Engineered cardiac tissues

Current Opinion in Biotechnology

Volumn 22, Issue 5, 2011, Pages 706-714

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

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOREACTOR DESIGN; CARDIAC TISSUE ENGINEERING; CARDIAC TISSUES; CELL SHEET ENGINEERING; CELL-BASED; DECELLULARIZATION; DEVELOPMENTAL BIOLOGY; DRUG SCREENING; FUNCTIONAL TISSUE; IN-VITRO; POLYMER SCIENCE; STEM CELL BIOLOGY; VASCULARIZATION;

BIOMATERIALS; BIOREACTORS; CYTOLOGY; DESIGN; GENETIC ENGINEERING; HEART; STEM CELLS; TISSUE;

SCAFFOLDS (BIOLOGY);

BIOENGINEERING; BIOREACTOR; CELL MATURATION; CELL SHEET ENGINEERING; EMBRYONIC STEM CELL; EQUIPMENT DESIGN; EXTRACELLULAR MATRIX; HEART; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; IN VIVO STUDY; NONHUMAN; ORGAN DECELLULARIZATION; PRIORITY JOURNAL; REVIEW; TISSUE ENGINEERING; VASCULARIZATION;

ANIMALS; HUMANS; MYOCARDIUM; MYOCYTES, CARDIAC; STEM CELLS; TISSUE ENGINEERING;

EID: 80053383932     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2011.04.004     Document Type: Review

References (68)

