Contractile threedimensional bioengineered heart muscle for myocardial regeneration. J Biomed Mater Res A 80, 719-731 (2007). (Pubitemid 46239085)
103. HTH Au, B Cui, ZE Chu, T Veres, M Radisic, Cell culture chips for simultaneous application of topographical and electrical cues enhance phenotype of cardiomyocytes. Lab on a Chip. 9, 564-575 (2009).
104. CY Tay, H Yu, M Pal, WS Leong, NS Tan, KW Ng, DT Leong, LP Tan, Micropatterned matrix directs differentiation of human mesenchymal stem cells towards myocardial lineage. Experimental Cell Research 316, 1159- 1168 (2010).
105. D Sasaki, T Shimizu, S Masuda, J Kobayashi, K Itoga, Y Tsuda, JK Yamashita, M Yamato, T Okano, Mass preparation of size-controlled mouse embryonic stem cell aggregates and induction of cardiac differentiation by cell patterning method. Biomaterials 30, 4384-4389 (2009).
106. B Korecky, CM Hai, K Rakusan, Functional capillary density in normal and transplanted rat hearts. Canadian Journal of Physiology and Pharmacology 60, 23-32 (1982). (Pubitemid 12184128)
107. H Naito, I Melnychenko, M Didie, K Schneiderbanger, P Schubert, S Rosenkranz, T Eschenhagen, WH Zimmermann, Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114, I72-78 (2006). (Pubitemid 44297132)
108. RK Iyer, LL Chiu, M Radisic, Microfabricated poly (ethylene glycol) templates enable rapid screening of triculture conditions for cardiac tissue engineering. J Biomed Mater Res A 89, 616-631 (2009).
109. N Asakawa, T Shimizu, Y Tsuda, S Sekiya, T Sasagawa, M Yamato, F Fukai, T Okano, Pre-vascularization of in vitro three-dimensional tissues created by cell sheet engineering. Biomaterials 31, 3903-3909 (2010).
110. T Sasagawa, T Shimizu, S Sekiya, Y Haraguchi, M Yamato, Y Sawa, T Okano, Design of prevascularized threedimensional cell-dense tissues using a cell sheet stacking manipulation technology. Biomaterials 31, 1646-1654 (2010).
111. H Sekine, T Shimizu, K Hobo, S Sekiya, J Yang, M Yamato, H Kurosawa, E Kobayashi, T Okano, Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 118, S145-S152 (2008).
112. LR Madden, DJ Mortisen, EM Sussman, SK Dupras, JA Fugate, JL Cuy, KD Hauch, MA Laflamme, CE Murry, BD Ratner, Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc Natl Acad Sci U S A 107, 15211-15216 (2010).
113. S Raghavan, CM Nelson, JD Baranski, E Lim, CS Chen, Geometrically controlled endothelial tubulogenesis in micropatterned gels. Tissue Eng Part A 16, 2255-2263 (2010).
114. CJ Bettinger, Z Zhang, S Gerecht, JT Borenstein, R Langer, Enhancement of In vitro Capillary Tube Formation by Substrate Nanotopography. Adv Mater 20, 99-103 (2008). (Pubitemid 351143301)
115. EC Martinez, J Wang, SU Gan, R Singh, CN Lee, T Kofidis, Ascorbic acid improves embryonic cardiomyoblast cell survival and promotes vascularization in potential myocardial grafts in vivo. Tissue Eng Part A 16, 1349-1361 (2010).
116. J Saif, TM Schwarz, DY Chau, J Henstock, P Sami, SF Leicht, PC Hermann, S Alcala, F Mulero, KM Shakesheff, C Heeschen, A Aicher, Combination of injectable multiple growth factor-releasing scaffolds and cell therapy as an advanced modality to enhance tissue neovascularization. Arterioscler Thromb Vasc Biol 30, 1897-1904 (2010).
117. SM Jay, BR Shepherd, JW Andrejecsk, TR Kyriakides, JS Pober, WM Saltzman, Dual delivery of VEGF and MCP-1 to support endothelial cell transplantation for therapeutic vascularization. Biomaterials 31, 3054-3062 (2010).
118. N Smart, CA Risebro, JE Clark, E Ehler, L Miquerol, A Rossdeutsch, MS Marber, PR Riley, Thymosin beta4 facilitates epicardial neovascularization of the injured adult heart. Ann N Y Acad Sci 1194, 97-104 (2010).
119. BD Westenbrink, WP Ruifrok, AA Voors, RG Tilton, DJ van Veldhuisen, RG Schoemaker, WH van Gilst, RA de Boer, Vascular endothelial growth factor is crucial for erythropoietin-induced improvement of cardiac function in heart failure. Cardiovasc Res 87, 30-39 (2010).
120. J Zhang, L Ding, Y Zhao, W Sun, B Chen, H Lin, X Wang, L Zhang, B Xu, J Dai, Collagen-targeting vascular endothelial growth factor improves cardiac performance after myocardial infarction. Circulation 119, 1776-1784 (2009).
121. LL Chiu, M Radisic, Scaffolds with covalently immobilized VEGF and Angiopoietin-1 for vascularization of engineered tissues. Biomaterials 31, 226-241 (2010).
122. LL Chiu, RD Weisel, RK Li, M Radisic, Defining conditions for covalent immobilization of angiogenic growth factors onto scaffolds for tissue engineering. J Tissue Eng Regen Med 5, 69-84 (2011).
123. Y Miyagi, LL Chiu, M Cimini, RD Weisel, M Radisic, RK Li, Biodegradable collagen patch with covalently immobilized VEGF for myocardial repair. Biomaterials 32, 1280-1290 (2011).
