Three-dimensional elastomeric scaffolds designed with cardiac-mimetic structural and mechanical features

Tissue Engineering - Part A

Volumn 19, Issue 5-6, 2013, Pages 793-807

  Neal, Rebekah A ^a   Jean, Aurélie ^b   Park, Hyoungshin ^a,c   Wu, Patrick B ^a   Hsiao, James ^c   Engelmayr, George C ^d   Langer, Robert ^a   Freed, Lisa E ^a,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c CHARLES STARK DRAPER LABORATORY   (United States)

^d Duke University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPECT RATIO; AUTOMOBILE MANUFACTURE; BIOMATERIALS; BIOMECHANICS; CELLS; GLYCEROL; HEART; INTERFACES (MATERIALS); MECHANICAL PROPERTIES; SILICON WAFERS; STRUTS; THREE DIMENSIONAL; THREE DIMENSIONAL COMPUTER GRAPHICS; TISSUE;

C2C12 MYOBLASTS; CARDIAC BIOMARKERS; CARDIAC PATIENTS; CARDIAC TISSUE ENGINEERING; CELL ELONGATION; DEGRADABLE BIOMATERIALS; ELASTOMERIC SCAFFOLDS; ELECTRICAL STIMULATIONS; EMPIRICAL INVESTIGATION; FE MODEL; FINITE ELEMENT MODELING; HIGH ASPECT RATIO; HIGH THROUGHPUT; INTERCONNECTED PORE NETWORKS; INTERCONNECTIVITY; LAYER-BY-LAYER ASSEMBLIES; LIVING CELL; MATERIAL SCIENCE; MECHANICAL FEATURE; MECHANICAL SUPPORT; MICROMOLDING; NEONATAL RAT; POLY(GLYCEROL SEBACATE); RAT HEART; STRUCTURAL FEATURE; TISSUE-ENGINEERED CONSTRUCTS;

SCAFFOLDS (BIOLOGY);

RATTUS;

BIOLOGICAL MARKER; BIOMIMETIC MATERIAL; DECANOIC ACID DERIVATIVE; DRUG DERIVATIVE; ELASTOMERIC; GLYCEROL; POLY(GLYCEROL SEBACATE); POLY(GLYCEROL-SEBACATE); POLYMER; TISSUE SCAFFOLD;

ANIMAL; ANISOTROPY; ARTICLE; BIOMECHANICS; CELL LINE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; FINITE ELEMENT ANALYSIS; HEART; HEART CONTRACTION; HEART MUSCLE CELL; METABOLISM; MOUSE; NEWBORN; PHYSIOLOGY; RAT; TISSUE ENGINEERING; ANALOGS AND DERIVATIVES; DRUG EFFECTS; TISSUE SCAFFOLD;

ANIMALS; ANIMALS, NEWBORN; ANISOTROPY; BIOLOGICAL MARKERS; BIOMECHANICAL PHENOMENA; BIOMIMETIC MATERIALS; CELL LINE; DECANOATES; FINITE ELEMENT ANALYSIS; GLYCEROL; HEART; MICE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; POLYMERS; RATS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84873396742     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0330     Document Type: Article

References (75)

