Journal of Biomedicine and Biotechnology
Volume 2010 (2010), Article ID 236147, 12 pages
doi:10.1155/2010/236147
Review Article

Three-Dimensional Culture of Human Embryonic Stem Cell Derived Hepatic Endoderm and Its Role in Bioartificial Liver Construction

Ruchi Sharma, Sebastian Greenhough, Claire N. Medine, and David C. Hay

Medical Research Council Centre for Regenerative Medicine, University of Edinburgh, 49 Little France Crescent, Edinburgh, Scotland EH16 4SB, UK

Received 7 September 2009; Accepted 3 December 2009

Academic Editor: James A. Ross

Copyright © 2010 Ruchi Sharma et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Ramadori, F. Moriconi, I. Malik, and J. Dudas, “Physiology and pathophysiology of liver inflammation, damage and repair,” Journal of Physiology and Pharmacology, vol. 59, supplement 1, pp. 107–117, 2008. View at Scopus
  2. T. E. Starzl and F. G. Lakkis, “The unfinished legacy of liver transplantation: emphasis on immunology,” Hepatology, vol. 43, no. 2, supplement 1, pp. S151–S163, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. F. G. Court, S. A. Wemyss-Holden, A. R. Dennison, and G. J. Maddern, “Bioartificial liver support devices: historical perspectives,” ANZ Journal of Surgery, vol. 73, no. 9, pp. 739–748, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Raia, J. R. Nery, and S. Mies, “Liver transplantation from live donors,” The Lancet, vol. 2, no. 8661, p. 497, 1989. View at Scopus
  5. D. S. Seaman, “Adult living donor liver transplantation: current status,” Journal of Clinical Gastroenterology, vol. 33, no. 2, pp. 97–106, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. R. A. F. M. Chamuleau, T. Deurholt, and R. Hoekstra, “Which are the right cells to be used in a bioartificial liver?” Metabolic Brain Disease, vol. 20, no. 4, pp. 327–335, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. R. K. Verbeeck, “Pharmacokinetics and dosage adjustment in patients with hepatic dysfunction,” European Journal of Clinical Pharmacology, vol. 64, no. 12, pp. 1147–1161, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. E. F. A. Brandon, C. D. Raap, I. Meijerman, J. H. Beijnen, and J. H. M. Schellens, “An update on in vitro test methods in human hepatic drug biotransformation research: pros and cons,” Toxicology and Applied Pharmacology, vol. 189, no. 3, pp. 233–246, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Gebhardt, J. G. Hengstler, D. Müller, et al., “New hepatocyte in vitro systems for drug metabolismml: metabolic capacity and recommendations for application in basic research and drug development, standard operation procedures,” Drug Metabolism Reviews, vol. 35, no. 2-3, pp. 145–213, 2003. View at Scopus
  10. D.-H. Park, C. V. Borlongan, D. J. Eve, and P. R. Sanberg, “The emerging field of cell and tissue engineering,” Medical Science Monitor, vol. 14, no. 11, pp. RA206–RA220, 2008. View at Scopus
  11. G. F. Muschler, C. Nakamoto, and L. G. Griffith, “Engineering principles of clinical cell-based tissue engineering,” Journal of Bone and Joint Surgery. American, vol. 86, no. 7, pp. 1541–1558, 2004. View at Scopus
  12. C. Mason and P. Dunnill, “The strong financial case for regenerative medicine and the regen industry,” Regenerative Medicine, vol. 3, no. 3, pp. 351–363, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. D. Gotthardt, C. Riediger, K. H. Weiss, et al., “Fulminant hepatic failure: etiology and indications for liver transplantation,” Nephrology, Dialysis, Transplantation, vol. 22, supplement 8, pp. viii5–viii8, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. S. A. Khan, N. Shah, R. Williams, and R. Jalan, “Acute liver failure: a review,” Clinics in Liver Disease, vol. 10, no. 2, pp. 239–258, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. S. Sen, R. Williams, and R. Jalan, “The pathophysiological basis of acute-on-chronic liver failure,” Liver, vol. 22, supplement 2, pp. 5–13, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Jalan