Generation of bioartificial heart tissue by combining a three-dimensional gel-based cardiac construct with decellularized small intestinal submucosa

Tissue Engineering - Part A

Volumn 20, Issue 3-4, 2014, Pages 799-809

  Vukadinovic Nikolic, Zlata ^a   Andrée, Birgit ^a   Dorfman, Suzanne E ^a   Pflaum, Michael ^a   Horvath, Tibor ^a   Lux, Marco ^a   Venturini, Letizia ^b   Bär, Antonia ^a   Kensah, George ^a   Lara, Angelica Roa ^a   Tudorache, Igor ^a   Cebotari, Serghei ^a   Hilfiker Kleiner, Denise ^b   Haverich, Axel ^a   Hilfiker, Andres ^a  

^a Leibniz Laboratories for Biotechnology and Artificial Organs   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEX NETWORKS; CYTOLOGY; ENDOTHELIAL CELLS; HEART; MICROELECTRODES; MORPHOLOGY; RATS; REPAIR; THREE DIMENSIONAL; TISSUE ENGINEERING;

ARTIFICIAL TISSUES; CARDIAC CONSTRUCTS; CLINICAL APPLICATION; ENDOTHELIAL CELL LINE; LONGITUDINAL AXIS; MICROELECTRODE ARRAY; RAT NEONATAL CARDIOMYOCYTES; SMALL INTESTINAL SUBMUCOSA;

TISSUE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA ADRENERGIC STIMULATION; BIOARTIFICIAL HEART; BIOARTIFICIAL ORGAN; CELL GROWTH; CELL ISOLATION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; GEL; HEART MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SMALL INTESTINE MUCOSA; SUBMUCOSA; TISSUE ENGINEERING;

ANIMALS; BIOARTIFICIAL ORGANS; CELL LINE; CELL MOVEMENT; CELL SHAPE; ELECTROPHYSIOLOGICAL PHENOMENA; ENDOTHELIAL CELLS; GELS; HEART; INTESTINAL MUCOSA; INTESTINE, SMALL; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA; SUS SCROFA; TISSUE SCAFFOLDS;

EID: 84894194833     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0184     Document Type: Article

References (56)

1. Shimizu, T., Yamato, M., Isoi, Y., Akutsu, T., Setomaru, T., Abe, K., Kikuchi, A., Umezu, M., and Okano, T. Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res 90, e40, 2002.
2. Zimmermann, W.H., Fink, C., Kralisch, D., Remmers, U., Weil, J., and Eschenhagen, T. Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnol Bioeng 68, 106, 2000.
3. Park, H., Radisic, M., Lim, J.O., Chang, B.H., and Vunjak-Novakovic, G. A novel composite scaffold for cardiac tissue engineering. In Vitro Cell Dev Biol Anim 41, 188, 2005.
4. Andrée, B., Bär, A., Haverich, A., and Hilfiker, A. Small intestinal submucosa segments as matrix for tissue engineering: review. Tissue Eng Part B Rev 19, 279, 2013.
5. Hoganson, D.M., Owens, G.E., O'Doherty, E.M., Bowley, C.M., Goldman, S.M., Harilal, D.O., Neville, C.M., Kro-nengold, R.T., and Vacanti, J.P. Preserved extracellular matrix components and retained biological activity in decellularized porcine mesothelium. Biomaterials 31, 6934, 2010.
6. Chen, W., Li, C., Wu, S., Xie, H., and Luo, J. [Effect of acellular process on small intestinal submucosa cell residue and growth factor content]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 24, 94, 2010.
7. Lindberg, K., and Badylak, S.F. Porcine small intestinal submucosa (SIS): a bioscaffold supporting in vitro primary human epidermal cell differentiation and synthesis of basement membrane proteins. Burns 27, 254, 2001.
8. Hata, H., Bär, A., Dorfman, S., Vukadinovic, Z., Sawa, Y., Haverich, A., and Hilfiker, A. Engineering a novel three-dimensional contractile myocardial patch with cell sheets and decellularised matrix. Eur J Cardiothorac Surg 38, 450, 2010.
9. Eschenhagen, T., and Zimmermann, W.H. Engineering myocardial tissue. Circ Res 97, 1220, 2005.
10. Carrier, R.L., Rupnick, M., Langer, R., Schoen, F.J., Freed, L.E., and Vunjak-Novakovic, G. Perfusion improves tissue architecture of engineered cardiac muscle. Tissue Eng 8, 175, 2002.
11. Zhang, T., Wan, L.Q., Xiong, Z., Marsano, A., Maidhof, R., Park, M., Yan, Y., and Vunjak-Novakovic, G. Channelled scaffolds for engineering myocardium with mechanical stimulation. J Tissue Eng Regen Med 2011 [Epub ahead of print]; DOI: 10.1002/term.481.
12. Sakaguchi, K., Shimizu, T., Horaguchi, S., Sekine, H., Ya-mato, M., Umezu, M., and Okano, T. In vitro engineering of vascularized tissue surrogates. Sci Rep 3, 1316, 2013.
13. Radisic, M., Park, H., Chen, F., Salazar-Lazzaro, J.E., Wang, Y., Dennis, R., Langer, R., Freed, L.E., and Vunjak-Nova-kovic, G. Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng 12, 2077, 2006.
14. Iyer, R.K., Radisic, M., Cannizzaro, C., and Vunjak-Nova-kovic, G. Synthetic oxygen carriers in cardiac tissue engineering. Artif Cells Blood Substit Immobil Biotechnol 35, 135, 2007.
15. Marsano, A., Maidhof, R., Luo, J., Fujikara, K., Konofagou, E.E., Banfi, A., and Vunjak-Novakovic, G. The effect of controlled expression of VEGF by transduced myoblasts in a cardiac patch on vascularization in a mouse model of myocardial infarction. Biomaterials 34, 393, 2013.
16. 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.
17. Tulloch, N.L., Muskheli, V., Razumova, M.V., Korte, F.S., Regnier, M., Hauch, K.D., Pabon, L., Reinecke, H., and Murry, C.E. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res 109, 47, 2011.
18. Tee, R., Morrison, W.A., Dusting, G.J., Liu, G.S., Choi, Y.S., Hsiao, S.T., and Dilley, R.J. Transplantation of engineered cardiac muscle flaps in syngeneic rats. Tissue Eng Part A 18, 1992, 2012.
19. Bär, A., Dorfman, S.E., Fischer, P., Hilfiker-Kleiner, D., Ce-botari, S., Tudorache, I., Suprunov, M., Haverich, A., and Hilfiker, A. The pro-angiogenic factor CCN1 enhances the re-endothelialization of biological vascularized matrices in vitro. Cardiovasc Res 85, 806, 2010.
20. Schultheiss, D., Gabouev, A.I., Kaufmann, P.M., Schlote, N., Mertsching, H., Haverich, A., Stief, C.G., and Jonas, U. [Biological vascularized matrix (BioVaM): a new method for solving the perfusion problems in tissue engineering]. Ur-ologe A 43, 1223, 2004.
21. Hilfiker-Kleiner, D., Kaminski, K., Kaminska, A., Fuchs, M., Klein, G., Podewski, E., Grote, K., Kiian, I., Wollert, K.C., Hilfiker, A., and Drexler, H. Regulation of proangiogenic factor CCN1 in cardiac muscle: impact of ischemia, pressure overload, and neurohumoral activation. Circulation 109, 2227, 2004.
22. Kensah, G., Gruh, I., Viering, J., Schumann, H., Dahlmann, J., Meyer, H., Skvorc, D., Bar, A., Akhyari, P., Heisterkamp, A., Haverich, A., and Martin, U. A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation. Tissue Eng Part C Methods 17, 463, 2011.
23. Hattori, F., Chen, H., Yamashita, H., Tohyama, S., Satoh, Y.S., Yuasa, S., Li, W., Yamakawa, H., Tanaka, T., Onitsuka, T., Shimoji, K., Ohno, Y., Egashira, T., Kaneda, R., Murata, M., Hidaka, K., Morisaki, T., Sasaki, E., Suzuki, T., Sano, M., Makino, S., Oikawa, S., and Fukuda, K. Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat Methods 7, 61, 2010.
24. Obermeyer, N., Janson, N., Bergmann, J., Buck, F., and Ito, W.D. Proteome analysis of migrating versus nonmigrating rat heart endothelial cells reveals distinct expression patterns. Endothelium 10, 167, 2003.
25. Demaison, C., Parsley, K., Brouns, G., Scherr, M., Battmer, K., Kinnon, C., Grez, M., and Thrasher, A.J. High-level transduction and gene expression in hematopoietic re-populating cells using a human immunodeficiency [correction of imunodeficiency] virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther 13, 803, 2002.
26. Scherr, M., Battmer, K., Ganser, A., and Eder, M. Modulation of gene expression by lentiviral-mediated delivery of small interfering RNA. Cell Cycle 2, 251, 2003.
27. Zufferey, R., Dull, T., Mandel, R.J., Bukovsky, A., Quiroz, D., Naldini, L., and Trono, D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 72, 9873, 1998.
28. Tandon, N., Cannizzaro, C., Figallo, E., Voldman, J., and Vunjak-Novakovic, G. Characterization of electrical stimulation electrodes for cardiac tissue engineering. Conf Proc IEEE Eng Med Biol Soc 1, 845, 2006.
29. Cannizzaro, C., Tandon, N., Figallo, E., Park, H., Gerecht, S., Radisic, M., Elvassore, N., and Vunjak-Novakovic, G. Practical aspects of cardiac tissue engineering with electrical stimulation. Methods Mol Med 140, 291, 2007.
30. Maidhof, R., Tandon, N., Lee, E.J., Luo, J., Duan, Y., Yeager, K., Konofagou, E., and Vunjak-Novakovic, G. Biomimetic perfusion and electrical stimulation applied in concert improved the assembly of engineered cardiac tissue. J Tissue Eng Regen Med 6, e12, 2011.
31. Zimmermann, W.H., Schneiderbanger, K., Schubert, P., Di-die, M., Munzel, F., Heubach, J.F., Kostin, S., Neuhuber, W.L., and Eschenhagen, T. Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90, 223, 2002.
32. Fink, C., Ergun, S., Kralisch, D., Remmers, U., Weil, J., and Eschenhagen, T. Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J 14, 669, 2000.
33. Gopalan, S.M., Flaim, C., Bhatia, S.N., Hoshijima, M., Knoell, R., Chien, K.R., Omens, J.H., and McCulloch, A.D. Aniso-tropic stretch-induced hypertrophy in neonatal ventricular myocytes micropatterned on deformable elastomers. Bio-technol Bioeng 81, 578, 2003.
34. Frey, N., and Olson, E.N. Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol 65, 45, 2003.
35. Sun, L.S., Legato, M.J., Rosen, T.S., Steinberg, S.F., and Rosen, M.R. Sympathetic innervation modulates ventricular impulse propagation and repolarisation in the immature rat heart. Cardiovasc Res 27, 459, 1993.
36. Radisic, M., Fast, V.G., Sharifov, O.F., Iyer, R.K., Park, H., and Vunjak-Novakovic, G. Optical mapping of impulse propagation in engineered cardiac tissue. Tissue Eng Part A 15, 851, 2009.
37. Black, L.D., 3rd, Meyers, J.D., Weinbaum, J.S., Shvelidze, Y.A., and Tranquillo, R.T. Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. Tissue Eng Part A 15, 3099, 2009.
38. Salameh, A., Wustmann, A., Karl, S., Blanke, K., Apel, D., Rojas-Gomez, D., Franke, H., Mohr, F.W., Janousek, J., and Dhein, S. Cyclic mechanical stretch induces cardiomyocyte orientation and polarization of the gap junction protein connexin43. Circ Res 106, 1592, 2010.
39. Montanez, E., Casaroli-Marano, R.P., Vilaro, S., and Pagan, R. Comparative study of tube assembly in three-dimensional collagen matrix and on Matrigel coats. Angiogenesis 5, 167, 2002.
40. Naito, H., Melnychenko, I., Didie, M., Schneiderbanger, K., Schubert, P., Rosenkranz, S., Eschenhagen, T., and Zim-mermann, W.H. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114, I72, 2006.
41. Voytik-Harbin, S.L., Brightman, A.O., Kraine, M.R., Wais-ner, B., and Badylak, S.F. Identification of extractable growth factors from small intestinal submucosa. J Cell Biochem 67, 478, 1997.
42. Li, F., Li, W., Johnson, S., Ingram, D., Yoder, M., and Bady-lak, S. Low-molecular-weight peptides derived from extracellular matrix as chemoattractants for primary endothelial cells. Endothelium 11, 199, 2004.
43. Tannock, I.F., and Kopelyan, I. Variation of pO2 in the growth medium of spheroids: interaction with glucose to influence spheroid growth and necrosis. Br J Cancer 53, 823, 1986.
44. Martinez, E.C., Wang, J., Gan, S.U., Singh, R., Lee, C.N., and Kofidis, T. Ascorbic acid improves embryonic cardiomyo-blast cell survival and promotes vascularization in potential myocardial grafts in vivo. Tissue Eng Part A 16, 1349, 2010.
45. Dvir, T., Kedem, A., Ruvinov, E., Levy, O., Freeman, I., Landa, N., Holbova, R., Feinberg, M.S., Dror, S., Etzion, Y., Leor, J., and Cohen, S. Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc Natl Acad Sci USA 106, 14990, 2009.
46. 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.
47. Wainwright, J.M., Czajka, C.A., Patel, U.B., Freytes, D.O., Tobita, K., Gilbert, T.W., and Badylak, S.F. Preparation of cardiac extracellular matrix from an intact porcine heart. Tissue Eng Part C Methods 16, 525, 2010.
48. Akhyari, P., Aubin, H., Gwanmesia, P., Barth, M., Hoffmann, S., Huelsmann, J., Preuss, K., and Lichtenberg, A. The quest for an optimized protocol for whole-heart decellular-ization: a comparison of three popular and a novel decel-lularization technique and their diverse effects on crucial extracellular matrix qualities. Tissue Eng Part C Methods 17, 915, 2011.
49. Sarig, U., Au-Yeung, G.C., Wang, Y., Bronshtein, T., Dahan, N., Boey, F.Y., Venkatraman, S.S., and Machluf, M. Thick acellular heart extracellular matrix with inherent vascula-ture: a potential platform for myocardial tissue regeneration. Tissue Eng Part A 18, 2125, 2012.
50. Schulte, J.B., Simionescu, A., and Simionescu, D.T. The acellular myocardial flap: a novel extracellular matrix scaffold enriched with patent microvascular networks and bio-compatible cell niches. Tissue Eng Part C Methods 19, 518, 2013.
51. Tudorache, I., Kostin, S., Meyer, T., Teebken, O., Bara, C., Hilfiker, A., Haverich, A., and Cebotari, S. Viable vascularized autologous patch for transmural myocardial reconstruction. Eur J Cardiothorac Surg 36, 306, 2009.
52. Haase, A., Olmer, R., Schwanke, K., Wunderlich, S., Merkert, S., Hess, C., Zweigerdt, R., Gruh, I., Meyer, J., Wagner, S., Maier, L.S., Han, D.W., Glage, S., Miller, K., Fischer, P., Scholer, H.R., and Martin, U. Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell 5, 434, 2009.
53. Zweigerdt, R. Large scale production of stem cells and their derivatives. Adv Biochem Eng Biotechnol 114, 201, 2009.
54. Matsuura, K., Wada, M., Shimizu, T., Haraguchi, Y., Sato, F., Sugiyama, K., Konishi, K., Shiba, Y., Ichikawa, H., Tachi-bana, A., Ikeda, U., Yamato, M., Hagiwara, N., and Okano, T. Creation of human cardiac cell sheets using pluripotent stem cells. Biochem Biophys Res Commun 425, 321, 2012.
55. Kawamura, M., Miyagawa, S., Miki, K., Saito, A., Fukush-ima, S., Higuchi, T., Kawamura, T., Kuratani, T., Daimon, T., Shimizu, T., Okano, T., and Sawa, Y. Feasibility, safety, and therapeutic efficacy of human induced pluripotent stem cell-derived cardiomyocyte sheets in a porcine ischemic cardio-myopathy model. Circulation 126, S29, 2012.
56. Kensah, G., Roa Lara, A., Dahlmann, J., Zweigerdt, R., Schwanke, K., Hegermann, J., Skvorc, D., Gawol, A., Azizian, A., Wagner, S., Maier, L.S., Krause, A., Drager, G., Ochs, M., Haverich, A., Gruh, I., and Martin, U. Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue in vitro. Eur Heart J 15, 1134, 2013.