1. Roger, V.L., Go, A.S., Lloyd-Jones, D.M., Benjamin, E.J., Berry, J.D., Borden, W.B., Bravata, D.M., Dai, S., Ford, E.S., Fox, C.S., Fullerton, H.J., Gillespie, C., Hailpern, S.M., Heit, J.A., Howard, V.J., Kissela, B.M., Kittner, S.J., Lackland, D.T., Lichtman, J.H., Lisabeth, L.D., Makuc, D.M., Marcus, G.M., Marelli, A., Matchar, D.B., Moy, C.S., Mozaffarian, D., Mussolino, M.E., Nichol, G., Paynter, N.P., Soliman, E.Z., Sorlie, P.D., Sotoodehnia, N., Turan, T.N., Virani, S.S., Wong, N.D., Woo, D., and Turner, M.B. Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 125, e2, 2012
2. Gilboa, S.M., Salemi, J.L., Nembhard, W.N., Fixler, D.E., and Correa, A. Mortality resulting from congenital heart disease among children and adults in the United States, 1999 to 2006/clinical perspective. Circulation 122, 2254, 2010
3. Zilla, P., Bezuidenhout, D., and Human, P. Prosthetic vas-cular grafts: wrong models, wrong questions and no healing. Biomaterials 28, 5009, 2007
4. Chikwe, J., Filsoufi, F., and Carpentier, A.F. Prosthetic valve selection for middle-aged patients with aortic stenosis. Nat Rev Cardiol 7, 711, 2010
5. Mann, D.L., Kubo, S.H., Sabbah, H.N., Starling, R.C., Jessup, M., Oh, J.K., and Acker, M.A. Beneficial effects of the CorCap cardiac support device: five-year results from the Acorn Trial. J Thorac Cardiovasc Surg 143, 1036, 2011
6. Tang, D., Yang, C., Geva, T., Gaudette, G., and del Nido, P.J. Multi-physics MRI-based two-layer fluid-structure interac-tion anisotropic models of human right and left ventricles with different patch materials: cardiac function assessment and mechanical stress analysis. Comput Struct 89,1059, 2011
7. Gorman, R., Jackson, B., Burdick, J., and Gorman, J. Infarct restraint to limit adverse ventricular remodeling. J Cardio-vasc Transl Res 4, 73, 2011
8. Tang, D., Yang, C., Geva, T., Gaudette, G., and Del Nido, P.J. Effect of patch mechanical properties on right ventricle function using MRI-based two-layer anisotropic models of human right and left ventricles. Comput Model Eng Sci 56, 113, 2010
9. Atluri, P., and Acker, M.A. Diastolic ventricular support with cardiac support devices: an alternative approach to prevent adverse ventricular remodeling. Heart Fail Rev Apr 15, 2012. [Epub ahead of print]; DOI: 10.1007/s10741-012-9312-4
10. Bursac, N., Papadaki, M., Cohen, R.J., Schoen, F.J., Eisen-berg, S.R., Carrier, R., Vunjak-Novakovic, G., and Freed, L.E. Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am J Physiol Heart Circ Physiol 277, H433, 1999
11. Engelmayr, G.C., Jr., Cheng, M., Bettinger, C.J., Borenstein, J.T., Langer, R., and Freed, L.E. Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat Mater 7, 1003, 2008
12. Lesman, A., Habib, M., Caspi, O., Gepstein, A., Arbel, G., Levenberg, S., and Gepstein, L. Transplantation of a tissue-engineered human vascularized cardiac muscle. Tissue Eng Part A 16, 115, 2010
13. Eschenhagen, T., Fink, C., Remmers, U., Scholz, H., Wattchow, J., Woil, J., Zimmermann, W., Dohmen, H.H., Schafer, H., Bishopric, N., Wakatsuki, T., and Elson, E. Three-dimensional reconstitution of embryonic cardiomyo-cytes in a collagen matrix: a new heart model system. FASEB J 11, 683, 1997
14. Davis, M.E., Hsieh, P.C., Takahashi, T., Song, Q., Zhang, S., Kamm, R.D., Grodzinsky, A.J., Anversa, P., and Lee, R.T. Local myocardial insulin-like growth factor 1 (IGF-1) deliv-ery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. PNAS 103, 8155, 2006
15. Ruvinov, E., Leor, J., and Cohen, S. The promotion of myocardial repair by the sequential delivery of IGF-1 and HGF from an injectable alginate biomaterial in a model of acute myocardial infarction. Biomaterials 32, 565, 2011
16. Liau, B., Christoforou, N., Leong, K.W., and Bursac, N. Pluripotent stem cell-derived cardiac tissue patch with ad-vanced structure and function. Biomaterials 32, 9180, 2011