and R. Williams, “Acute-on-chronic liver failure: pathophysiological basis of therapeutic options,” Blood Purification, vol. 20, no. 3, pp. 252–261, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Jalan, “Acute liver failure: current management and future prospects,” Journal of Hepatology, vol. 42, supplement 1, pp. S115–S123, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. R. Jalan and R. Williams, “Bio-artificial liver support for acute liver failure: should we be using it to treat patients?” Transplantation, vol. 73, no. 2, pp. 165–166, 2002. View at Scopus
  19. R. Jalan and J. Bernuau, “Induction of cerebral hyperemia by ammonia plus endotoxin: does hyperammonemia unlock the blood-brain barrier?” Journal of Hepatology, vol. 47, no. 2, pp. 168–171, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. C. H. C. Dejong, M. C. G. van de Poll, P. B. Soeters, R. Jalan, and S. W. M. Olde Damink, “Aromatic amino acid metabolism during liver failure,” Journal of Nutrition, vol. 137, no. 6, pp. 1579S–1585S, 2007. View at Scopus
  21. J. P. Liu, L. L. Gluud, B. Als-Nielsen, and C. Gluud, “Artificial and bioartificial support systems for liver failure,” Cochrane Database of Systematic Reviews, no. 1, Article ID CD003628, 2004. View at Scopus
  22. L. L. Kjaergard, J. Liu, B. Als-Nielsen, and C. Gluud, “Artificial and bioartificial support systems for acute and acute-on-chronic liver failure: a systematic review,” Journal of the American Medical Association, vol. 289, no. 2, pp. 217–222, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Jalan, S. Sen, C. Steiner, D. Kapoor, A. Alisa, and R. Williams, “Extracorporeal liver support with molecular adsorbents recirculating system in patients with severe acute alcoholic hepatitis,” Journal of Hepatology, vol. 38, no. 1, pp. 24–31, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. W. Laleman, A. Wilmer, P. Evenepoel, et al., “Effect of the molecular adsorbent recirculating system and Prometheus devices on systemic haemodynamics and vasoactive agents in patients with acute-on-chronic alcoholic liver failure,” Critical Care, vol. 10, no. 4, article R108, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. V. Stadlbauer, P. Krisper, R. Aigner, et al., “Effect of extracorporeal liver support by MARS and Prometheus on serum cytokines in acute-on-chronic liver failure,” Critical Care, vol. 10, article R169, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. A. Sgroi, V. Serre-Beinier, P. Morel, and L. Bühler, “What clinical alternatives to whole liver transplantation? Current status of artificial devices and hepatocyte transplantation,” Transplantation, vol. 87, no. 4, pp. 457–466, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. N. Kobayashi, “Life support of artificial liver: development of a bioartificial liver to treat liver failure,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 16, no. 2, pp. 113–117, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. M. P. van de Kerkhove, R. Hoekstra, R. A. F. M. Chamuleau, and T. M. van Gulik, “Clinical application of bioartificial liver support systems,” Annals of Surgery, vol. 240, no. 2, pp. 216–230, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Naruse, “Artificial liver support: future aspects,” Journal of Artificial Organs, vol. 8, no. 2, pp. 71–76, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. I. J. Fox, A. N. Langnas, L. W. Fristoe, et al., “Successful application of extracorporeal liver perfusion: a technology whose time has come,” American Journal of Gastroenterology, vol. 88, no. 11, pp. 1876–1881, 1993. View at Scopus
  31. A. Xiong, T. W. Austin, E. Lagasse, et al., “Isolation of human fetal liver progenitors and their enhanced proliferation by three-dimensional coculture with endothelial cells,” Tissue Engineering Part A, vol. 14, no. 6, pp. 995–1006, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. C.-B. Yu, X.-P. Pan, and L.-J. Li, “Progress in bioreactors of bioartificial livers,” Hepatobiliary and Pancreatic Diseases International, vol. 8, no. 2, pp. 134–140, 2009. View at Scopus