1. Lloyd-Jones D., Adams R.J., Brown T.M., Carnethon M., Dai S., De Simone G., Ferguson T.B., Ford E., Furie K., Gillespie C., et al. Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 2010, 121:e46-e215.
2. Radisic M., Malda J., Epping E., Geng W., Langer R., Vunjak-Novakovic G. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol Bioeng 2006, 93:332-343.
3. Radisic M., Park H., Chen F., Salazar-Lazzaro J.E., Wang Y., Dennis R., Langer R., Freed L.E., Vunjak-Novakovic G. Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng 2006, 12:2077-2091.
4. Radisic M., Park H., Gerecht S., Cannizzaro C., Langer R., Vunjak-Novakovic G. Biomimetic approach to cardiac tissue engineering. Philos Trans R Soc Lond B Biol Sci 2007, 362:1357-1368.
5. Barash Y., Dvir T., Tandeitnik P., Ruvinov E., Guterman H., Cohen S. Electric field stimulation integrated into perfusion bioreactor for cardiac tissue engineering. Tissue Eng Part C Methods 2010, 16:1417-1426.
6. Brown M.A., Iyer R.K., Radisic M. Pulsatile perfusion bioreactor for cardiac tissue engineering. Biotechnol Prog 2008, 24:907-920.
7. Zimmermann W.H., Schneiderbanger K., Schubert P., Didie M., Munzel F., Heubach J.F., Kostin S., Neuhuber W.L., Eschenhagen T. Tissue engineering of a differentiated cardiac muscle construct. Circ Res 2002, 90:223-230.
8. Zimmermann W.H., Melnychenko I., Wasmeier G., Didie M., Naito H., Nixdorff U., Hess A., Budinsky L., Brune K., Michaelis B., et al. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 2006, 12:452-458.
9. Radisic M., Park H., Shing H., Consi T., Schoen F.J., Langer R., Freed L.E., Vunjak-Novakovic G. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci U S A 2004, 101:18129-18134.
10. Tandon N., Cannizzaro C., Chao P.H., Maidhof R., Marsano A., Au H.T., Radisic M., Vunjak-Novakovic G. Electrical stimulation systems for cardiac tissue engineering. Nat Protoc 2009, 4:155-173.
11. Chiu L.L., Iyer R.K., King J.P., Radisic M. Biphasic electrical field stimulation aids in tissue engineering of multicell-type cardiac organoids. Tissue Eng Part A 2008, 14:1-13.
12. Miyagawa S., Sawa Y., Sakakida S., Taketani S., Kondoh H., Memon I.A., Imanishi Y., Shimizu T., Okano T., Matsuda H. Tissue cardiomyoplasty using bioengineered contractile cardiomyocyte sheets to repair damaged myocardium: their integration with recipient myocardium. Transplantation 2005, 80:1586-1595.
13. Furuta A., Miyoshi S., Itabashi Y., Shimizu T., Kira S., Hayakawa K., Nishiyama N., Tanimoto K., Hagiwara Y., Satoh T., et al. Pulsatile cardiac tissue grafts using a novel three-dimensional cell sheet manipulation technique functionally integrates with the host heart, in vivo. Circ Res 2006, 98:705-712.
14. Matsuura K., Honda A., Nagai T., Fukushima N., Iwanaga K., Tokunaga M., Shimizu T., Okano T., Kasanuki H., Hagiwara N., et al. Transplantation of cardiac progenitor cells ameliorates cardiac dysfunction after myocardial infarction in mice. J Clin Invest 2009, 119:2204-2217.
15. Bel A., Planat-Bernard V., Saito A., Bonnevie L., Bellamy V., Sabbah L., Bellabas L., Brinon B., Vanneaux V., Pradeau P., et al. Composite cell sheets: a further step toward safe and effective myocardial regeneration by cardiac progenitors derived from embryonic stem cells. Circulation 2010, 122:S118-123.
16. Sawa Y. Myocardial regeneration for heart failure. Nippon Rinsho 2010, 68:719-725.
17. Di Donato M., Sabatier M., Dor V., Gensini G.F., Toso A., Maioli M., Stanley A.W., Athanasuleas C., Buckberg G. Effects of the Dor procedure on left ventricular dimension and shape and geometric correlates of mitral regurgitation one year after surgery. J Thorac Cardiovasc Surg 2001, 121:91-96.
18. Kochupura P.V., Azeloglu E.U., Kelly D.J., Doronin S.V., Badylak S.F., Krukenkamp I.B., Cohen I.S., Gaudette G.R. Tissue-engineered myocardial patch derived from extracellular matrix provides regional mechanical function. Circulation 2005, 112:I144-149.
19. Kelly D.J., Rosen A.B., Schuldt A.J., Kochupura P.V., Doronin S.V., Potapova I.A., Azeloglu E.U., Badylak S.F., Brink P.R., Cohen I.S., et al. Increased myocyte content and mechanical function within a tissue-engineered myocardial patch following implantation. Tissue Eng Part A 2009, 15:2189-2201.
20. DeQuach J.A., Mezzano V., Miglani A., Lange S., Keller G.M., Sheikh F., Christman K.L. Simple and high yielding method for preparing tissue specific extracellular matrix coatings for cell culture. PLoS ONE 2010, 5:e13039.
21. Ott H.C., Matthiesen T.S., Goh S.K., Black L.D., Kren S.M., Netoff T.I., Taylor D.A. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 2008, 14:213-221.