17. Serrao, G.W., Turnbull, I.C., Ancukiewicz, D., Kim do, E., Kao, E., Cashman, T.J., Hadri, L., Hajjar, R.J., and Costa, K.D. Myocyte-depleted engineered cardiac tissues support therapeutic potential of mesenchymal stem cells. Tissue Eng Part A 18, 1322, 2012
18. Radisic, M., Yang, L., Boublik, J., Cohen, R.J., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Medium perfusion enables engineering of compact and contractile cardiac tis-sue. Am J Physiol Heart Circ Physiol 286, H507, 2004
19. Boublik, J., Park, H., Radisic, M., Tognana, E., Chen, F., Pei, M., Vunjak-Novakovic, G., and Freed, L.E. Mechanical properties and remodeling of hybrid cardiac constructs made from heart cells, fibrin, and biodegradable, elastomeric knitted fabric. Tissue Eng 11, 1122, 2005
20. Park, H., Larson, B.L., Guillemette, M.D., Jain, S.R., Hua, C., Engelmayr, G.C., Jr., and Freed, L.E. The significance of pore microarchitecture in a multi-layered elastomeric scaffold for contractile cardiac muscle constructs. Biomaterials 32, 1856, 2011
21. Lesman, A., Koffler, J., Atlas, R., Blinder, Y.J., Kam, Z., and Levenberg, S. Engineering vessel-like networks within multicellular fibrin-based constructs. Biomaterials 32, 7856, 2011
22. L'Heureux, N., Dusserre, N., Konig, G., Victor, B., Keire, P., Wight, T.N., Chronos, N.A.F., Kyles, A.E., Gregory, C.R., Hoyt, G., Robbins, R.C., and McAllister, T.N. Human tissue-engineered blood vessels for adult arterial revascularization. Nat Med 12, 361, 2006
23. Baar, K., Birla, R., Boluyt, M.O., Borschel, G.H., Arruda, E.M., and Dennis, R.G. Self-organization of rat cardiac cells into contractile 3-D cardiac tissue. FASEB J 19, 275, 2005
24. Stevens, K.R., Kreutziger, K.L., Dupras, S.K., Korte, F.S., Regnier, M., Muskheli, V., Nourse, M.B., Bendixen, K., Reinecke, H., and Murry, C.E. Physiological function and transplantation of scaffold-free and vascularized human car-diac muscle tissue. Proc Natl Acad Sci U S A 106,16568,2009
25. Ott, H.C., Matthiesen, T.S., Goh, S.K., Black, L.D., Kren, S.M., Netoff, T.I., and Taylor, D.A. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 14, 213, 2008
26. Langer, R., and Vacanti, J.P. Tissue engineering. Science 260, 920, 1993
27. Zimmermann, W.H., Melnychenko, I., Wasmeier, G., Didie, M., Naito, H., Nixdorff, U., Hess, A., Budinsky, L., Brune, K., Michaelis, B., Dhein, S., Schwoerer, A., Ehmke, H., and Eschenhagen, T. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12, 452, 2006
28. Dahl, S.L.M., Kypson, A.P., Lawson, J.H., Blum, J.L., Strader, J.T., Li, Y., Manson, R.J., Tente, W.E., DiBernardo, L., Hensley, M.T., Carter, R., Williams, T.P., Prichard, H.L., Dey, M.S., Begelman, KG., and Niklason, L.E. Readily available tissue-engineered vascular grafts. Sci Transl Med 3, 68ra9, 2011
29. Hibino, N., Shin'oka, T., Matsumura, G., Ikada, Y., and Kurosawa, H. The tissue-engineered vascular graft using bone marrow without culture. J Thorac Cardiovasc Surg 129, 1064, 2005
30. McAllister, T.N., Maruszewski, M., Garrido, S.A., Wy-strychowski, W., Dusserre, N., Marini, A., Zagalski, K., Fiorillo, A., Avila, H., Manglano, X., Antonelli, J., Kocher, A., Zembala, M., Cierpka, L., de la Fuente, L.M., and L'Heureux, N. Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: a multicentre cohort study. Lancet 373, 1440, 2009
31. Dohmen, P.M., Lembcke, A., Holinski, S., Pruss, A., and Konertz, W. Ten years of clinical results with a tissue-engineered pulmonary valve. Ann Thorac Surg 92,1308,2011
32. Freed, L.E., Engelmayr, G.C., Jr., Borenstein, J.T., Moutos, F.T., and Guilak, F. Advanced material strategies for tissue engineering scaffolds. Adv Mater 21, 3410, 2009
33. Jacot, J.G., McCulloch, A.D., and Omens, J.H. Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys J 95, 3479, 2008
34. Bhana, B., Iyer, R.K., Chen, W.L., Zhao, R., Sider, K.L., Likhitpanichkul, M., Simmons, C.A., and Radisic, M. Influ-ence of substrate stiffness on the phenotype of heart cells. Biotechnol Bioeng 105, 1148, 2010