  33. M. P. van de Kerkhove, P. P. C. Poyck, T. Deurholt, R. Hoekstra, R. A. F. M. Chamuleau, and T. M. van Gulik, “Liver support therapy: an overview of the AMC-bioartificial liver research,” Digestive Surgery, vol. 22, no. 4, pp. 254–264, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. J.-H. Frühauf, H. Mertsching, S. Giri, N. R. Frühauf, and A. Bader, “Porcine endogenous retrovirus released bya bioartificial liver infects primary human cells,” Liver International, vol. 29, no. 10, pp. 1553–1561, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. R. A. F. M. Chamuleau, P. P. C. Poyck, and M.-P. van de Kerkhove, “Bioartificial liver: its pros and cons,” Therapeutic Apheresis and Dialysis, vol. 10, no. 2, pp. 168–174, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. A. J. Ellis, R. D. Hughes, J. A. Wendon, et al., “Pilot-controlled trial of the extracorporeal liver assist device in acute liver failure,” Hepatology, vol. 24, no. 6, pp. 1446–1451, 1996. View at Publisher · View at Google Scholar · View at Scopus
  37. V. Racanelli and B. Rehermann, “The liver as an immunological organ,” Hepatology, vol. 43, no. 2, supplement 1, pp. S54–S62, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. D. M. Cross and M. K. Bayliss, “A commentary on the use of hepatocytes in drug metabolism studies during drug discovery and development,” Drug Metabolism Reviews, vol. 32, no. 2, pp. 219–240, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. N. Cheng, E. Wauthier, and L. M. Reid, “Mature human hepatocytes from ex vivo differentiation of alginate-encapsulated hepatoblasts,” Tissue Engineering Part A, vol. 14, no. 1, pp. 1–7, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. I. J. Fox and S. C. Strom, “To be or not to be: generation of hepatocytes from cells outside the liver,” Gastroenterology, vol. 134, no. 3, pp. 878–881, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. P. A. Clavien and R. Graf, “Liver regeneration and platelets,” British Journal of Surgery, vol. 96, no. 9, pp. 965–966, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. J. P. Miranda, S. B. Leite, U. Muller-Vieira, A. Rodrigues, M. J. T. Carrondo, and P. M. Alves, “Towards an extended functional hepatocyte in vitro culture,” Tissue Engineering Part C, vol. 15, no. 2, pp. 157–167, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. E. A. M. Gale, “Lessons from the glitazones: a story of drug development,” The Lancet, vol. 357, no. 9271, pp. 1870–1875, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. J. A. Thomson, J. Itskovitz-Eldor, S. S. Shapiro, et al., “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998. View at Scopus
  45. B. E. Reubinoff, M. F. Pera, C.-Y. Fong, A. Trounson, and A. Bongso, “Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro,” Nature Biotechnology, vol. 18, no. 4, pp. 399–404, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. H. J. Rippon and A. E. Bishop, “Embryonic stem cells,” Cell Proliferation, vol. 37, no. 1, pp. 23–34, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Lavon and N. Benvenisty, “Study of hepatocyte differentiation using embryonic stem cells,” Journal of Cellular Biochemistry, vol. 96, no. 6, pp. 1193–1202, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. J. Itskovitz-Eldor, M. Schuldiner, D. Karsenti, et al., “Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers,” Molecular Medicine, vol. 6, no. 2, pp. 88–95, 2000. View at Scopus
  49. H. Baharvand, S. M. Hashemi, S. K. Ashtiani, and A. Farrokhi, “Differentiation of human embryonic stem cells into hepatocytes in 2D and 3D culture systems in vitro,” International Journal of Developmental Biology, vol. 50, no. 7, pp. 645–652, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. T. Imamura, L. Cui, R. Teng, et al., “Embryonic stem cell-derived embryoid bodies in three-dimensional culture system form hepatocyte-like cells in vitro and in vivo,” Tissue Engineering, vol. 10, no. 11-12, pp. 1716–1724, 2004. View at Scopus