124. T Dvir, A Kedem, E Ruvinov, O Levy, I Freeman, N Landa, R Holbova, MS Feinberg, S Dror, Y Etzion, J Leor, S Cohen, Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc Natl Acad Sci U S A 106, 14990-14995 (2009).
125. AN Morritt, SK Bortolotto, RJ Dilley, X Han, AR Kompa, D McCombe, CE Wright, S Itescu, JA Angus, WA Morrison, Cardiac tissue engineering in an in vivo vascularized chamber. Circulation 115, 353-360 (2007). (Pubitemid 46148509)
126. YS Choi, K Matsuda, GJ Dusting, WA Morrison, RJ Dilley, Engineering cardiac tissue in vivo from human adipose-derived stem cells. Biomaterials 31, 2236-2242 (2010).
127. DJ Tilkorn, A Bedogni, E Keramidaris, X Han, JA Palmer, AM Dingle, BS Cowling, MD Williams, SM McKay, L Pepe, A Deftereos, WA Morrison, AJ Penington, GM Mitchell, Implanted myoblast survival is dependent on the degree of vascularization in a novel delayed implantation/prevascularization tissue engineering model. Tissue Eng Part A 16, 165-178 (2010).
128. A Hansen, A Eder, M Bönstrup, M Flato, M Mewe, S Schaaf, B Aksehirlioglu, A Schwörer, J Uebeler, T Eschenhagen, Development of a Drug Screening Platform Based on Engineered Heart Tissue. Circulation research 107, 35-44 (2010).
129. S Etzion, A Battler, IM Barbash, E Cagnano, P Zarin, Y Granot, LH Kedes, RA Kloner, J Leor, Influence of embryonic cardiomyocyte transplantation on the progression of heart failure in a rat model of extensive myocardial infarction. J Mol Cell Cardiol 33, 1321-1330 (2001). (Pubitemid 32613424)
130. MH Soonpaa, GY Koh, MG Klug, LJ Field, Formation of nascent intercalated disks between grafted fetal cardiomyocytes and host myocardium. Science 264, 98-101 (1994). (Pubitemid 24144494)
131. RK Li, ZQ Jia, MH Weisel, DA Mickel, J Zhang, MK Mohabeer, V Rao, J Ivanov, Cardiomyocyte transplantation improved heart function. Annals of Thoracic Surgery 62, 654-660 (1996).
132. J Muller-Ehmsen, KL Peterson, L Kedes, P Whittaker, JS Dow, TI Long, PW Laird, RA Kloner, Rebuilding a damaged heart: long-term survival of transplanted neonatal rat cardiomyocytes after myocardial infarction and effect on cardiac function. Circulation 105, 1720-1726 (2002). (Pubitemid 34298618)
133. H Reinecke, M Zhang, T Bartosek, CE Murry, Survival, integration, and differentiation of cardiomyocyte grafts: a study in normal and injured rat hearts. Circulation 100, 193-202 (1999). (Pubitemid 29330019)
134. H Huwer, J Winning, B Vollmar, C Welter, C Lohbach, MD Menger, HJ Schafers, Long-term cell survival and hemodynamic improvements after neonatal cardiomyocyte and satellite cell transplantation into healed myocardial cryoinfarcted lesions in rats. Cell Transplant 12, 757-767 (2003). (Pubitemid 37409743)
135. P Menasche, AA Hagege, M Scorsin, B Pouzet, M Desnos, D Duboc, K Schwartz, JT Vilquin, JP Marolleau, Myoblast transplantation for heart failure. Lancet 357, 279-280 (2001). (Pubitemid 32120862)
136. LB Balsam, AJ Wagers, JL Christensen, T Kofidis, IL Weissman, RC Robbins, Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428, 668-673 (2004). (Pubitemid 38524811)
137. CE Murry, MH Soonpaa, H Reinecke, H Nakajima, HO Nakajima, M Rubart, KB Pasumarthi, JI Virag, SH Bartelmez, V Poppa, G Bradford, JD Dowell, DA Williams, LJ Field, Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428, 664-668 (2004). (Pubitemid 38524810)
138. JG Shake, PJ Gruber, WA Baumgartner, G Senechal, J Meyers, JM Redmond, MF Pittenger, BJ Martin, Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann Thorac Surg 73, 1919-1925 (2002).
139. C Toma, MF Pittenger, KS Cahill, BJ Byrne, PD Kessler, Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105, 93-98 (2002). (Pubitemid 34049148)
140. NF Grigoropoulos, A Mathur, Stem cells in cardiac repair. Curr Opin Pharmacol 6, 169-175 (2006). (Pubitemid 43362131)
141. MA Laflamme, CE Murry, Regenerating the heart. Nat Biotechnol 23, 845-856 (2005). (Pubitemid 43093128)
142. MJ Lipinski, GG Biondi-Zoccai, A Abbate, R Khianey, I Sheiban, J Bartunek, M Vanderheyden, HS Kim, HJ Kang, BE Strauer, GW Vetrovec, Impact of intracoronary cell therapy on left ventricular function in the setting of acute myocardial infarction: a collaborative systematic review and meta-analysis of controlled clinical trials. J Am Coll Cardiol 50, 1761-1767 (2007). (Pubitemid 47600592)
143. J Dengler, H Song, N Thavandiran, S Masse, GA Wood, K Nanthakumar, PW Zandstra, M Radisic, Engineered heart tissue enables study of residual undifferentiated embryonic stem cell activity in a cardiac environment. Biotechnol Bioeng 108, 704-719 (2011).