35. Vunjak-Novakovic, G., Lui, K.O., Tandon, N., and Chien, K.R. Bioengineering heart muscle: a paradigm for regener-ative medicine. Annu Rev Biomed Eng 13, 245, 2011
36. Reis, L.A., Chiu, L.L., Liang, Y., Hyunh, K., Momen, A., and Radisic, M. A peptide-modified chitosan-collagen hydrogel for cardiac cell culture and delivery. Acta Biomater 8, 1022, 2011
37. Fomovsky, G.M., Rouillard, A.D., and Holmes, J.W. Regional mechanics determine collagen fiber structure in healing myocardial infarcts. J Mol Cell Cardiol 52, 1083, 2012
38. Holmes, J.W., Borg, T.K., and Covell, J.W. Structure and mechanics of healing myocardial infarcts. Annu Rev Biomed Eng 7, 223, 2005
39. Fomovsky, G.M., J.R., M., Ailawadi, G., and Holmes, J.W. Model-based design of mechanical therapies for myocardial infarction. J Cardiovasc Transl Res 4, 82, 2011
40. Fomovsky, G.M., Clark, S.A., Parker, K.M., Ailawadi, G., and Holmes, J.W. Anisotropic reinforcement of acute ante-roapical infarcts improves pump function. Circ Heart Fail 5, 515, 2012
41. Wang, Y., Ameer, G.A., Sheppard, B.J., and Langer, R. A tough biodegradable elastomer. Nat Biotechnol 20, 602, 2002
42. Rai, R., Tallawi, M., Grigore, A., and Boccaccini, A.R Synthesis, properties and biomedical applications of poly(glycerol sebacate) (PGS): a review. Prog Polym Sci 37, 1051, 2012
43. Wang, Y., Kim, Y.M., and Langer, R In vivo degradation characteristics of poly(glycerol sebacate). J Biomed Mater Res 66A, 192, 2003
44. Pomerantseva, I., Krebs, N., Hart, A., Neville, C.M., Huang, AY., and Sundback, C.A Degradation behavior of poly(glycerol sebacate). J Biomed Mater Res A 91,1038,2009
45. Sundback, C.A., Shyu, J.Y., Wang, Y., Faquin, W.C., Langer, R.S., Vacanti, J.P., and Hadlock, T.A. Biocompatibility analysis of poly(glycerol sebacate) as a nerve guide material. Biomaterials 26, 5454, 2005
46. Motlagh, D., Yang, J., Lui, K.Y., Webb, A.R., and Ameer, GA. Hemocompatibility evaluation of poly(glycerol-seba-cate) in vitro for vascular tissue engineering. Biomaterials 27, 4315, 2006
47. Chen, Q.Z., Bismarck, A., Hansen, U., Junaid, S., Tran, M.Q., Harding, S.E., Ali, N.N., and Boccaccini, A.R. Characterisa-tion of a soft elastomer poly(glycerol sebacate) designed to match the mechanical properties of myocardial tissue. Bio-materials 29, 47, 2008
48. Kemppainen, J.M. and Hollister, S.J. Tailoring the mechani-cal properties of 3D-designed poly(glycerol sebacate) scaf-folds for cartilage applications. J Biomed Mater Res 94, 9, 2010
49. Radisic, M., Park, H., Chen, F., Salazar-Lazzaro, J.E., Wang, Y., Dennis, R.G., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Biomimetic approach to cardiac tissue engi-neering: oxygen carriers and channeled scaffolds. Tissue Eng 12, 2077, 2006
50. Crapo, P.M., and Wang, Y. Hydrostatic pressure indepen-dently increases elastin and collagen co-expression in small-diameter engineered arterial constructs. J Biomed Mater Res A 96A, 673, 2011
51. Guillemette, M.D., Park, H., Hsiao, J.C., Jain, S.R., Larson, B.L., Langer, R., and Freed, L.E. Combined technologies for microfabricating elastomeric cardiac tissue engineering scaffolds. Macromol Biosci 10, 1330, 2010
52. Jean, A. and Engelmayr, G.C., Jr. Finite element analysis of an accordion-like honeycomb scaffold for cardiac tissue engineering. J Biomech 43, 3035, 2010
53. Jean, A. and Engelmayr, G.C. Anisotropic collagen fibril-logenesis within microfabricated scaffolds: implications for biomimetic tissue engineering. Adv Healthc Mater 1,112,2012
54. Radisic, M., Park, H., Martens, T.P., Salazar-Lazaro, J.E., Geng, W., Wang, Y., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Pre-treatment of synthetic elastomeric scaffolds by cardiac fibroblasts improves engineered heart tissue. J Biomed Mater Res 86A, 713, 2008