  51. H. Basma, A. Soto-Gutiérrez, G. R. Yannam, et al., “Differentiation and transplantation of human embryonic stem cell-derived hepatocytes,” Gastroenterology, vol. 136, no. 3, pp. 990–999, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. D. C. Hay, D. Zhao, A. Ross, R. Mandalam, J. Lebkowski, and W. Cui, “Direct differentiation of human embryonic stem cells to hepatocyte-like cells exhibiting functional activities,” Cloning and Stem Cells, vol. 9, no. 1, pp. 51–62, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. D. C. Hay, D. Zhao, J. Fletcher, et al., “Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo,” Stem Cells, vol. 26, no. 4, pp. 894–902, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. D. C. Hay, J. Fletcher, C. Payne, et al., “Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 34, pp. 12301–12306, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. J. Fletcher, W. Cui, K. Samuel, et al., “The inhibitory role of stromal cell mesenchyme on human embryonic stem cell hepatocyte differentiation is overcome by Wnt3a treatment,” Cloning and Stem Cells, vol. 10, no. 3, pp. 331–339, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. S. Agarwal, K. L. Holton, and R. Lanza, “Efficient differentiation of functional hepatocytes from human embryonic stem cells,” Stem Cells, vol. 26, no. 5, pp. 1117–1127, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. Y. Duan, A. Catana, Y. Meng, et al., “Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo,” Stem Cells, vol. 25, no. 12, pp. 3058–3068, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. D. M. Dalgetty, C. N. Medine, J. P. Iredale, and D. C. Hay, “Progress and future challenges in stem cell-derived liver technologies,” American Journal of Physiology, vol. 297, no. 2, pp. G241–G248, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. N. Lavon, O. Yanuka, and N. Benvenisty, “Differentiation and isolation of hepatic-like cells from human embryonic stem cells,” Differentiation, vol. 72, no. 5, pp. 230–238, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. L. Rambhatla, C.-P. Chiu, P. Kundu, Y. Peng, and M. K. Carpenter, “Generation of hepatocyte-like cells from human embryonic stem cells,” Cell Transplantation, vol. 12, no. 1, pp. 1–11, 2003. View at Scopus
  61. D. T. Scadden, “The stem-cell niche as an entity of action,” Nature, vol. 441, no. 7097, pp. 1075–1079, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. D. E. Discher, D. J. Mooney, and P. W. Zandstra, “Growth factors, matrices, and forces combine and control stem cells,” Science, vol. 324, no. 5935, pp. 1673–1677, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. A. J. Engler, S. Sen, H. L. Sweeney, and D. E. Discher, “Matrix elasticity directs stem cell lineage specification,” Cell, vol. 126, no. 4, pp. 677–689, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. J. Lee, M. J. Cuddihy, and N. A. Kotov, “Three-dimensional cell culture matrices: state of the art,” Tissue Engineering Part B, vol. 14, no. 1, pp. 61–86, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. A. Abbott, “Biology's new dimension,” Nature, vol. 424, no. 6951, pp. 870–872, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. T. Sun, S. Jackson, J. W. Haycock, and S. MacNeil, “Culture of skin cells in 3D rather than 2D improves their ability to survive exposure to cytotoxic agents,” Journal of Biotechnology, vol. 122, no. 3, pp. 372–381, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. P. S. Amenta and D. Harrison, “Expression and potential role of the extracellular matrix in hepatic ontogenesis: a review,” Microscopy Research and Technique, vol. 39, no. 4, pp. 372–386, 1997. View at Publisher · View at Google Scholar · View at Scopus