22. Taylor D.A. From stem cells and cadaveric matrix to engineered organs. Curr Opin Biotechnol 2009, 20:598-605.
23. Korecky B., Hai C.M., Rakusan K. Functional capillary density in normal and transplanted rat hearts. Can J Physiol Pharmacol 1982, 60:23-32.
24. Radisic M., Park H., Martens T.P., Salazar-Lazaro J.E., Geng W., Wang Y., Langer R., Freed L.E., Vunjak-Novakovic G. Pre-treatment of synthetic elastomeric scaffolds by cardiac fibroblasts improves engineered heart tissue. J Biomed Mater Res A 2007, 86:713-772.
25. Iyer R.K., Chui J., Radisic M. Spatiotemporal tracking of cells in tissue-engineered cardiac organoids. J Tissue Eng Regen Med 2009, 3:196-207.
26. Iyer R.K., Chiu L.L., Radisic M. Microfabricated poly(ethylene glycol) templates enable rapid screening of triculture conditions for cardiac tissue engineering. J Biomed Mater Res A 2008, 89:616-631.
27. Naito H., Melnychenko I., Didie M., Schneiderbanger K., Schubert P., Rosenkranz S., Eschenhagen T., Zimmermann W.H. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 2006, 114:I72-78.
28. Sasagawa T., Shimizu T., Sekiya S., Haraguchi Y., Yamato M., Sawa Y., Okano T. Design of prevascularized three-dimensional cell-dense tissues using a cell sheet stacking manipulation technology. Biomaterials 2010, 31:1646-1654.
29. Sekine H., Shimizu T., Hobo K., Sekiya S., Yang J., Yamato M., Kurosawa H., Kobayashi E., Okano T. Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 2008, 118:S145-152.
30. Saif J., Schwarz T.M., Chau D.Y., Henstock J., Sami P., Leicht S.F., Hermann P.C., Alcala S., Mulero F., Shakesheff K.M., et al. Combination of injectable multiple growth factor-releasing scaffolds and cell therapy as an advanced modality to enhance tissue neovascularization. Arterioscler Thromb Vasc Biol 2010, 30:1897-1904.
31. Jay S.M., Shepherd B.R., Andrejecsk J.W., Kyriakides T.R., Pober J.S., Saltzman W.M. Dual delivery of VEGF and MCP-1 to support endothelial cell transplantation for therapeutic vascularization. Biomaterials 2010, 31:3054-3062.
32. Smart N., Risebro C.A., Clark J.E., Ehler E., Miquerol L., Rossdeutsch A., Marber M.S., Riley P.R. Thymosin beta4 facilitates epicardial neovascularization of the injured adult heart. Ann N Y Acad Sci 2010, 1194:97-104.
33. Martinez E.C., Wang J., Gan S.U., Singh R., Lee C.N., Kofidis T. Ascorbic acid improves embryonic cardiomyoblast cell survival and promotes vascularization in potential myocardial grafts in vivo. Tissue Eng Part A 2010, 16:1349-1361.
34. Zhang J., Ding L., Zhao Y., Sun W., Chen B., Lin H., Wang X., Zhang L., Xu B., Dai J. Collagen-targeting vascular endothelial growth factor improves cardiac performance after myocardial infarction. Circulation 2009, 119:1776-1784.
35. Chiu L.L., Radisic M. Scaffolds with covalently immobilized VEGF and Angiopoietin-1 for vascularization of engineered tissues. Biomaterials 2010, 31:226-241.
36. Chiu L.L., Weisel R.D., Li R.K., Radisic M. Defining conditions for covalent immobilization of angiogenic growth factors onto scaffolds for tissue engineering. J Tissue Eng Regen Med 2011, 5:69-84.
37. Miyagi Y., Chiu L.L., Cimini M., Weisel R.D., Radisic M., Li R.K. Biodegradable collagen patch with covalently immobilized VEGF for myocardial repair. Biomaterials 2011, 32:1280-1290.
38. Dvir T., Kedem A., Ruvinov E., Levy O., Freeman I., Landa N., Holbova R., Feinberg M.S., Dror S., Etzion Y., et al. Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc Natl Acad Sci U S A 2009, 106:14990-14995.
39. Madden L.R., Mortisen D.J., Sussman E.M., Dupras S.K., Fugate J.A., Cuy J.L., Hauch K.D., Laflamme M.A., Murry C.E., Ratner B.D. Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc Natl Acad Sci U S A 2010, 107:15211-15216.
40. Morritt A.N., Bortolotto S.K., Dilley R.J., Han X., Kompa A.R., McCombe D., Wright C.E., Itescu S., Angus J.A., Morrison W.A. Cardiac tissue engineering in an in vivo vascularized chamber. Circulation 2007, 115:353-360.
41. Tilkorn D.J., Bedogni A., Keramidaris E., Han X., Palmer J.A., Dingle A.M., Cowling B.S., Williams M.D., McKay S.M., Pepe L., et al. Implanted myoblast survival is dependent on the degree of vascularization in a novel delayed implantation/prevascularization tissue engineering model. Tissue Eng Part A 2010, 16:165-178.
42. Kim D.H., Lipke E.A., Kim P., Cheong R., Thompson S., Delannoy M., Suh K.Y., Tung L., Levchenko A. Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs. Proc Natl Acad Sci U S A 2010, 107:565-570.
43. Au H.T., Cheng I., Chowdhury M.F., Radisic M. Interactive effects of surface topography and pulsatile electrical field stimulation on orientation and elongation of fibroblasts and cardiomyocytes. Biomaterials 2007, 28:4277-4293.