55. 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., and Harding, S.E. An elastomeric patch de-rived from poly(glycerol sebacate) for delivery of embryonic stem cells to the heart. Biomaterials 31, 3885, 2010
56. Stuckey, D.J., Ishii, H., Chen, Q.Z., Boccaccini, A.R., Hansen, U., Carr, C.A., Roether, J.A., Jawad, H., Tyler, D.J., Ali, N.N., Clarke, K., and Harding, S.E. Magnetic resonance imaging evaluation of remodeling by cardiac elastomeric tissue scaffold biomaterials in a rat model of myocardial infarction. Tissue Eng Part A 16, 3395, 2010
57. Wang, J., Bettinger, C.J., Langer, R.S., and Borenstein, J.T. Biodegradable microfluidic scaffolds for tissue engineering from amino alcohol-based poly(ester amide) elastomers. Organogenesis 6, 212, 2010
58. Neeley, W.L., Redenti, S., Klassen, H., Tao, S., Desai, T., Young, M.J., and Langer, R. A microfabricated scaffold for retinal progenitor cell grafting. Biomaterials 29, 418, 2008
59. Rasband, W. ImageJ. 1.45s ed. Bethesda, MD: National In-stitutes of Health, 2011
60. Naito, H., Melnychenko, I., Didie, M., Schneiderbanger, K., Schubert, P., Rosenkranz, S., Eschenhagen, T., and Zimmermann, W.H. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circula-tion 114, I72, 2006
61. Radisic, M., Park, H., Shing, H., Consi, T., Schoen, F.J., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Func-tional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. PNAS 101, 18129, 2004
62. Cheng, M., Moretti, M., Engelmayr, G.C., and Freed, L.E. Insulin-like growth factor-I and slow, bi-directional perfu-sion enhance the formation of tissue-engineered cardiac grafts. Tissue Eng Part A 15, 645, 2009
63. Engelmayr, G.C., Jr., Papworth, G.D., Watkins, S.C., Mayer, J.E., Jr., and Sacks, M.S. Guidance of engineered tissue collagen orientation by large-scale scaffold microstructures. J Biomech 39, 1819, 2006
64. Fidkowski, C., Kaazempur-Mofrad, M.R., Borenstein, J., Vacanti, J.P., Langer, R., and Wang, Y. Endothelialized mi-crovasculature based on a biodegradable elastomer. Tissue Eng 11, 302, 2005
65. Bettinger, C.J., Weinberg, E.J., Kulig, K.M., Vacanti, J.P., Wang, Y., Borenstein, J.T., and Langer, R. Three-dimensional microfluidic tissue-engineering scaffolds using a flexible biodegradable polymer. Adv Mater 18, 165, 2006
66. Nawroth, J.C., Lee, H., Feinberg, A.W., Ripplinger, C.M., McCain, M.L., Grosberg, A., Dabiri, J.O., and Parker, K.K. A tissue-engineered jellyfish with biomimetic propulsion. Nat Biotechnol 30, 792, 2012
67. Lesman, A., Gepstein, L., and Levenberg, S. Vascularization shaping the heart. Ann NY Acad Sci 1188, 46, 2010
68. Wong, K.H., Chan, J.M., Kamm, R.D., and Tien, J. Micro-fluidic models of vascular functions. Annu Rev Biomed Eng 14, 205, 2012
69. Miller, J.S., Stevens, K.R., Yang, M.T., Baker, B.M., Nguyen, D.H., Cohen, D.M., Toro, E., Chen, A.A., Galie, P.A., Yu, X., Chaturvedi, R., Bhatia, S.N., and Chen, C.S. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 11, 768, 2012
70. Charest, J.L., Garcia, A.J., and King, W.P. Myoblast align-ment and differentiation on cell culture substrates with mi-croscale topography and model chemistries. Biomaterials 28, 2202, 2007
71. Cheng, M.Y., Park, H., Engelmayr, G.C., Moretti, M., and Freed, L.E. Effects of regulatory factors on engineered car-diac tissue in vitro. Tissue Eng 13, 2709, 2007
72. Tandon, N., Cannizzaro, C., Chao, P.H., Maidhof, R., Marsano, A., Au, H.T., Radisic, M., and Vunjak-Novakovic, G. Electrical stimulation systems for cardiac tissue engi-neering. Nat Protoc 4, 155, 2009
73. Shim, J., Grosberg, A., Nawroth, J.C., Parker, K.K., and Bertoldi, K. Modeling of cardiac muscle thin films: pre-stretch, passive and active behavior. J Biomech 45, 832, 2012
74. Liau, B., Zhang, D., and Bursac, N. Functional cardiac tissue engineering. Regenerative Med 7, 187, 2012
75. Walsh, R.G. Design and features of the Acorn CorCap cardiac support device: the concept of passive mechanical diastolic support. Heart Fail Rev 10, 101, 2005