  68. J. A. Burdick and G. Vunjak-Novakovic, “Engineered microenvironments for controlled stem cell differentiation,” Tissue Engineering Part A, vol. 15, no. 2, pp. 205–219, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. R. McClelland, E. Wauthier, J. Uronis, and L. Reid, “Gradients in the liver's extracellular matrix chemistry from periportal to pericentral zones: influence on human hepatic progenitors,” Tissue Engineering Part A, vol. 14, no. 1, pp. 59–70, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. S. F. Abu-Absi, J. R. Friend, L. K. Hansen, and W.-S. Hu, “Structural polarity and functional bile canaliculi in rat hepatocyte spheroids,” Experimental Cell Research, vol. 274, no. 1, pp. 56–67, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  71. M. Ohno, K. Motojima, T. Okano, and A. Taniguchi, “Maturation of the extracellular matrix and cell adhesion molecules in layered co-cultures of HepG2 and endothelial cells,” Journal of Biochemistry, vol. 145, no. 5, pp. 591–597, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. S. Ng, Y.-N. Wu, Y. Zhou, et al., “Optimization of 3-D hepatocyte culture by controlling the physical and chemical properties of the extra-cellular matrices,” Biomaterials, vol. 26, no. 16, pp. 3153–3163, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. T. T. Chang and M. Hughes-Fulford, “Monolayer and spheroid culture of human liver hepatocellular carcinoma cell line cells demonstrate distinct global gene expression patterns and functional phenotypes,” Tissue Engineering Part A, vol. 15, no. 3, pp. 559–567, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  74. T. Koyama, T. Ehashi, N. Ohshima, and H. Miyoshi, “Efficient proliferation and maturation of fetal liver cells in three-dimensional culture by stimulation of oncostatin m, epidermal growth factor, and dimethyl sulfoxide,” Tissue Engineering Part A, vol. 15, no. 5, pp. 1099–1107, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  75. L. G. Griffith and G. Naughton, “Tissue engineering—current challenges and expanding opportunities,” Science, vol. 295, no. 5557, pp. 1009–1010, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  76. M. Sokolsky-Papkov, K. Agashi, A. Olaye, K. Shakesheff, and A. J. Domb, “Polymer carriers for drug delivery in tissue engineering,” Advanced Drug Delivery Reviews, vol. 59, no. 4-5, pp. 187–206, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  77. D. Du, K. S. Furukawa, and T. Ushida, “3D culture of osteoblast-like cells by unidirectional or oscillatory flow for bone tissue engineering,” Biotechnology and Bioengineering, vol. 102, no. 6, pp. 1670–1678, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  78. H. Liu and K. Roy, “Biomimetic three-dimensional cultures significantly increase hematopoietic differentiation efficacy of embryonic stem cells,” Tissue Engineering, vol. 11, no. 1-2, pp. 319–330, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  79. D. R. Nisbet, D. Moses, T. R. Gengenbach, J. S. Forsythe, D. I. Finkelstein, and M. K. Horne, “Enhancing neurite outgrowth from primary neurones and neural stem cells using thermoresponsive hydrogel scaffolds for the repair of spinal cord injury,” Journal of Biomedical Materials Research Part A, vol. 89, no. 1, pp. 24–35, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  80. E. Syková, P. Jendelová, L. Urdzíková, P. Lesný, and A. Hejčl, “Bone marrow stem cells and polymer hydrogels—two strategies for spinal cord injury repair,” Cellular and Molecular Neurobiology, vol. 26, no. 7-8, pp. 1113–1129, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  81. N. Cheng, E. Wauthier, and L. M. Reid, “Mature human hepatocytes from ex vivo differentiation of alginate-encapsulated hepatoblasts,” Tissue Engineering Part A, vol. 14, no. 1, pp. 1–7, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  82. T. Elkayam, S. Amitay-Shaprut, M. Dvir-Ginzberg, T. Harel, and S. Cohen, “Enhancing the drug metabolism activities of C3A—a human hepatocyte cell line—by tissue engineering