A review of cellularization strategies for tissue engineering of whole organs

Frontiers in Bioengineering and Biotechnology

Volumn 3, Issue MAR, 2015, Pages

  Scarritt, Michelle E ^a   Pashos, Nicholas C ^a,b   Bunnell, Bruce A ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TULANE UNIVERSITY   (United States)

Author keywords

Cellularization; Decellularization; Matrices; Native scaffolds; Recellularization; Tissue engineering; Whole organs

Indexed keywords

EID: 85042577683     PISSN: None     EISSN: 22964185     Source Type: Journal    
DOI: 10.3389/fbioe.2015.00043     Document Type: Review

References (149)

1. Adamson, I. Y. (1992). Relationship of mesenchymal changes to alveolar epithelial cell differentiation in fetal rat lung. Anat. Embryol. 185, 275-280. doi:10.1007/BF00211826
2. Akhyari, P., Aubin, H., Gwanmesia, P., Barth, M., Hoffmann, S., Huelsmann, J., et al. (2011). The quest for an optimized protocol for whole-heart decellularization: a comparison of three popular and a novel decellularization technique and their diverse effects on crucial extracellular matrix qualities. Tissue Eng. Part C Methods 17, 915-926. doi:10.1089/ten. TEC.2011.0210
3. Badylak, S. F., Freytes, D. O., and Gilbert, T. W. (2009). Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater. 5, 1-13. doi:10.1016/j.actbio.2008.09.013
4. Badylak, S. F., Taylor, D., and Uygun, K. (2011). Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu. Rev. Biomed. Eng. 13, 27-53. doi:10.1146/annurev-bioeng-071910-124743
5. Bao, J., Shi, Y., Sun, H., Yin, X., Yang, R., Li, L., et al. (2011). Construction of a portal implantable functional tissue-engineered liver using perfusion-decellularized matrix and hepatocytes in rats. Cell Transplant. 20, 753-766. doi:10.3727/096368910X536572
6. Baptista, P. M., Siddiqui, M. M., Lozier, G., Rodriguez, S. R., Atala, A., and Soker, S. (2011). The use of whole organ decellularization for the generation of a vascularized liver organoid. Hepatology 53, 604-617. doi:10.1002/hep.24067
7. Barakat, O., Abbasi, S., Rodriguez, G., Rios, J., Wood, R. P., Ozaki, C., et al. (2012). Use of decellularized porcine liver for engineering humanized liver organ. J. Surg. Res. 173, e11-e25. doi:10.1016/j.jss.2011.09.033
8. Bastian, F., Stelzmuller, M. E., Kratochwill, K., Kasimir, M. T., Simon, P., and Weigel, G. (2008). IgG deposition and activation of the classical complement pathway involvement in the activation of human granulocytes by decellularized porcine heart valve tissue. Biomaterials 29, 1824-1832. doi:10.1016/j.biomaterials.2008.01.005
9. Berger, M. J., Adams, S. D., Tigges, B. M., Sprague, S. L., Wang, X. J., Collins, D. P., et al. (2006). Differentiation of umbilical cord blood-derived multilineage progenitor cells into respiratory epithelial cells. Cytotherapy 8, 480-487. doi:10.1080/14653240600941549
10. Bonandrini, B., Figliuzzi, M., Papadimou, E., Morigi, M., Perico, N., Casiraghi, F., et al. (2014). Recellularization of well-preserved acellular kidney scaffold using embryonic stem cells. Tissue Eng. Part A 20, 1486-1498. doi:10.1089/ten. TEA.2013.0269
11. Bonenfant, N. R., Sokocevic, D., Wagner, D. E., Borg, Z. D., Lathrop, M. J., Lam, Y. W., et al. (2013). The effects of storage and sterilization on de-cellularized and re-cellularized whole lung. Biomaterials 34, 3231-3245. doi:10.1016/j.biomaterials.2013.01.031
12. Bonvillain, R. W., Danchuk, S., Sullivan, D. E., Betancourt, A. M., Semon, J. A., Eagle, M. E., et al. (2012). A nonhuman primate model of lung regeneration: detergent-mediated decellularization and initial in vitro recellularization with mesenchymal stem cells. Tissue Eng. Part A 18, 2437-2452. doi:10.1089/ten. TEA.2011.0594
13. Bonvillain, R. W., Scarritt, M. E., Pashos, N. C., Mayeux, J. P., Meshberger, C. L., Betancourt, A. M., et al. (2013). Nonhuman primate lung decellularization and recellularization using a specialized large-organ bioreactor. J. Vis. Exp. 82, e50825. doi:10.3791/50825
14. Booth, A. J., Hadley, R., Cornett, A. M., Dreffs, A. A., Matthes, S. A., Tsui, J. L., et al. (2012). Acellular normal and fibrotic human lung matrices as a culture system for in vitro investigation. Am. J. Respir. Crit. Care Med. 186, 866-876. doi:10.1164/rccm.201204-0754OC