44. Au H., Cui B., Chu Z., Veres T., Radisic M. Cell culture chips for simultaneous application of topographical and electrical cues enhance phenotype of cardiomyocytes. Lab Chip 2009, 10.1039/b810034a.
45. Badie N., Bursac N. Novel micropatterned cardiac cell cultures with realistic ventricular microstructure. Biophys J 2009, 96:3873-3885.
46. Badrossamay M.R., McIlwee H.A., Goss J.A., Parker K.K. Nanofiber assembly by rotary jet-spinning. Nano Lett 2010, 10:2257-2261.
47. Alford P.W., Feinberg A.W., Sheehy S.P., Parker K.K. Biohybrid thin films for measuring contractility in engineered cardiovascular muscle. Biomaterials 2010, 31:3613-3621.
48. Bian W., Bursac N. Engineered skeletal muscle tissue networks with controllable architecture. Biomaterials 2009, 30:1401-1412.
49. Legant W.R., Pathak A., Yang M.T., Deshpande V.S., McMeeking R.M., Chen C.S. Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues. Proc Natl Acad Sci U S A 2009, 106:10097-10102.
50. Chung C.Y., Bien H., Sobie E.A., Dasari V., McKinnon D., Rosati B., Entcheva E. Hypertrophic phenotype in cardiac cell assemblies solely by structural cues and ensuing self-organization. FASEB J 2010.
51. Engelmayr G.C., Cheng M., Bettinger C.J., Borenstein J.T., Langer R., Freed L.E. Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat Mater 2008, 7:1003-1010.
52. Soonpaa M.H., Field L.J. Survey of studies examining mammalian cardiomyocyte DNA synthesis. Circ Res 1998, 83:15-26.
53. Moretti A., Caron L., Nakano A., Lam J.T., Bernshausen A., Chen Y., Qyang Y., Bu L., Sasaki M., Martin-Puig S., et al. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 2006, 127:1151-1165.
54. Smith R.R., Barile L., Cho H.C., Leppo M.K., Hare J.M., Messina E., Giacomello A., Abraham M.R., Marban E. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007, 115:896-908.
55. Guo X.M., Zhao Y.S., Chang H.X., Wang C.Y., E L.L., Zhang X.A., Duan C.M., Dong L.Z., Jiang H., Li J., et al. Creation of engineered cardiac tissue in vitro from mouse embryonic stem cells. Circulation 2006, 113:2229-2237.
56. Domian I.J., Chiravuri M., van der Meer P., Feinberg A.W., Shi X., Shao Y., Wu S.M., Parker K.K., Chien K.R. Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science 2009, 326:426-429.
57. Caspi O., Lesman A., Basevitch Y., Gepstein A., Arbel G., Habib I.H., Gepstein L., Levenberg S. Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 2007, 100:263-272.
58. Chen Q.Z., Ishii H., Thouas G.A., Lyon A.R., Wright J.S., Blaker J.J., Chrzanowski W., Boccaccini A.R., Ali N.N., Knowles J.C., et al. An elastomeric patch derived from poly(glycerol sebacate) for delivery of embryonic stem cells to the heart. Biomaterials 2010, 31:3885-3893.
59. Lesman A., Habib M., Caspi O., Gepstein A., Arbel G., Levenberg S., Gepstein L. Transplantation of a tissue-engineered human vascularized cardiac muscle. Tissue Eng Part A 2010, 16:115-125.
60. Stevens K.R., Pabon L., Muskheli V., Murry C.E. Scaffold-free human cardiac tissue patch created from embryonic stem cells. Tissue Eng Part A 2009, 15:1211-1222.
61. Stevens K.R., Kreutziger K.L., Dupras S.K., Korte F.S., Regnier M., Muskheli V., Nourse M.B., Bendixen K., Reinecke H., Murry C.E. Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc Natl Acad Sci U S A 2009, 106:16568-16573.
62. Hansen A., Eder A., Bonstrup M., Flato M., Mewe M., Schaaf S., Aksehirlioglu B., Schworer A., Uebeler J., Eschenhagen T. Development of a drug screening platform based on engineered heart tissue. Circ Res 2010, 107:35-44.
63. Laflamme M.A., Murry C.E. Regenerating the heart. Nat Biotechnol 2005, 23:845-856.
64. Lipinski M.J., Biondi-Zoccai G.G., Abbate A., Khianey R., Sheiban I., Bartunek J., Vanderheyden M., Kim H.S., Kang H.J., Strauer B.E., et al. 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 2007, 50:1761-1767.
65. Dengler J., Song H., Thavandiran N., Masse S., Wood G.A., Nanthakumar K., Zandstra P.W., Radisic M. Engineered heart tissue enables study of residual undifferentiated embryonic stem cell activity in a cardiac environment. Biotechnol Bioeng 2010, 108:704-719.
66. Song H., Yoon C., Kattman S.J., Dengler J., Masse S., Thavaratnam T., Gewarges M., Nanthakumar K., Rubart M., Keller G.M., et al. Interrogating functional integration between injected pluripotent stem cell-derived cells and surrogate cardiac tissue. Proc Natl Acad Sci U S A 2010, 107:3329-3334.
67. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
68. Zhang J., Wilson G.F., Soerens A.G., Koonce C.H., Yu J., Palecek S.P., Thomson J.A., Kamp T.J. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 2009, 104:e30-41.