within alginate scaffolds,” Tissue Engineering, vol. 12, no. 5, pp. 1357–1368, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  83. P. Roach, D. Eglin, K. Rohde, and C. C. Perry, “Modern biomaterials: a review—bulk properties and implications of surface modifications,” Journal of Materials Science: Materials in Medicine, vol. 18, no. 7, pp. 1263–1277, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  84. E. Dawson, G. Mapili, K. Erickson, S. Taqvi, and K. Roy, “Biomaterials for stem cell differentiation,” Advanced Drug Delivery Reviews, vol. 60, no. 2, pp. 215–228, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  85. K. Rezwan, Q. Z. Chen, J. J. Blaker, and A. R. Boccaccini, “Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering,” Biomaterials, vol. 27, no. 18, pp. 3413–3431, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  86. W. S. Turner, E. Schmelzer, R. McClelland, E. Wauthier, W. Chen, and L. M. Reid, “Human hepatoblast phenotype maintained by hyaluronan hydrogels,” Journal of Biomedical Materials Research Part B, vol. 82, no. 1, pp. 156–168, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  87. C. J. Bettinger, K. M. Cyr, A. Matsumoto, R. Langer, J. T. Borenstein, and D. L. Kaplan, “Silk fibroin microfluidic devices,” Advanced Materials, vol. 19, no. 19, pp. 2847–2850, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  88. Y. M. Elçin, V. Dixit, and G. Gitnick, “Hepatocyte attachment on biodegradable modified chitosan membranes: in vitro evaluation for the development of liver organoids,” Artificial Organs, vol. 22, no. 10, pp. 837–846, 1998. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Ishii, K. Fukumitsu, K. Yasuchika, et al., “Effects of extracellular matrixes and growth factors on the hepatic differentiation of human embryonic stem cells,” American Journal of Physiology, vol. 295, no. 2, pp. G313–G321, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  90. M. Schug, T. Heise, A. Bauer, et al., “Primary rat hepatocytes as in vitro system for gene expression studies: comparison of sandwich, Matrigel and 2D cultures,” Archives of Toxicology, vol. 82, no. 12, pp. 923–931, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. M. M. Stevens, H. F. Qanadilo, R. Langer, and V. P. Shastri, “A rapid-curing alginate gel systemml: utility in periosteum-derived cartilage tissue engineering,” Biomaterials, vol. 25, no. 5, pp. 887–894, 2004. View at Publisher · View at Google Scholar · View at Scopus
  92. A. D. Augst, H. J. Kong, and D. J. Mooney, “Alginate hydrogels as biomaterials,” Macromolecular Bioscience, vol. 6, no. 8, pp. 623–633, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  93. S. Fang, Y.-D. Qiu, L. Mao, X.-L. Shi, D.-C. Yu, and Y.-T. Ding, “Differentiation of embryoid-body cells derived from embryonic stem cells into hepatocytes in alginate microbeads in vitro,” Acta Pharmacologica Sinica, vol. 28, no. 12, pp. 1924–1930, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  94. J. J. Marler, J. Upton, R. Langer, and J. P. Vacanti, “Transplantation of cells in matrices for tissue regeneration,” Advanced Drug Delivery Reviews, vol. 33, no. 1-2, pp. 165–182, 1998. View at Publisher · View at Google Scholar · View at Scopus
  95. H.-Y. Cheung, K.-T. Lau, T.-P. Lu, and D. Hui, “A critical review on polymer-based bio-engineered materials for scaffold development,” Composites Part B, vol. 38, no. 3, pp. 291–300, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. C. Liu, Z. Xia, and J. T. Czernuszka, “Design and development of three-dimensional scaffolds for tissue engineering,” Chemical Engineering Research and Design, vol. 85, no. 7, pp. 1051–1064, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. M. Kellomäki and P. Törmälä, “Processing of resorbable poly-α-hydroxy acids for use as tissue-engineering scaffolds,” in Biopolymer Methods in Tissue Engineering, A. P. Hollander and P. V. Hatton, Eds., pp. 1–10, Humana Press, Totowa, NJ, USA, 2004.