15. Bourin, P., Bunnell, B. A., Casteilla, L., Dominici, M., Katz, A. J., March, K. L., et al. (2013). Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the international federation for adipose therapeutics and science (IFATS) and the international society for cellular therapy (ISCT). Cytotherapy 15, 641-648. doi:10.1016/j.jcyt.2013.02.006
16. Burke, J. F., Yannas, I. V., Quinby, W. C. Jr., Bondoc, C. C., and Jung, W. K. (1981). Successful use of a physiologically acceptable artificial skin in the treatment of extensive burn injury. Ann. Surg. 194, 413-428. doi:10.1097/00000658-198110000-00005
17. Calle, E. A., Petersen, T. H., and Niklason, L. E. (2011). Procedure for lung engineering. J. Vis. Exp. 49, 2651. doi:10.3791/2651
18. Caralt, M., Uzarski, J. S., Iacob, S., Obergfell, K. P., Berg, N., Bijonowski, B. M., et al. (2015). Optimization and critical evaluation of decellularization strategies to develop renal extracellular matrix scaffolds as biological templates for organ engineering and transplantation. Am. J. Transplant. 15, 64-75. doi:10.1111/ajt.12999
19. Caralt, M., Velasco, E., Lanas, A., and Baptista, P. M. (2014). Liver bioengineering: from the stage of liver decellularized matrix to the multiple cellular actors and bioreactor special effects. Organogenesis 10, 250-259. doi:10.4161/org.29892
20. Cebotari, S., Tudorache, I., Ciubotaru, A., Boethig, D., Sarikouch, S., Goerler, A., et al. (2011). Use of fresh decellularized allografts for pulmonary valve replacement may reduce the reoperation rate in children and young adults: early report. Circulation 124(11 Suppl.), S115-S123. doi:10.1161/CIRCULATIONAHA.110.012161
21. Cicha, I., Ruffer, A., Cesnjevar, R., Glockler, M., Agaimy, A., Daniel, W. G., et al. (2011). Early obstruction of decellularized xenogenic valves in pediatric patients: involvement of inflammatory and fibroproliferative processes. Cardiovasc. Pathol. 20, 222-231. doi:10.1016/j.carpath.2010.04.006
22. Clause, K. C., Liu, L. J., and Tobita, K. (2010). Directed stem cell differentiation: the role of physical forces. Cell Commun. Adhes. 17, 48-54. doi:10.3109/15419061.2010.492535
23. Cooper, D. K., Koren, E., and Oriol, R. (1994). Oligosaccharides and discordant xenotransplantation. Immunol. Rev. 141, 31-58. doi:10.1111/j.1600-065X.1994.tb00871.x
24. Cortiella, J., Niles, J., Cantu, A., Brettler, A., Pham, A., Vargas, G., et al. (2010). Influence of acellular natural lung matrix on murine embryonic stem cell differentiation and tissue formation. Tissue Eng. Part A 16, 2565-2580. doi:10.1089/ten.tea.2009.0730
25. Craft, R. O., and May, J. W. Jr. (2011). Staged nipple reconstruction with vascularized SurgiMend acellular dermal matrix. Plast. Reconstr. Surg. 127, 148e-149e. doi:10.1097/PRS.0b013e3182131e74
26. Crapo, P. M., Gilbert, T. W., and Badylak, S. F. (2011). An overview of tissue and whole organ decellularization processes. Biomaterials 32, 3233-3243. doi:10.1016/j.biomaterials.2011.01.057
27. Crawford, B., Koshy, S. T., Jhamb, G., Woodford, C., Thompson, C. M., Levy, A. S., et al. (2012). Cardiac decellularization with long-term storage and repopulation with canine peripheral blood progenitor cells. Can. J. Chem. Eng. 90, 1457-1464. doi:10.1002/cjce.20670
28. Dalmasso, A. P., Vercellotti, G. M., Fischel, R. J., Bolman, R. M., Bach, F. H., and Platt, J. L. (1992). Mechanism of complement activation in the hyperacute rejection of porcine organs transplanted into primate recipients. Am. J. Pathol. 140, 1157-1166.
29. Daly, A. B., Wallis, J. M., Borg, Z. D., Bonvillain, R. W., Deng, B., Ballif, B. A., et al. (2011). Initial binding and recellularization of decellularized mouse lung scaffolds with bone marrow-derived mesenchymal stromal cells. Tissue Eng. Part A 18, 1-16. doi:10.1089/ten. TEA.2011.0301
30. Dohmen, P. M. (2012). Clinical results of implanted tissue engineered heart valves. HSR Proc. Intensive Care Cardiovasc. Anesth. 4, 225-231.
31. Eitan, Y., Sarig, U., Dahan, N., and Machluf, M. (2010). Acellular cardiac extracellular matrix as a scaffold for tissue engineering: in vitro cell support, remodeling, and biocompatibility. Tissue Eng. Part C Methods 16, 671-683. doi:10.1089/ten. TEC.2009.0111
32. Engler, A. J., Sen, S., Sweeney, H. L., and Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689. doi:10.1016/j.cell.2006.06.044
33. Engler, A. J., Sweeney, H. L., Discher, D. E., and Schwarzbauer, J. E. (2007). Extracellular matrix elasticity directs stem cell differentiation. J. Musculoskelet. Neuronal. Interact. 7, 335.
34. Folkman, J., and Hochberg, M. (1973). Self-regulation of growth in three dimensions. J. Exp. Med. 138, 745-753. doi:10.1084/jem.138.4.745
35. Frith, J. E., Mills, R. J., Hudson, J. E., and Cooper-White, J. J. (2012). Tailored integrin-extracellular matrix interactions to direct human mesenchymal stem cell differentiation. Stem Cells Dev. 21, 2442-2456. doi:10.1089/scd.2011.0615
36. Galili, U., Macher, B. A., Buehler, J., and Shohet, S. B. (1985). Human natural anti-alpha-galactosyl IgG. II. The specific recognition of alpha (1-3)-linked galactose residues. J. Exp. Med. 162, 573-582. doi:10.1084/jem.162.2.573
37. Galili, U., Rachmilewitz, E. A., Peleg, A., and Flechner, I. (1984). A unique natural human IgG antibody with anti-alpha-galactosyl specificity. J. Exp. Med. 160, 1519-1531. doi:10.1084/jem.160.5.1519
38. Galili, U., Shohet, S. B., Kobrin, E., Stults, C. L., and Macher, B. A. (1988). Man, apes, and old world monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells. J. Biol. Chem. 263, 17755-17762.
39. Ghaedi, M., Calle, E. A., Mendez, J. J., Gard, A. L., Balestrini, J., Booth, A., et al. (2013). Human iPS cell-derived alveolar epithelium repopulates lung extracellular matrix. J. Clin. Invest. 123, 4950-4962. doi:10.1172/JCI68793
40. Gilbert, T. W. (2012). Strategies for tissue and organ decellularization. J. Cell. Biochem. 113, 2217-2222. doi:10.1002/jcb.24130
41. Gilbert, T. W., Sellaro, T. L., and Badylak, S. F. (2006). Decellularization of tissues and organs. Biomaterials 27, 3675-3683. doi:10.1016/j.biomaterials.2006.02.014
42. Gilpin, S. E., Guyette, J. P., Gonzalez, G., Ren, X., Asara, J. M., Mathisen, D. J., et al. (2014). Perfusion decellularization of human and porcine lungs: bringing the matrix to clinical scale. J. Heart Lung Transplant. 33, 298-308. doi:10.1016/j.healun.2013.10.030
43. Gimble, J. M., Bunnell, B. A., Chiu, E. S., and Guilak, F. (2011). Concise review: adipose-derived stromal vascular fraction cells and stem cells: let's not get lost in translation. Stem Cells 29, 749-754. doi:10.1002/stem.629
44. Gimble, J. M., Bunnell, B. A., and Guilak, F. (2012). Human adipose-derived cells: an update on the transition to clinical translation. Regen. Med. 7, 225-235. doi:10.2217/rme.11.119
45. Goh, S. K., Bertera, S., Olsen, P., Candiello, J. E., Halfter, W., Uechi, G., et al. (2013). Perfusion-decellularized pancreas as a natural 3D scaffold for pancreatic tissue and whole organ engineering. Biomaterials 34, 6760-6772. doi:10.1016/j.biomaterials.2013.05.066
46. Gong, Z., and Niklason, L. E. (2011). Use of human mesenchymal stem cells as alternative source of smooth muscle cells in vessel engineering. Methods Mol. Biol. 698, 279-294. doi:10.1007/978-1-60761-999-4_21
47. Griffin, M., Bhandari, R., Hamilton, G., Chan, Y. C., and Powell, J. T. (1993). Alveolar type II cell-fibroblast interactions, synthesis and secretion of surfactant and type I collagen. J. Cell. Sci. 105(Pt 2), 423-432.
48. Guilak, F., Cohen, D. M., Estes, B. T., Gimble, J. M., Liedtke, W., and Chen, C. S. (2009). Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5, 17-26. doi:10.1016/j.stem.2009.06.016
49. Guyette, J. P., Gilpin, S. E., Charest, J. M., Tapias, L. F., Ren, X., and Ott, H. C. (2014). Perfusion decellularization of whole organs. Nat. Protoc. 9, 1451-1468. doi:10.1038/nprot.2014.097
50. Hall, C. W., Liotta, D., and De Bakey, M. E. (1966). Artificial skin. Trans. Am. Soc. Artif. Intern. Organs 12, 340-345.
51. Hoffman, A. M., Paxson, J. A., Mazan, M. R., Davis, A. M., Tyagi, S., Murthy, S., et al. (2011). Lung-derived mesenchymal stromal cell post-transplantation survival, persistence, paracrine expression, and repair of elastase-injured lung. Stem Cells Dev. 20, 1779-1792. doi:10.1089/scd.2011.0105
52. Hulsmann, J., Aubin, H., Kranz, A., Godehardt, E., Munakata, H., Kamiya, H., et al. (2013). A novel customizable modular bioreactor system for whole-heart cultivation under controlled 3D biomechanical stimulation. J. Artif. Organs 16, 294-304. doi:10.1007/s10047-013-0705-5
53. Ismail, S., Samadikuchaksaraei, A., Bishop, A., Polak, J. M., and Mantalaris, A. (2012). Development of a novel three-dimensional, automatable and integrated bioprocess for the differentiation of embryonic stem cells into pulmonary alveolar cells in a rotating vessel bioreactor system. Tissue Eng. Part C Methods 18, 263-272. doi:10.1089/ten. TEC.2011.0299
54. Janis, J. E., O'Neill, A. C., Ahmad, J., Zhong, T., and Hofer, S. O. (2012). Acellular dermal matrices in abdominal wall reconstruction: a systematic review of the current evidence. Plast. Reconstr. Surg. 130(5 Suppl. 2), 183S-193S. doi:10.1097/PRS.0b013e3182605cfc
55. Jensen, T., Roszell, B., Zang, F., Girard, E., Matson, A., Thrall, R., et al. (2012). A rapid lung de-cellularization protocol supports embryonic stem cell differentiation in vitro and following implantation. Tissue Eng. Part C Methods 18, 632-646. doi:10.1089/ten. TEC.2011.0584
56. Ji, R., Zhang, N., You, N., Li, Q., Liu, W., Jiang, N., et al. (2012). The differentiation of MSCs into functional hepatocyte-like cells in a liver biomatrix scaffold and their transplantation into liver-fibrotic mice. Biomaterials 33, 8995-9008. doi:10.1016/j.biomaterials.2012.08.058
57. Jiang, W. C., Cheng, Y. H., Yen, M. H., Chang, Y., Yang, V. W., and Lee, O. K. (2014). Cryo-chemical decellularization of the whole liver for mesenchymal stem cells-based functional hepatic tissue engineering. Biomaterials 35, 3607-3617. doi:10.1016/j.biomaterials.2014.01.024
58. Kadota, Y., Yagi, H., Inomata, K., Matsubara, K., Hibi, T., Abe, Y., et al. (2014). Mesenchymal stem cells support hepatocyte function in engineered liver grafts. Organogenesis 10, 268-277. doi:10.4161/org.27879
59. Kajbafzadeh, A. M., Sabetkish, N., Sabetkish, S., Tavangar, S., Beigi, R. H., Talebi, M., et al. (2014). Lung tissue engineering and preservation of alveolar microstructure using a novel casting method. Biotech. Histochem. 90, 111-123. doi:10.3109/10520295.2014.957724
60. Kallenbach, K., Leyh, R. G., Lefik, E., Walles, T., Wilhelmi, M., Cebotari, S., et al. (2004). Guided tissue regeneration: porcine matrix does not transmit PERV. Biomaterials 25, 3613-3620. doi:10.1016/j.biomaterials.2003.10.040
61. Kasimir, M. T., Rieder, E., Seebacher, G., Nigisch, A., Dekan, B., Wolner, E., et al. (2006). Decellularization does not eliminate thrombogenicity and inflammatory stimulation in tissue-engineered porcine heart valves. J. Heart Valve Dis. 15, 278-286.
62. Keane, T. J., Londono, R., Turner, N. J., and Badylak, S. F. (2012). Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 33, 1771-1781. doi:10.1016/j.biomaterials.2011.10.054
63. Lama, V. N., Smith, L., Badri, L., Flint, A., Andrei, A. C., Murray, S., et al. (2007). Evidence for tissue-resident mesenchymal stem cells in human adult lung from studies of transplanted allografts. J. Clin. Invest. 117, 989-996. doi:10.1172/JCI29713
64. Lawrence, B. J., Devarapalli, M., and Madihally, S. V. (2009). Flow dynamics in bioreactors containing tissue engineering scaffolds. Biotechnol. Bioeng. 102, 935-947. doi:10.1002/bit.22106
65. Le Bas-Bernardet, S., Tillou, X., Poirier, N., Dilek, N., Chatelais, M., Devalliere, J., et al. (2011). Xenotransplantation of galactosyl-transferase knockout, CD55, CD59, CD39, and fucosyl-transferase transgenic pig kidneys into baboons. Transplant. Proc. 43, 3426-3430. doi:10.1016/j.transproceed.2011.09.024
66. Lecht, S., Stabler, C. T., Rylander, A. L., Chiaverelli, R., Schulman, E. S., Marcinkiewicz, C., et al. (2014). Enhanced reseeding of decellularized rodent lungs with mouse embryonic stem cells. Biomaterials 35, 3252-3262. doi:10.1016/j.biomaterials.2013.12.093
67. Levenberg, S., Rouwkema, J., Macdonald, M., Garfein, E. S., Kohane, D. S., Darland, D. C., et al. (2005). Engineering vascularized skeletal muscle tissue. Nat. Biotechnol. 23, 879-884. doi:10.1038/nbt1109
68. Lichtenberg, A., Cebotari, S., Tudorache, I., Sturz, G., Winterhalter, M., Hilfiker, A., et al. (2006). Flow-dependent re-endothelialization of tissue-engineered heart valves. J. Heart Valve Dis. 15, 287-293.
69. Liu, J. Y., Swartz, D. D., Peng, H. F., Gugino, S. F., Russell, J. A., and Andreadis, S. T. (2007). Functional tissue-engineered blood vessels from bone marrow progenitor cells. Cardiovasc. Res. 75, 618-628. doi:10.1016/j.cardiores.2007.04.018
70. Lozito, T. P., Kuo, C. K., Taboas, J. M., and Tuan, R. S. (2009a). Human mesenchymal stem cells express vascular cell phenotypes upon interaction with endothelial cell matrix. J. Cell. Biochem. 107, 714-722. doi:10.1002/jcb.22167
71. Lozito, T. P., Taboas, J. M., Kuo, C. K., and Tuan, R. S. (2009b). Mesenchymal stem cell modification of endothelial matrix regulates their vascular differentiation. J. Cell. Biochem. 107, 706-713. doi:10.1002/jcb.22166
72. Lu, T. Y., Lin, B., Kim, J., Sullivan, M., Tobita, K., Salama, G., et al. (2013). Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells. Nat. Commun. 4, 2307. doi:10.1038/ncomms3307
73. Lwebuga-Mukasa, J. S., Ingbar, D. H., and Madri, J. A. (1986). Repopulation of a human alveolar matrix by adult rat type II pneumocytes in vitro. A novel system for type II pneumocyte culture. Exp. Cell Res. 162, 423-435. doi:10.1016/0014-4827(86)90347-2
74. Marra, K. G., Brayfield, C. A., and Rubin, J. P. (2011). Adipose stem cell differentiation into smooth muscle cells. Methods Mol. Biol. 702, 261-268. doi:10.1007/978-1-61737-960-4_19
75. Mendez, J. J., Ghaedi, M., Steinbacher, D., and Niklason, L. (2014). Epithelial cell differentiation of human mesenchymal stromal cells in decellularized lung scaffolds. Tissue Eng. Part A 20, 1735-1746. doi:10.1089/ten. TEA.2013.0647
76. Merna, N., Robertson, C., La, A., and George, S. C. (2013). Optical imaging predicts mechanical properties during decellularization of cardiac tissue. Tissue Eng. Part C Methods 19, 802-809. doi:10.1089/ten. TEC.2012.0720
77. Mirmalek-Sani, S. H., Orlando, G., McQuilling, J. P., Pareta, R., Mack, D. L., Salvatori, M., et al. (2013a). Porcine pancreas extracellular matrix as a platform for endocrine pancreas bioengineering. Biomaterials 34, 5488-5495. doi:10.1016/j.biomaterials.2013.03.054
78. Mirmalek-Sani, S. H., Sullivan, D. C., Zimmerman, C., Shupe, T. D., and Petersen, B. E. (2013b). Immunogenicity of decellularized porcine liver for bioengineered hepatic tissue. Am. J. Pathol. 183, 558-565. doi:10.1016/j.ajpath.2013.05.002
79. Moroni, F., and Mirabella, T. (2014). Decellularized matrices for cardiovascular tissue engineering. Am. J. Stem Cells 3, 1-20.
80. Nagao, R. J., Ouyang, Y., Keller, R., Lee, C., Suggs, L. J., and Schmidt, C. E. (2013). Preservation of capillary-beds in rat lung tissue using optimized chemical decellularization. J. Mater. Chem. B Mater. Biol. Med. 1, 4801-4808. doi:10.1039/c3tb20640h
81. Nakayama, K. H., Batchelder, C. A., Lee, C. I., and Tarantal, A. F. (2010). Decellularized rhesus monkey kidney as a three-dimensional scaffold for renal tissue engineering. Tissue Eng. Part A 16, 2207-2216. doi:10.1089/ten. TEA.2009.0602
82. Nakayama, K. H., Batchelder, C. A., Lee, C. I., and Tarantal, A. F. (2011). Renal tissue engineering with decellularized rhesus monkey kidneys: age-related differences. Tissue Eng. Part A 17, 2891-2901. doi:10.1089/ten. TEA.2010.0714
83. Nakayama, K. H., Lee, C. C., Batchelder, C. A., and Tarantal, A. F. (2013). Tissue specificity of decellularized rhesus monkey kidney and lung scaffolds. PLoS ONE 8:e64134. doi:10.1371/journal.pone.0064134
84. Neumann, A., Sarikouch, S., Breymann, T., Cebotari, S., Boethig, D., Horke, A., et al. (2014). Early systemic cellular immune response in children and young adults receiving decellularized fresh allografts for pulmonary valve replacement. Tissue Eng. Part A 20, 1003-1011. doi:10.1089/ten. TEA.2013.0316
85. Ng, S. L., Narayanan, K., Gao, S., and Wan, A. C. (2011). Lineage restricted progenitors for the repopulation of decellularized heart. Biomaterials 32, 7571-7580. doi:10.1016/j.biomaterials.2011.06.065
86. Nichols, J. E., Niles, J., Riddle, M., Vargas, G., Schilagard, T., Ma, L., et al. (2013). Production and assessment of decellularized pig and human lung scaffolds. Tissue Eng. Part A 19, 2045-2062. doi:10.1089/ten. TEA.2012.0250
87. Nunes, S. S., Maijub, J. G., Krishnan, L., Ramakrishnan, V. M., Clayton, L. R., Williams, S. K., et al. (2013). Generation of a functional liver tissue mimic using adipose stromal vascular fraction cell-derived vasculatures. Sci. Rep. 3, 2141. doi:10.1038/srep02141
88. Oberwallner, B., Brodarac, A., Choi, Y. H., Saric, T., Anic, P., Morawietz, L., et al. (2014). Preparation of cardiac extracellular matrix scaffolds by decellularization of human myocardium. J. Biomed. Mater. Res. A. 102, 3263-3272. doi:10.1002/jbm.a.35000
89. O'Connor, N. E., Mulliken, J. B., Banks-Schlegel, S., Kehinde, O., and Green, H. (1981). Grafting of burns with cultured epithelium prepared from autologous epidermal cells. Lancet 1, 75-78. doi:10.1016/S0140-6736(81)90006-4
90. O'Neill, J. D., Anfang, R., Anandappa, A., Costa, J., Javidfar, J., Wobma, H. M., et al. (2013). Decellularization of human and porcine lung tissues for pulmonary tissue engineering. Ann. Thorac. Surg. 96, 1046-1055. doi:10.1016/j.athoracsur.2013.04.022
91. Orlando, G., Booth, C., Wang, Z., Totonelli, G., Ross, C. L., Moran, E., et al. (2013). Discarded human kidneys as a source of ECM scaffold for kidney regeneration technologies. Biomaterials 34, 5915-5925. doi:10.1016/j.biomaterials.2013.04.033
92. Orlando, G., Farney, A. C., Iskandar, S. S., Mirmalek-Sani, S. H., Sullivan, D. C., Moran, E., et al. (2012). Production and implantation of renal extracellular matrix scaffolds from porcine kidneys as a platform for renal bioengineering investigations. Ann. Surg. 256, 363-370. doi:10.1097/SLA.0b013e31825a02ab
93. Ott, H. C., Clippinger, B., Conrad, C., Schuetz, C., Pomerantseva, I., Ikonomou, L., et al. (2010). Regeneration and orthotopic transplantation of a bioartificial lung. Nat. Med. 16, 927-933. doi:10.1038/nm.2193
94. Ott, H. C., Matthiesen, T. S., Goh, S. K., Black, L. D., Kren, S. M., Netoff, T. I., et al. (2008). Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 14, 213-221. doi:10.1038/nm1684
95. Palakkan, A. A., Hay, D. C., Anil Kumar, P. R., Kumary, T. V., and Ross, J. A. (2013). Liver tissue engineering and cell sources: issues and challenges. Liver Int. 33, 666-676. doi:10.1111/liv.12134
96. Park, K. M., Park, S. M., Yang, S. R., Hong, S. H., and Woo, H. M. (2013). Preparation of immunogen-reduced and biocompatible extracellular matrices from porcine liver. J. Biosci. Bioeng. 115, 207-215. doi:10.1016/j.jbiosc.2012.08.023
97. Pennesi, G., Scaglione, S., Giannoni, P., and Quarto, R. (2011). Regulatory influence of scaffolds on cell behavior: how cells decode biomaterials. Curr. Pharm. Biotechnol. 12, 151-159. doi:10.2174/138920111794295684
98. Petersen, T. H., Calle, E. A., Colehour, M. B., and Niklason, L. E. (2011). Bioreactor for the long-term culture of lung tissue. Cell Transplant. 20, 1117-1126. doi:10.3727/096368910X544933
99. Petersen, T. H., Calle, E. A., Colehour, M. B., and Niklason, L. E. (2012). Matrix composition and mechanics of decellularized lung scaffolds. Cells Tissues Organs 195, 222-231. doi:10.1159/000324896
100. Petersen, T. H., Calle, E. A., Zhao, L., Lee, E. J., Gui, L., Raredon, M. B., et al. (2010). Tissue-engineered lungs for in vivo implantation. Science 329, 538-541. doi:10.1126/science.1189345
101. Prabha, S., and Verghese, S. (2008). Existence of proviral porcine endogenous retrovirus in fresh and decellularised porcine tissues. Indian J. Med. Microbiol. 26, 228-232. doi:10.4103/0255-0857.42032
102. Price, A. P., England, K. A., Matson, A. M., Blazar, B. R., and Panoskaltsis-Mortari, A. (2010). Development of a decellularized lung bioreactor system for bioengineering the lung: the matrix reloaded. Tissue Eng. Part A 16, 2581-2591. doi:10.1089/ten. TEA.2009.0659
103. Qian, H., Yang, H., Xu, W., Yan, Y., Chen, Q., Zhu, W., et al. (2008). Bone marrow mesenchymal stem cells ameliorate rat acute renal failure by differentiation into renal tubular epithelial-like cells. Int. J. Mol. Med. 22, 325-332. doi:10.3892/ijmm_00000026
104. Reilly, G. C., and Engler, A. J. (2010). Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 43, 55-62. doi:10.1016/j.jbiomech.2009.09.009
105. Remlinger, N. T., Wearden, P. D., and Gilbert, T. W. (2012). Procedure for decellularization of porcine heart by retrograde coronary perfusion. J. Vis. Exp. 70, e50059. doi:10.3791/50059
106. Ren, H., Shi, X., Tao, L., Xiao, J., Han, B., Zhang, Y., et al. (2013). Evaluation of two decellularization methods in the development of a whole-organ decellularized rat liver scaffold. Liver Int. 33, 448-458. doi:10.1111/liv.12088
107. Robertson, M. J., Dries-Devlin, J. L., Kren, S. M., Burchfield, J. S., and Taylor, D. A. (2014). Optimizing recellularization of whole decellularized heart extracellular matrix. PLoS ONE 9:e90406. doi:10.1371/journal.pone.0090406
108. Rochon, M. H., Fradette, J., Fortin, V., Tomasetig, F., Roberge, C. J., Baker, K., et al. (2010). Normal human epithelial cells regulate the size and morphology of tissue-engineered capillaries. Tissue Eng. Part A 16, 1457-1468. doi:10.1089/ten. TEA.2009.0090
109. Ross, E. A., Abrahamson, D. R., St John, P., Clapp, W. L., Williams, M. J., Terada, N., et al. (2012). Mouse stem cells seeded into decellularized rat kidney scaffolds endothelialize and remodel basement membranes. Organogenesis 8, 49-55. doi:10.4161/org.20209
110. Ross, E. A., Williams, M. J., Hamazaki, T., Terada, N., Clapp, W. L., Adin, C., et al. (2009). Embryonic stem cells proliferate and differentiate when seeded into kidney scaffolds. J. Am. Soc. Nephrol. 20, 2338-2347. doi:10.1681/ASN.2008111196
111. Sabetkish, S., Kajbafzadeh, A. M., Sabetkish, N., Khorramirouz, R., Akbarzadeh, A., Seyedian, S. L., et al. (2014). Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix liver scaffolds. J. Biomed. Mater. Res. A. 103, 1498-1508. doi:10.1002/jbm.a.35291
112. Sandrin, M. S., and McKenzie, I. F. (1994). Gal alpha (1,3)Gal, the major xenoantigen(s) recognised in pigs by human natural antibodies. Immunol. Rev. 141, 169-190. doi:10.1111/j.1600-065X.1994.tb00877.x
113. Scalea, J., Hanecamp, I., Robson, S. C., and Yamada, K. (2012). T-cell-mediated immunological barriers to xenotransplantation. Xenotransplantation 19, 23-30. doi:10.1111/j.1399-3089.2011.00687.x
114. Scarritt, M. E., Bonvillain, R. W., Burkett, B. J., Wang, G., Glotser, E. Y., Zhang, Q., et al. (2014). Hypertensive rat lungs retain hallmarks of vascular disease upon decellularization but support the growth of mesenchymal stem cells. Tissue Eng. Part A 20, 1426-1443. doi:10.1089/ten. TEA.2013.0438
115. Schmitt, S., Hendricks, P., Weir, J., Somasundaram, R., Sittampalam, G. S., and Nirmalanandhan, V. S. (2012). Stretching mechanotransduction from the lung to the lab: approaches and physiological relevance in drug discovery. Assay Drug Dev. Technol. 10, 137-147. doi:10.1089/adt.2011.418
116. Scobie, L., and Takeuchi, Y. (2009). Porcine endogenous retrovirus and other viruses in xenotransplantation. Curr. Opin. Organ Transplant 14, 175-179. doi:10.1097/MOT.0b013e328327984d
117. Seaman, B. J., Akbari, S. R., and Davison, S. P. (2012). A novel technique for nipple-areola complex reconstruction: the acellular dermal matrix onlay graft. Plast. Reconstr. Surg. 129, 580e-581e. doi:10.1097/PRS.0b013e3182419c68
118. Shamis, Y., Hasson, E., Soroker, A., Bassat, E., Shimoni, Y., Ziv, T., et al. (2011). Organ-specific scaffolds for in vitro expansion, differentiation, and organization of primary lung cells. Tissue Eng. Part C Methods 17, 861-870. doi:10.1089/ten.tec.2010.0717
119. Shirakigawa, N., Ijima, H., and Takei, T. (2012). Decellularized liver as a practical scaffold with a vascular network template for liver tissue engineering. J. Biosci. Bioeng. 114, 546-551. doi:10.1016/j.jbiosc.2012.05.022
120. Shirakigawa, N., Takei, T., and Ijima, H. (2013). Base structure consisting of an endothelialized vascular-tree network and hepatocytes for whole liver engineering. J. Biosci. Bioeng. 116, 740-745. doi:10.1016/j.jbiosc.2013.05.020
121. Shitrit, S. B., Ramon, Y., and Bertasi, G. (2014). Use of a novel acellular dermal matrix allograft to treat complex trauma wound: a case study. Int. J. Burns Trauma 4, 62-65.
122. Shupe, T., Williams, M., Brown, A., Willenberg, B., and Petersen, B. E. (2010). Method for the decellularization of intact rat liver. Organogenesis 6, 134-136. doi:10.4161/org.6.2.11546
123. Sicari, B. M., Rubin, J. P., Dearth, C. L., Wolf, M. T., Ambrosio, F., Boninger, M., et al. (2014). An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci. Transl. Med. 6, 234ra58. doi:10.1126/scitranslmed.3008085
124. Simon, P., Kasimir, M. T., Seebacher, G., Weigel, G., Ullrich, R., Salzer-Muhar, U., et al. (2003). Early failure of the tissue engineered porcine heart valve SYNERGRAFT in pediatric patients. Eur. J. Cardiothorac. Surg. 23, 1002-1006. doi:10.1016/S1010-7940(03)00094-0
125. Sokocevic, D., Bonenfant, N. R., Wagner, D. E., Borg, Z. D., Lathrop, M. J., Lam, Y. W., et al. (2013). The effect of age and emphysematous and fibrotic injury on the re-cellularization of de-cellularized lungs. Biomaterials 34, 3256-3269. doi:10.1016/j.biomaterials.2013.01.028
126. Song, J. J., Guyette, J. P., Gilpin, S. E., Gonzalez, G., Vacanti, J. P., and Ott, H. C. (2013). Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat. Med. 19, 646-651. doi:10.1038/nm.3154
127. Song, J. J., Kim, S. S., Liu, Z., Madsen, J. C., Mathisen, D. J., Vacanti, J. P., et al. (2011). Enhanced in vivo function of bioartificial lungs in rats. Ann. Thorac. Surg. 92, 998-1005. doi:10.1016/j.athoracsur.2011.05.018
128. Soto-Gutierrez, A., Zhang, L., Medberry, C., Fukumitsu, K., Faulk, D., Jiang, H., et al. (2011). A whole-organ regenerative medicine approach for liver replacement. Tissue Eng. Part C Methods 17, 677-686. doi:10.1089/ten.tec.2010.0698
129. Spira, M., Fissette, J., Hall, C. W., Hardy, S. B., and Gerow, F. J. (1969). Evaluation of synthetic fabrics as artificial skin grafts to experimental burn wounds. J. Biomed. Mater. Res. 3, 213-234. doi:10.1002/jbm.820030203
130. Sullivan, D. C., Mirmalek-Sani, S. H., Deegan, D. B., Baptista, P. M., Aboushwareb, T., Atala, A., et al. (2012). Decellularization methods of porcine kidneys for whole organ engineering using a high-throughput system. Biomaterials 33, 7756-7764. doi:10.1016/j.biomaterials.2012.07.023
131. Toma, C., Pittenger, M. F., Cahill, K. S., Byrne, B. J., and Kessler, P. D. (2002). Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105, 93-98. doi:10.1161/hc0102.101442
132. Tse, J. R., and Engler, A. J. (2011). Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate. PLoS ONE 6:e15978. doi:10.1371/journal.pone.0015978
133. Uygun, B. E., Soto-Gutierrez, A., Yagi, H., Izamis, M. L., Guzzardi, M. A., Shulman, C., et al. (2010). Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat. Med. 16, 814-820. doi:10.1038/nm.2170
134. Wagner, D. E., Bonenfant, N. R., Parsons, C. S., Sokocevic, D., Brooks, E. M., Borg, Z. D., et al. (2014). Comparative decellularization and recellularization of normal versus emphysematous human lungs. Biomaterials 35, 3281-3297. doi:10.1016/j.biomaterials.2013.12.103
135. Wagner, D. E., Bonvillain, R. W., Jensen, T., Girard, E. D., Bunnell, B. A., Finck, C. M., et al. (2013). Can stem cells be used to generate new lungs? Ex vivo lung bioengineering with decellularized whole lung scaffolds. Respirology 18, 895-911. doi:10.1111/resp.12102
136. Wainwright, J. M., Czajka, C. A., Patel, U. B., Freytes, D. O., Tobita, K., Gilbert, T. W., et al. (2010). Preparation of cardiac extracellular matrix from an intact porcine heart. Tissue Eng. Part C Methods 16, 525-532. doi:10.1089/ten. TEC.2009.0392
137. Walldorf, J., Aurich, H., Cai, H., Runge, D., Christ, B., Strom, S. C., et al. (2004). Expanding hepatocytes in vitro before cell transplantation: donor age-dependent proliferative capacity of cultured human hepatocytes. Scand. J. Gastroenterol. 39, 584-593. doi:10.1080/00365520410005586
138. Wallis, J. M., Borg, Z. D., Daly, A. B., Deng, B., Ballif, B. A., Allen, G. B., et al. (2012). Comparative assessment of detergent-based protocols for mouse lung de-cellularization and re-cellularization. Tissue Eng. Part C Methods 18, 420-432. doi:10.1089/ten. TEC.2011.0567
139. Wang, B., Borazjani, A., Tahai, M., de Jongh Curry, A. L., Simionescu, D. T., Guan, J., et al. (2010). Fabrication of cardiac patch with decellularized porcine myocardial scaffold and bone marrow mononuclear cells. J. Biomed. Mater. Res. A. 94, 1100-1110. doi:10.1002/jbm.a.32781
140. Wang, B., Wang, G., To, F., Butler, J. R., Claude, A., McLaughlin, R. M., et al. (2013). Myocardial scaffold-based cardiac tissue engineering: application of coordinated mechanical and electrical stimulations. Langmuir 29, 11109-11117. doi:10.1021/la401702w
141. Wang, G., Bunnell, B. A., Painter, R. G., Quiniones, B. C., Tom, S., Lanson, N. A., et al. (2005). Adult stem cells from bone marrow stroma differentiate into airway epithelial cells: potential therapy for cystic fibrosis. Proc. Natl. Acad. Sci. U.S.A. 102, 186-191. doi:10.1073/pnas.0504161102
142. Wang, X., Cui, J., Zhang, B. Q., Zhang, H., Bi, Y., Kang, Q., et al. (2014). Decellularized liver scaffolds effectively support the proliferation and differentiation of mouse fetal hepatic progenitors. J. Biomed. Mater. Res. A. 102, 1017-1025. doi:10.1002/jbm.a.34764
143. Weymann, A., Patil, N. P., Sabashnikov, A., Jungebluth, P., Korkmaz, S., Li, S., et al. (2014). Bioartificial heart: a human-sized porcine model-the way ahead. PLoS ONE 9:e111591. doi:10.1371/journal.pone.0111591
144. Yagi, H., Fukumitsu, K., Fukuda, K., Kitago, M., Shinoda, M., Obara, H., et al. (2013). Human-scale whole-organ bioengineering for liver transplantation: a regenerative medicine approach. Cell Transplant. 22, 231-242. doi:10.3727/096368912X654939
145. Yoo, D., and Giulivi, A. (2000). Xenotransplantation and the potential risk of xenogeneic transmission of porcine viruses. Can. J. Vet. Res. 64, 193-203.
146. Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920. doi:10.1126/science.1151526
147. Zhang, Y., He, Y., Bharadwaj, S., Hammam, N., Carnagey, K., Myers, R., et al. (2009). Tissue-specific extracellular matrix coatings for the promotion of cell proliferation and maintenance of cell phenotype. Biomaterials 30, 4021-4028. doi:10.1016/j.biomaterials.2009.04.005
148. Zheng, W., Xie, Y., Zhang, W., Wang, D., Ma, W., Wang, Z., et al. (2012). Fluid flow stress induced contraction and re-spread of mesenchymal stem cells: a microfluidic study. Integr. Biol. (Camb) 4, 1102-1111. doi:10.1039/c2ib20094e
149. Zhou, P., Lessa, N., Estrada, D. C., Severson, E. B., Lingala, S., Zern, M. A., et al. (2011). Decellularized liver matrix as a carrier for the transplantation of human fetal and primary hepatocytes in mice. Liver Transpl. 17, 418-427. doi:10.1002/lt.22270