  98. G. Chan and D. J. Mooney, “New materials for tissue engineering: towards greater control over the biological response,” Trends in Biotechnology, vol. 26, no. 7, pp. 382–392, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  99. H. Huang, S. Hanada, N. Kojima, and Y. Sakai, “Enhanced functional maturation of fetal porcine hepatocytes in three-dimensional poly-L-lactic acid scaffolds: a culture condition suitable for engineered liver tissues in large-scale animal studies,” Cell Transplantation, vol. 15, no. 8-9, pp. 799–809, 2006. View at Scopus
  100. J. L. Jiang, N. Kojima, L. Guo, et al., “Efficacy of engineered liver tissue based on poly-L-lactic acid scaffolds and fetal mouse liver cells cultured with oncostatin M, nicotinamide, and dimethyl sulfoxide,” Tissue Engineering, vol. 10, no. 9-10, pp. 1577–1586, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  101. S. Hanada, N. Kojima, and Y. Sakai, “Soluble factor-dependent in vitro growth and maturation of rat fetal liver cells in a three-dimensional culture system,” Tissue Engineering Part A, vol. 14, no. 1, pp. 149–160, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  102. N.-J. Cho, M. Elazar, A. Xiong, et al., “Viral infection of human progenitor and liver-derived cells encapsulated in three-dimensional PEG-based hydrogel,” Biomedical Materials, vol. 4, no. 1, Article ID 011001, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  103. M. Sokolsky-Papkov, K. Agashi, A. Olaye, K. Shakesheff, and A. J. Domb, “Polymer carriers for drug delivery in tissue engineering,” Advanced Drug Delivery Reviews, vol. 59, no. 4-5, pp. 187–206, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  104. B. D. Ratner and S. J. Bryant, “Biomaterials: where we have been and where we are going,” Annual Review of Biomedical Engineering, vol. 6, pp. 41–75, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  105. J. P. Desai, A. Pillarisetti, and A. D. Brooks, “Engineering approaches to biomanipulation,” Annual Review of Biomedical Engineering, vol. 9, pp. 35–53, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  106. R. J. Zdrahala and I. J. Zdrahala, “Biomedical applications of polyurethanes: a review of past promises, present realities, and a vibrant future,” Journal of Biomaterials Applications, vol. 14, no. 1, pp. 67–90, 1999. View at Scopus
  107. H. Ijima, T. Matsushita, K. Nakazawa, Y. Fujii, and K. Funatsu, “Hepatocyte spheroids in polyurethane foams: functional analysis and application for a hybrid artificial liver,” Tissue Engineering, vol. 4, no. 2, pp. 213–226, 1998. View at Publisher · View at Google Scholar · View at Scopus
  108. H. Ijima, K. Nakazawa, H. Mizumoto, T. Matsushita, and K. Funatsu, “Formation of a spherical multicellular aggregate (spheroid) of animal cells in the pores of polyurethane foam as a cell culture substratum and its application to a hybrid artificial liver,” Journal of Biomaterials Science, Polymer Edition, vol. 9, no. 7, pp. 765–778, 1998. View at Scopus
  109. J. Fukuda, R. Sakiyama, K. Nakazawa, et al., “Mass preparation of primary porcine hepatocytes and the design of a hybrid artificial liver module using spheroid culture for a clinical trial,” International Journal of Artificial Organs, vol. 24, no. 11, pp. 799–806, 2001. View at Scopus
  110. K. Matsumoto, H. Mizumoto, K. Nakazawa, H. Ijima, K. Funatsu, and T. Kajiwara, “Hepatic differentiation of mouse embryonic stem cells in a three-dimensional culture system using polyurethane foam,” Journal of Bioscience and Bioengineering, vol. 105, no. 4, pp. 350–354, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  111. E. S. Place, J. H. George, C. K. Williams, and M. M. Stevens, “Synthetic polymer scaffolds for tissue engineering,” Chemical Society Reviews, vol. 38, no. 4, pp. 1139–1151, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  112. S. C. Baker, G. Rohman, J. Southgate, and N. R. Cameron, “The relationship between the mechanical properties and cell behaviour on PLGA and PCL scaffolds for bladder tissue engineering,” Biomaterials, vol. 30, no. 7, pp. 1321–1328, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  113. D. E. Discher, P. Janmey, and Y.-L. Wang, “Tissue cells feel and respond to the stiffness of their substrate,” Science, vol. 310, no. 5751, pp. 1139–1143, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  114. M. Bokhari, R. J. Carnachan, N. R. Cameron, and S. A. Przyborski, “Novel cell culture device enabling three-dimensional cell growth and improved cell function,” Biochemical and Biophysical Research Communications, vol. 354, no. 4, pp. 1095–1100, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  115. P. Thevenot, W. Hu, and L. Tang, “Surface chemistry influences implant biocompatibility,” Current Topics in Medicinal Chemistry, vol. 8, no. 4, pp. 270–280, 2008. View at Publisher · View at Google Scholar · View at Scopus
  116. P. Thevenot, A. Nair, J. Dey, J. Yang, and L. Tang, “Method to analyze three-dimensional cell distribution and infiltration in degradable scaffolds,” Tissue Engineering Part C, vol. 14, no. 4, pp. 319–331, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  117. M. Dvir-Ginzberg, I. Gamlieli-Bonshtein, R. Agbaria, and S. Cohen, “Liver tissue engineering within alginate scaffolds: effects of cell-seeding density on hepatocyte viability, morphology, and function,” Tissue Engineering, vol. 9, no. 4, pp. 757–766, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  118. H. Shin, S. Jo, and A. G. Mikos, “Biomimetic materials for tissue engineering,” Biomaterials, vol. 24, no. 24, pp. 4353–4364, 2003. View at Publisher · View at Google Scholar · View at Scopus
  119. D. G. Anderson, J. A. Burdick, and R. Langer, “Smart biomaterials,” Science, vol. 305, no. 5692, pp. 1923–1924, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  120. S. Duggal, K. B. Frønsdal, K. Szöke, A. Shahdadfar, J. E. Melvik, and J. E. Brinchmann, “Phenotype and gene expression of human mesenchymal stem cells in alginate scaffolds,” Tissue Engineering Part A, vol. 15, no. 7, pp. 1763–1773, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  121. Y. Du, S.-M. Chia, R. Han, S. Chang, H. Tang, and H. Yu, “3D hepatocyte monolayer on hybrid RGD/galactose substratum,” Biomaterials, vol. 27, no. 33, pp. 5669–5680, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  122. M. P. Lutolf, J. L. Lauer-Fields, H. G. Schmoekel, et al., “Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 9, pp. 5413–5418, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  123. S. Zhang and C. E. Semino, “Design peptide scaffolds for regenerative medicine,” Advances in Experimental Medicine and Biology, vol. 534, pp. 147–163, 2003. View at Scopus
  124. C. E. Semino, J. R. Merok, G. G. Crane, G. Panagiotakos, and S. Zhang, “Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds,” Differentiation, vol. 71, no. 4-5, pp. 262–270, 2003. View at Publisher · View at Google Scholar · View at Scopus
  125. L. Ferreira, J. M. Karp, L. Nobre, and R. Langer, “New opportunities: the use of nanotechnologies to manipulate and track stem cells,” Cell Stem Cell, vol. 3, no. 2, pp. 136–146, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  126. F. Loffredo and R. T. Lee, “Therapeutic vasculogenesis: it takes two,” Circulation Research, vol. 103, no. 2, pp. 128–130, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  127. P. P. C. Poyck, G. Mareels, R. Hoekstra, et al., “Enhanced oxygen availability improves liver-specific functions of the AMC bioartificial liver,” Artificial Organs, vol. 32, no. 2, pp. 116–126, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  128. M. Radisic, H. Park, F. Chen, et al., “Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds,” Tissue Engineering, vol. 12, no. 8, pp. 2077–2091, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  129. S. H. Oh, C. L. Ward, A. Atala, J. J. Yoo, and B. S. Harrison, “Oxygen generating scaffolds for enhancing engineered tissue survival,” Biomaterials, vol. 30, no. 5, pp. 757–762, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  130. J. T. Borenstein, E. J. Weinberg, B. K. Orrick, C. Sundback, M. R. Kaazempur-Mofrad, and J. P. Vacanti, “Microfabrication of three-dimensional engineered scaffolds,” Tissue Engineering, vol. 13, no. 8, pp. 1837–1844, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  131. J. J. Moon, M. S. Hahn, I. Kim, B. A. Nsiah, and J. L. West, “Micropatterning of poly(ethylene glycol) diacrylate hydrogels with biomolecules to regulate and guide endothelial morphogenesis,” Tissue Engineering Part A, vol. 15, no. 3, pp. 579–585, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  132. J. J. Moon and J. L. West, “Vascularization of engineered tissues: approaches to promote angiogenesis in biomaterials,” Current Topics in Medicinal Chemistry, vol. 8, no. 4, pp. 300–310, 2008. View at Publisher · View at Google Scholar · View at Scopus
  133. A. Carraro, W.-M. Hsu, K. M. Kulig, et al., “In vitro analysis of a hepatic device with intrinsic microvascular-based channels,” Biomedical Microdevices, vol. 10, no. 6, pp. 795–805, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus