Liver tissue engineering: promises and prospects of new technology

References

• Khanna A, Jain A, Eghtesad B, Rakela J. Liver transplantation for metabolic liver diseases. Surg Clin North Am. 1999; 79: 153–62, ix.
   Google Scholar
• Dodson SF, Issa S, Bonham A. Liver transplantation for chronic viral hepatitis. Surg Clin North Am. 1999;79: 131–45.
   Google Scholar
• Shaw BW Jr. Transplantation in the elderly patient. Surg Clin North Am. 1994;74:389–400.
   Google Scholar
• Fiegel HC, Kaufmann PM, Bruns H, Kluth D, Horch RE, Vacanti JP, . Hepatic tissue engineering: from transplantation to customized cell-based liver directed therapies from the laboratory. J Cell Mol Med. 2008;12:56–66.
   Google Scholar
• Torok E, Pollok JM, Ma PX, Kaufmann PM, Dandri M, Petersen J, . Optimization of hepatocyte spheroid formation for hepatic tissue engineering on three-dimensional biodegradable polymer within a flow bioreactor prior to implantation. Cells Tissues Organs. 2001;169:34–41.
   Google Scholar
• Mooney DJ, Sano K, Kaufmann PM, Majahod K, Schloo B, Vacanti JP, . Long-term engraftment of hepatocytes transplanted on biodegradable polymer sponges. J Biomed Mater Res. 1997;37:413–20.
   PubMed Web of Science ®Google Scholar
• Ouyang EC, Wu CH, Walton C, Promrat K, Wu GY. Transplantation of human hepatocytes into tolerized genetically immunocompetent rats. World J Gastroenterol. 2001;7:324–30.
   PubMed Web of Science ®Google Scholar
• Seppen J, Filali EE, Elferink RO. Small animal models of hepatocyte transplantation. Methods Mol Biol. 2009;481:75–82.
   Google Scholar
• Weber A, Groyer-Picard MT, Dagher I. Hepatocyte transplantation techniques: large animal models. Methods Mol Biol. 2009;481:83–96.
   Google Scholar
• Kulig KM, Vacanti JP. Hepatic tissue engineering. Transpl Immunol. 2004;12:303–10.
   PubMed Web of Science ®Google Scholar
• Zhao Q, Ren H, Li X, Chen Z, Zhang X, Gong W, . Differentiation of human umbilical cord mesenchymal stromal cells into low immunogenic hepatocyte-like cells. Cytotherapy. 2009;11:414–26.
   PubMed Web of Science ®Google Scholar
• Shi XL, Qiu YD, Wu XY, Xie T, Zhu ZH, Chen LL, . In vitro differentiation of mouse bone marrow mononuclear cells into hepatocyte-like cells. Hepatol Res. 2005;31:223–31.
   Google Scholar
• Zhang YN, Lie PC, Wei X. Differentiation of mesenchymal stromal cells derived from umbilical cord Wharton's jelly into hepatocyte-like cells. Cytotherapy. 2009;11:548–58.
   PubMed Web of Science ®Google Scholar
• Sell S. Heterogeneity and plasticity of hepatocyte lineage cells. Hepatology. 2001;33:738–50.
   PubMed Web of Science ®Google Scholar
• Kang YH, Berthiaume F, Nath BD, Yarmush ML. Growth factors and nonparenchymal cell conditioned media induce mitogenic responses in stable long-term adult rat hepatocyte cultures. Exp Cell Res. 2004;293:239–47.
   PubMed Web of Science ®Google Scholar
• Mizuguchi T, Hui T, Palm K, Sugiyama N, Mitaka T, Demetriou AA, . Enhanced proliferation and differentiation of rat hepatocytes cultured with bone marrow stromal cells. J Cell Physiol. 2001;189:106–19.
   PubMed Web of Science ®Google Scholar
• Uyama N, Shimahara Y, Kawada N, Seki S, Okuyama H, Iimuro Y, . Regulation of cultured rat hepatocyte proliferation by stellate cells. J Hepatol. 2002;36:590–9.
   PubMed Web of Science ®Google Scholar
• Cho CH, Berthiaume F, Tilles AW, Yarmush ML. A new technique for primary hepatocyte expansion in vitro. Biotechnol Bioeng. 2008;101:345–56.
   PubMed Web of Science ®Google Scholar
• Shiojiri N, Lemire JM, Fausto N. Cell lineages and oval cell progenitors in rat liver development. Cancer Res. 1991;51:2611–20.
   PubMed Web of Science ®Google Scholar
• Evarts RP, Nagy P, Marsden E, Thorgeirsson SS. A precursor–product relationship exists between oval cells and hepatocytes in rat liver. Carcinogenesis. 1987;8:1737–40.
   PubMed Web of Science ®Google Scholar
• Evarts RP, Nagy P, Nakatsukasa H, Marsden E, Thorgeirsson SS. In vivo differentiation of rat liver oval cells into hepatocytes. Cancer Res. 1989;49:1541–7.
   PubMed Web of Science ®Google Scholar
• Qian Y, Lin Z, Chen J, Fan Y, Davey T, Cake M, . Natural bone collagen scaffold combined with autologous enriched bone marrow cells for induction of osteogenesis in an ovine spinal fusion model. Tissue Eng Part A. 2009;15:3547–58.
   PubMed Web of Science ®Google Scholar
• Sell S. The role of progenitor cells in repair of liver injury and in liver transplantation. Wound Repair Regen. 2001;9:467–82.
   Google Scholar
• Oh SH, Hatch HM, Petersen BE. Hepatic oval ‘stem’ cell in liver regeneration. Semin Cell Dev Biol. 2002;13:405–9.
   PubMed Web of Science ®Google Scholar
• Singh AK, Pancholi N, Patel J, Litbarg NO, Gudehithlu KP, Sethupathi P, . Omentum facilitates liver regeneration. World J Gastroenterol. 2009;15:1057–64.
   PubMed Web of Science ®Google Scholar
• Wang P, Liu T, Cong M, Wu X, Bai Y, Yin C, . Expression of extracellular matrix genes in cultured hepatic oval cells: an origin of hepatic stellate cells through transforming growth factor beta? Liver Int. 2009;29:575–84.
   Google Scholar
• Mitaka T, Mizuguchi T, Sato F, Mochizuki C, Mochizuki Y. Growth and maturation of small hepatocytes. J Gastroenterol Hepatol. 1998;13(Suppl):S70–7.
   Google Scholar
• Gordon GJ, Butz GM, Grisham JW, Coleman WB. Isolation, short-term culture, and transplantation of small hepatocyte-like progenitor cells from retrorsine-exposed rats. Transplantation. 2002;73:1236–43.
   Google Scholar
• Best DH, Coleman WB. Treatment with 2-AAF blocks the small hepatocyte-like progenitor cell response in retrorsine-exposed rats. J Hepatol. 2007;46:1055–63.
   PubMed Web of Science ®Google Scholar
• Shibata C, Mizuguchi T, Kikkawa Y, Nobuoka T, Oshima H, Kawasaki H, . Liver repopulation and long-term function of rat small hepatocyte transplantation as an alternative cell source for hepatocyte transplantation. Liver Transpl. 2006;12:78–87.
   PubMed Web of Science ®Google Scholar
• Ikeda S, Mitaka T, Harada K, Sugimoto S, Hirata K, Mochizuki Y. Proliferation of rat small hepatocytes after long-term cryopreservation. J Hepatol. 2002;37:7–14.
   PubMed Web of Science ®Google Scholar
• Kobayashi N, Miyazaki M, Fukaya K, Inoue Y, Sakaguchi M, Noguchi H, . Treatment of surgically induced acute liver failure with transplantation of highly differentiated immortalized human hepatocytes. Cell Transplant. 2000;9:733–5.
   Google Scholar
• Inoue Y, Miyazaki M, Tsuji T, Sakaguchi M, Fukaya K, Huh NH, . Reactivation of liver-specific gene expression in an immortalized human hepatocyte cell line by introduction of the human HNF4alpha2 gene. Int J Mol Med. 2001;8:481–7.
   PubMed Web of Science ®Google Scholar
• Ito M, Ito R, Yoshihara D, Ikeno M, Kamiya M, Suzuki N, . Immortalized hepatocytes using human artificial chromo-some. Cell Transplant. 2008;17:165–71.
   Google Scholar
• Ito M, Ikeno M, Nagata H, Yamamoto T, Hiroguchi A, Fox IJ, . Treatment of nonalbumin rats by transplantation of immortalized hepatocytes using artificial human chromosome. Transplant Proc. 2009;41:422–4.
   Google Scholar
• Lim PL, Tan W, Latchoumycandane C, Mok WC, Khoo YM, Lee HS, . Molecular and functional characterization of drug-metabolizing enzymes and transporter expression in the novel spontaneously immortalized human hepatocyte line HC-04. Toxicol In Vitro. 2007;21:1390–401.
   PubMed Web of Science ®Google Scholar
• Wege H, Chui MS, Le HT, Strom SC, Zern MA. In vitro expansion of human hepatocytes is restricted by telo-mere-dependent replicative aging. Cell Transplant. 2003;12:897–906.
   Google Scholar
• Wege H, Le HT, Chui MS, Liu L, Wu J, Giri R, . Telomerase reconstitution immortalizes human fetal hepatocytes without disrupting their differentiation potential. Gastroenterology. 2003;124:432–44.
   PubMed Web of Science ®Google Scholar
• Matsumura T, Takesue M, Westerman KA, Okitsu T, Sakaguchi M, Fukazawa T, . Establishment of an immortalized human-liver endothelial cell line with SV40T and hTERT. Transplantation. 2004;77:1357–65.
   PubMedGoogle Scholar
• Watanabe T, Shibata N, Westerman KA, Okitsu T, Allain JE, Sakaguchi M, . Establishment of immortalized human hepatic stellate scavenger cells to develop bioartificial livers. Transplantation. 2003;75:1873–80.
   PubMed Web of Science ®Google Scholar
• Delgado JP, Parouchev A, Allain JE, Pennarun G, Gauthier LR, Dutrillaux AM, . Long-term controlled immortalization of a primate hepatic progenitor cell line after Simian virus 40 T-Antigen gene transfer. Oncogene. 2005;24:541–51.
   Google Scholar
• Kobayashi N, Fujiwara T, Westerman KA, Inoue Y, Sakaguchi M, Noguchi H, . Prevention of acute liver failure in rats with reversibly immortalized human hepatocytes. Science. 2000;287:1258–62.
   PubMed Web of Science ®Google Scholar
• Kobayashi N. Life support of artificial liver: development of a bioartificial liver to treat liver failure. J Hepatobil Pancreat Surg. 2009;16:113–7.
   PubMedGoogle Scholar
• Friedenstein AJ, Chailakhyan RK, Gerasimov UV. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet. 1987;20:263–72.
   PubMedGoogle Scholar
• Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, . Bone marrow as a potential source of hepatic oval cells. Science. 1999;284:1168–70.
   PubMed Web of Science ®Google Scholar
• Theise ND, Nimmakayalu M, Gardner R, Illei PB, Morgan G, Teperman L, . Liver from bone marrow in humans. Hepatology. 2000;32:11–6.
   PubMed Web of Science ®Google Scholar
• Oh SH, Miyazaki M, Kouchi H, Inoue Y, Sakaguchi M, Tsuji T, . Hepatocyte growth factor induces differentiation of adult rat bone marrow cells into a hepatocyte lineage in vitro. Biochem Biophys Res Commun. 2000;279:500–4.
   PubMed Web of Science ®Google Scholar
• Schwartz RE, Reyes M, Koodie L, Jiang Y, Blackstad M, Lund T, . Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest. 2002;109:1291–302.
   PubMed Web of Science ®Google Scholar
• Kazemnejad S, Allameh A, Soleimani M, Gharehbaghian A, Mohammadi Y, Amirizadeh N, . Biochemical and molecular characterization of hepatocyte-like cells derived from human bone marrow mesenchymal stem cells on a novel three-dimensional biocompatible nanofibrous scaffold. J Gastroenterol Hepatol. 2009;24:278–87.
   PubMed Web of Science ®Google Scholar
• Gu J, Shi X, Zhang Y, Chu X, Hang H, Ding Y. Establishment of a three-dimensional co-culture system by porcine hepatocytes and bone marrow mesenchymal stem cells in vitro. Hepatol Res. 2009;39:398–407.
   Google Scholar
• Gu J, Shi X, Zhang Y, Ding Y. Heterotypic interactions in the preservation of morphology and functionality of porcine hepatocytes by bone marrow mesenchymal stem cells in vitro. J Cell Physiol. 2009;219:100–8.
   Google Scholar
• Keller GM. In vitro differentiation of embryonic stem cells. Curr Opin Cell Biol. 1995;7:862–9.
   PubMed Web of Science ®Google Scholar
• Odorico JS, Kaufman DS, Thomson JA. Multilineage differentiation from human embryonic stem cell lines. Stem Cells. 2001;19:193–204.
   PubMed Web of Science ®Google Scholar
• Park J, Cho CH, Parashurama N, Li Y, Berthiaume F, Toner M, . Microfabrication-based modulation of embryonic stem cell differentiation. Lab Chip. 2007;7:1018–28.
   PubMed Web of Science ®Google Scholar
• Soto-Gutierrez A, Navarro-Alvarez N, Zhao D, Rivas-Carrillo JD, Lebkowski J, Tanaka N, . Differentiation of mouse embryonic stem cells to hepatocyte-like cells by co-culture with human liver nonparenchymal cell lines. Nat Protoc. 2007;2:347–56.
   PubMedGoogle Scholar
• Kuai XL, Cong XQ, Li XL, Xiao SD. Generation of hepatocytes from cultured mouse embryonic stem cells. Liver Transpl. 2003;9:1094–9.
   PubMed Web of Science ®Google Scholar
• Teramoto K, Asahina K, Kumashiro Y, Kakinuma S, Chinzei R, Shimizu-Saito K, . Hepatocyte differentiation from embryonic stem cells and umbilical cord blood cells. J Hepatobiliary Pancreat Surg. 2005;12:196–202.
   PubMedGoogle Scholar
• Saito K, Yoshikawa M, Ouji Y, Moriya K, Nishiofuku M, Ueda S, . Promoted differentiation of cynomolgus monkey ES cells into hepatocyte-like cells by co-culture with mouse fetal liver-derived cells. World J Gastroenterol. 2006;12:6818–27.
   Google Scholar
• Jochheim A, Hillemann T, Kania G, Scharf J, Attaran M, Manns MP, . Quantitative gene expression profiling reveals a fetal hepatic phenotype of murine ES-derived hepatocytes. Int J Dev Biol. 2004;48:23–9.
   Google Scholar
• Agarwal S, Holton KL, Lanza R. Efficient differentiation of functional hepatocytes from human embryonic stem cells. Stem Cells. 2008;26:1117–27.
   PubMed Web of Science ®Google Scholar
• Shiraki N, Umeda K, Sakashita N, Takeya M, Kume K, Kume S. Differentiation of mouse and human embryonic stem cells into hepatic lineages. Genes Cells. 2008;13:731–46.
   PubMed Web of Science ®Google Scholar
• Hay DC, Zhao D, Fletcher J, Hewitt ZA, McLean D, Urruticoechea-Uriguen A, . Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo. Stem Cells. 2008;26:894–902.
   PubMed Web of Science ®Google Scholar
• Cho CH, Parashurama N, Park EY, Suganuma K, Nahmias Y, Park J, . Homogeneous differentiation of hepatocyte-like cells from embryonic stem cells: applications for the treatment of liver failure. FASEB J. 2008;22:898–909.
   PubMed Web of Science ®Google Scholar
• Basma H, Soto-Gutierrez A, Yannam GR, Liu L, Ito R, Yamamoto T, . Differentiation and transplantation of human embryonic stem cell-derived hepatocytes. Gastroenterology. 2009;136:990–9.
   PubMed Web of Science ®Google Scholar
• Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood. 2004;103:1669–75.
   PubMed Web of Science ®Google Scholar
• Tang XP, Yang X, Zhang M, Wang WL, Chen LM. [Clinical and experimental study of the therapeutic effect of umbilical cord blood stem cell transplantation on liver failure and heart damage in severe viral hepatitis patients]. Zhonghua Gan Zang Bing Za Zhi. 2005;13:259–63.
   Google Scholar
• Di Campli C, Piscaglia AC, Pierelli L, Rutella S, Bonanno G, Alison MR, . A human umbilical cord stem cell rescue therapy in a murine model of toxic liver injury. Dig Liver Dis. 2004;36:603–13.
   PubMedGoogle Scholar
• Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, . Human adipose tissue is a source of multi-potent stem cells. Mol Biol Cell. 2002;13:4279–95.
   PubMed Web of Science ®Google Scholar
• Rodriguez AM, Elabd C, Amri EZ, Ailhaud G, Dani C. The human adipose tissue is a source of multipotent stem cells. Biochimie. 2005;87:125–8.
   PubMed Web of Science ®Google Scholar
• Seo MJ, Suh SY, Bae YC, Jung JS. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem Biophys Res Commun. 2005;328:258–64.
   PubMed Web of Science ®Google Scholar
• Yang P, Yin S, Cui L, Li H, Wu Y, Liu W, . [Experiment of adipose derived stem cells induced into smooth muscle cells]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi. 2008;22:481–6.
   Google Scholar
• Nincheri P, Luciani P, Squecco R, Donati C, Bernacchioni C, Borgognoni L, . Sphingosine 1-phosphate induces differentiation of adipose tissue-derived mesenchymal stem cells towards smooth muscle cells. Cell Mol Life Sci. 2009;66:1741–54.
   Google Scholar
• Tang YJ, Zhang LH, Liu JM, Dong WR, Guo JS, Wang HH, . [Induced differentiation of rat adipose-derived stem cells into Schwann-like cells.]. Nan Fang Yi Ke Da Xue Xue Bao. 2009;29:680–4.
   Google Scholar
• Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Quinn G, . Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology. 2007;46:219–28.
   PubMed Web of Science ®Google Scholar
• Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Osaki M, . Rapid hepatic fate specification of adipose-derived stem cells and their therapeutic potential for liver failure. J Gastroenterol Hepatol. 2009;24:70–7.
   PubMed Web of Science ®Google Scholar
• Mistry AS, Mikos AG. Tissue engineering strategies for bone regeneration. Adv Biochem Eng Biotechnol. 2005;94:1–22.
   PubMed Web of Science ®Google Scholar
• Temenoff JS, Mikos AG. Review: tissue engineering for regeneration of articular cartilage. Biomaterials. 2000;21:431–40.
   PubMed Web of Science ®Google Scholar
• Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, . Engineering vascularized skeletal muscle tissue. Nat Biotechnol. 2005;23:879–84.
   PubMed Web of Science ®Google Scholar
• Guillouzo A. Liver cell models in in vitro toxicology. Environ Health Perspect. 1998;106(Suppl 2):511–32.
   PubMedGoogle Scholar
• Maher JJ. Primary hepatocyte culture: is it home away from home? Hepatology. 1988;8:1162–6.
   PubMed Web of Science ®Google Scholar
• Powers MJ, Rodriguez RE, Griffith LG. Cell-substratum adhesion strength as a determinant of hepatocyte aggregate morphology. Biotechnol Bioeng. 1997;53:415–26.
   PubMed Web of Science ®Google Scholar
• Griffith LG, Lopina S. Microdistribution of substratum-bound ligands affects cell function: hepatocyte spreading on PEO-tethered galactose. Biomaterials. 1998;19:979–86.
   PubMed Web of Science ®Google Scholar
• Hammond JS, Beckingham IJ, Shakesheff KM. Scaffolds for liver tissue engineering. Expert Rev Med Devices. 2006;3:21–7.
   PubMed Web of Science ®Google Scholar
• Kaufmann PM, Heimrath S, Kim BS, Mooney DJ. Highly porous polymer matrices as a three-dimensional culture system for hepatocytes. Cell Transplant. 1997;6:463–8.
   PubMed Web of Science ®Google Scholar
• Mikos AG, McIntire LV, Anderson JM, Babensee JE. Host response to tissue engineered devices. Adv Drug Deliv Rev. 1998;33:111–39.
   PubMed Web of Science ®Google Scholar
• Anderson JM, Langone JJ. Issues and perspectives on the biocompatibility and immunotoxicity evaluation of implanted controlled release systems. J Control Release. 1999;57:107–13.
   PubMed Web of Science ®Google Scholar
• Nam YS, Yoon JJ, Lee JG, Park TG. Adhesion behaviours of hepatocytes cultured onto biodegradable polymer surface modified by alkali hydrolysis process. J Biomater Sci Polym Ed. 1999;10:1145–58.
   PubMed Web of Science ®Google Scholar
• Chung TW, Yang J, Akaike T, Cho KY, Nah JW, Kim SI, . Preparation of alginate/galactosylated chitosan scaffold for hepatocyte attachment. Biomaterials. 2002;23:2827–34.
   PubMed Web of Science ®Google Scholar
• Seo SJ, Kim IY, Choi YJ, Akaike T, Cho CS. Enhanced liver functions of hepatocytes cocultured with NIH 3T3 in the alginate/galactosylated chitosan scaffold. Biomaterials. 2006;27:1487–95.
   PubMed Web of Science ®Google Scholar
• Feng ZQ, Chu X, Huang NP, Wang T, Wang Y, Shi X, . The effect of nanofibrous galactosylated chitosan scaffolds on the formation of rat primary hepatocyte aggregates and the maintenance of liver function. Biomaterials. 2009;30:2753–63.
   PubMed Web of Science ®Google Scholar
• Chu XH, Shi XL, Feng ZQ, Gu ZZ, Ding YT. Chitosan nanofiber scaffold enhances hepatocyte adhesion and function. Biotechnol Lett. 2009;31:347–52.
   Google Scholar
• Gotoh Y, Niimi S, Hayakawa T, Miyashita T. Preparation of lactose–silk fibroin conjugates and their application as a scaffold for hepatocyte attachment. Biomaterials. 2004;25:1131–40.
   PubMed Web of Science ®Google Scholar
• Jiang J, Kojima N, Kinoshita T, Miyajima A, Yan W, Sakai Y. Cultivation of fetal liver cells in a three-dimensional poly-L-lactic acid scaffold in the presence of oncostatin M. Cell Transplant. 2002;11:403–6.
   Google Scholar
• Miyoshi H, Ehashi T, Ema H, Hsu HC, Nakauchi H, Ohshima N. Long-term culture of fetal liver cells using a three-dimensional porous polymer substrate. Asaio J. 2000; 46:397–402.
   Google Scholar
• Sakai Y, Jiang J, Kojima N, Kinoshita T, Miyajima A. Enhanced in vitro maturation of fetal mouse liver cells with oncostatin M, nicotinamide, and dimethyl sulfoxide. Cell Transplant. 2002;11:435–41.
   Google Scholar
• Mitaka T, Sattler GL, Pitot HC, Mochizuki Y. Characteristics of small cell colonies developing in primary cultures of adult rat hepatocytes. Virchows Arch B Cell Pathol Incl Mol Pathol. 1992;62:329–35.
   PubMedGoogle Scholar
• Mitaka T, Sato F, Mizuguchi T, Yokono T, Mochizuki Y. Reconstruction of hepatic organoid by rat small hepatocytes and hepatic nonparenchymal cells. Hepatology. 1999;29:111–25.
   PubMed Web of Science ®Google Scholar
• Jiang J, Kojima N, Guo L, Naruse K, Makuuchi M, Miyajima A, . 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 Eng. 2004;10:1577–86.
   Google Scholar
• Reid LM. Stem cell biology, hormone/matrix synergies and liver differentiation. Curr Opin Cell Biol. 1990;2:121–30.
   PubMed Web of Science ®Google Scholar
• Nezu T, Winnik FM. Interaction of water-soluble collagen with poly(acrylic acid). Biomaterials. 2000;21:415–9.
   PubMedGoogle Scholar
• Yagi K, Michibayashi N, Kurikawa N, Nakashima Y, Mizoguchi T, Harada A, . Effectiveness of fructose-modified chitosan as a scaffold for hepatocyte attachment. Biol Pharm Bull. 1997;20:1290–4.
   PubMed Web of Science ®Google Scholar
• Madihally SV, MatthewH W. Porous chitosan scaffolds for tissue engineering. Biomaterials. 1999;20:1133–42.
   PubMed Web of Science ®Google Scholar
• Hsieh WC, Chang CP, Lin SM. Morphology and characterization of 3D micro-porous structured chitosan scaffolds for tissue engineering. Colloids Surf B Biointerfaces. 2007;57:250–5.
   PubMed Web of Science ®Google Scholar
• Taravel MN, Domard A. Collagen and its interactions with chitosan, III Some biological and mechanical properties. Biomaterials. 1996;17:451–5.
   PubMed Web of Science ®Google Scholar
• Hirano S, Zhang M, Nakagawa M, Miyata T. Wet spun chitosan–collagen fibers, their chemical N-modifications, and blood compatibility. Biomaterials. 2000;21:997–1003.
   PubMed Web of Science ®Google Scholar
• Gingras M, Paradis I, Berthod F. Nerve regeneration in a collagen-chitosan tissue-engineered skin transplanted on nude mice. Biomaterials. 2003;24:1653–61.
   PubMed Web of Science ®Google Scholar
• Shanmugasundaram N, Ravichandran P, Reddy PN, Ramamurty N, Pal S, Rao KP. Collagen-chitosan polymeric scaffolds for the in vitro culture of human epidermoid carcinoma cells. Biomaterials. 2001;22:1943–51.
   PubMed Web of Science ®Google Scholar
• Wang X, Yan Y, Xiong Z, Lin F, Wu R, Zhang R, . Preparation and evaluation of ammonia-treated collagen/ chitosan matrices for liver tissue engineering. J Biomed Mater Res B Appl Biomater. 2005;75:91–8.
   Google Scholar
• Jiankang H, Dichen L, Yaxiong L, Bo Y, Hanxiang Z, Qin L, . Preparation of chitosan-gelatin hybrid scaffolds with well-organized microstructures for hepatic tissue engineering. Acta Biomater. 2009;5:453–61.
   PubMed Web of Science ®Google Scholar
• Kim SS, Utsunomiya H, Koski JA, Wu BM, Cima MJ, Sohn J, . Survival and function of hepatocytes on a novel three-dimensional synthetic biodegradable polymer scaffold with an intrinsic network of channels. Ann Surg. 1998;228:8–13.
   PubMed Web of Science ®Google Scholar
• Lysaght MJ, Aebischer P. Encapsulated cells as therapy. Sci Am. 1999;280:76–82.
   PubMed Web of Science ®Google Scholar
• Mooney DJ, Kaufmann PM, Sano K, Schwendeman SP, Majahod K, Schloo B, . Localized delivery of epidermal growth factor improves the survival of transplanted hepatocytes. Biotechnol Bioeng. 1996;50:422–9.
   PubMed Web of Science ®Google Scholar
• Folkman J, Shing Y. Control of angiogenesis by heparin and other sulfated polysaccharides. Adv Exp Med Biol. 1992;313:355–64.
   PubMedGoogle Scholar
• Wang X, Yan Y, Lin F, Xiong Z, Wu R, Zhang R, . Preparation and characterization of a collagen/chitosan/ heparin matrix for an implantable bioartificial liver. J Biomater Sci Polym Ed. 2005;16:1063–80.
   PubMed Web of Science ®Google Scholar
• Mooney DJ, Park S, Kaufmann PM, Sano K, McNamara K, Vacanti JP, . Biodegradable sponges for hepatocyte transplantation. J Biomed Mater Res. 1995;29:959–65.
   PubMed Web of Science ®Google Scholar
• Fiegel HC, Havers J, Kneser U, Smith MK, Moeller T, Kluth D, . Influence of flow conditions and matrix coatings on growth and differentiation of three-dimensionally cultured rat hepatocytes. Tissue Eng. 2004;10:165–74.
   Google Scholar
• Lee H, Cusick RA, Browne F, Ho Kim T, Ma PX, Utsunomiya H, . Local delivery of basic fibroblast growth factor increases both angiogenesis and engraftment of hepatocytes in tissue-engineered polymer devices. Transplantation. 2002;73:1589–93.
   PubMed Web of Science ®Google Scholar
• Kang IK, Kim GJ, Kwon OH, Ito Y. Co-culture of hepatocytes and fibroblasts by micropatterned immobilization of beta-galactose derivatives. Biomaterials. 2004;25:4225–32.
   Google Scholar
• Fukuda J, Sakai Y, Nakazawa K. Novel hepatocyte culture system developed using microfabrication and collagen/ polyethylene glycol microcontact printing. Biomaterials. 2006;27:1061–70.
   PubMed Web of Science ®Google Scholar
• Leclerc E, Corlu A, Griscom L, Baudoin R, Legallais C. Guidance of liver and kidney organotypic cultures inside rectangular silicone microchannels. Biomaterials. 2006;27:4109–19.
   PubMedGoogle Scholar
• Toh YC, Zhang C, Zhang J, Khong YM, Chang S, Samper VD, . A novel 3D mammalian cell perfusion-culture system in microfluidic channels. Lab Chip. 2007;7:302–9.
   PubMed Web of Science ®Google Scholar
• Schumacher K, Khong YM, Chang S, Ni J, Sun W, Yu H. Perfusion culture improves the maintenance of cultured liver tissue slices. Tissue Eng. 2007;13:197–205.
   PubMedGoogle Scholar
• Anderson JR, Chiu DT, Jackman RJ, Cherniavskaya O, McDonald JC, Wu H, . Fabrication of topologically complex three-dimensional microfluidic systems in PDMS by rapid prototyping. Anal Chem. 2000;72:3158–64.
   PubMed Web of Science ®Google Scholar
• Chiu DT, Jeon NL, Huang S, Kane RS, Wargo CJ, Choi IS, . Patterned deposition of cells and proteins onto surfaces by using three-dimensional microfluidic systems. Proc Natl Acad Sci USA. 2000;97:2408–13.
   PubMed Web of Science ®Google Scholar
• Leclerc E, Sakai Y, Fujii T. Microfluidic PDMS (polydimethylsiloxane) bioreactor for large-scale culture of hepatocytes. Biotechnol Prog. 2004;20:750–5.
   PubMed Web of Science ®Google Scholar
• Chang TM, Prakash S. Therapeutic uses of microencapsulated genetically engineered cells. Mol Med Today. 1998;4:221–7.
   PubMedGoogle Scholar
• Lanza RP, Hayes JL, Chick WL. Encapsulated cell technology. Nat Biotechnol. 1996;14:1107–11.
   PubMed Web of Science ®Google Scholar
• Gomez N, Balladur P, Calmus Y, Baudrimont M, Honiger J, Delelo R, . Evidence for survival and metabolic activity of encapsulated xenogeneic hepatocytes transplanted without immunosuppression in Gunn rats. Transplantation. 1997;63:1718–23.
   PubMed Web of Science ®Google Scholar
• Skjak-Braek G. Alginates: biosyntheses and some structure– function relationships relevant to biomedical and biotechno-logical applications. Biochem Soc Trans. 1992;20:27–33.
   PubMed Web of Science ®Google Scholar
• Hari PR, Chandy T, Sharma CP. Chitosan/calcium alginate microcapsules for intestinal delivery of nitrofurantoin. J Microencapsul. 1996;13:319–29.
   PubMed Web of Science ®Google Scholar
• Smidsrod O, Skjak-Braek G. Alginate as immobilization matrix for cells. Trends Biotechnol. 1990;8:71–8.
   PubMed Web of Science ®Google Scholar
• Lim F, Moss RD. Microencapsulation of living cells and tissues. J Pharm Sci. 1981;70:351–4.
   PubMed Web of Science ®Google Scholar
• Shoichet MS, Li RH, White ML, Winn SR. Stability of hydrogels used in cell encapsulation: an in vitro comparison of alginate and agarose. Biotechnol Bioeng. 1996;50:374–81.
   PubMed Web of Science ®Google Scholar
• Yagi K, Tsuda K, Serada M, Yamada C, Kondoh A, Miura Y. Rapid formation of multicellular spheroids of adult rat hepatocytes by rotation culture and their immobilization within calcium alginate. Artif Organs. 1993;17:929–34.
   Google Scholar
• Smetana K Jr. Cell biology of hydrogels. Biomaterials. 1993;14:1046–50.
   PubMed Web of Science ®Google Scholar
• Yang J, Goto M, Ise H, Cho CS, Akaike T. Galactosylated alginate as a scaffold for hepatocytes entrapment. Biomaterials. 2002;23:471–9.
   PubMed Web of Science ®Google Scholar
• Giancotti FG, Ruoslahti E. Integrin signaling. Science. 1999;285:1028–32.
   PubMed Web of Science ®Google Scholar
• Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol. 2005;23:47–55.
   PubMed Web of Science ®Google Scholar
• Griffith LG, Naughton G. Tissue engineering: current challenges and expanding opportunities. Science. 2002;295:1009–14.
   PubMed Web of Science ®Google Scholar
• Smets FN, Chen Y, Wang LJ, Soriano HE. Loss of cell anchorage triggers apoptosis (anoikis) in primary mouse hepatocytes. Mol Genet Metab. 2002;75:344–52.
   Google Scholar
• Rosen K, Shi W, Calabretta B, Filmus J. Cell detachment triggers p38 mitogen-activated protein kinase-dependent overexpression of Fas ligand. A novel mechanism of anoikis of intestinal epithelial cells. J Biol Chem. 2002;277:46123–30.
   Google Scholar
• Dang JM, Leong KW. Natural polymers for gene delivery and tissue engineering. Adv Drug Deliv Rev. 2006;58:487–99.
   PubMed Web of Science ®Google Scholar
• Kim IY, Seo SJ, Moon HS, Yoo MK, Park IY, Kim BC, . Chitosan and its derivatives for tissue engineering applications. Biotechnol Adv. 2008;26:1–21.
   PubMed Web of Science ®Google Scholar
• Dodane V, Amin Khan M, Merwin JR. Effect of chitosan on epithelial permeability and structure. Int J Pharm. 1999;182:21–32.
   PubMed Web of Science ®Google Scholar
• Lee JE, Kim KE, Kwon IC, Ahn HJ, Lee SH, Cho H, . Effects of the controlled-released TGF-beta 1 from chitosan microspheres on chondrocytes cultured in a collagen/ chitosan/glycosaminoglycan scaffold. Biomaterials. 2004;25:4163–73.
   PubMed Web of Science ®Google Scholar
• Mattioli-Belmonte M, Gigante A, Muzzarelli RA, Politano R, De Benedittis A, Specchia N, . N,N-dicarboxymethyl chitosan as delivery agent for bone morphogenetic protein in the repair of articular cartilage. Med Biol Eng Comput. 1999;37:130–4.
   PubMed Web of Science ®Google Scholar
• Hoemann CD, Chenite A, Sun J, Hurtig M, Serreqi A, Lu Z, . Cytocompatible gel formation of chitosan– glycerol phosphate solutions supplemented with hydroxyl ethyl cellulose is due to the presence of glyoxal. J Biomed Mater Res A. 2007;83:521–9.
   Google Scholar
• Hoemann CD, Hurtig M, Rossomacha E, Sun J, Chevrier A, Shive MS, . Chitosan–glycerol phosphate/blood implants improve hyaline cartilage repair in ovine microfracture defects. J Bone Joint Surg Am. 2005;87:2671–86.
   PubMed Web of Science ®Google Scholar
• Mooney DJ, Kaufmann PM, Sano K, McNamara KM, Vacanti JP, Langer R. Transplantation of hepatocytes using porous, biodegradable sponges. Transplant Proc. 1994;26:3425–6.
   PubMedGoogle Scholar
• Chan C, Berthiaume F, Nath BD, Tilles AW, Toner M, Yarmush ML. Hepatic tissue engineering for adjunct and temporary liver support: critical technologies. Liver Transpl. 2004;10:1331–42.
   Google Scholar
• Kedem A, Perets A, Gamlieli-Bonshtein I, Dvir-Ginzberg M, Mizrahi S, Cohen S. Vascular endothelial growth factor-releasing scaffolds enhance vascularization and engraftment of hepatocytes transplanted on liver lobes. Tissue Eng. 2005;11:715–22.
   PubMedGoogle Scholar
• Kaihara S, Borenstein J, Koka R, Lalan S, Ochoa ER, Ravens M, . Silicon micromachining to tissue engineer branched vascular channels for liver fabrication. Tissue Eng. 2000;6:105–17.
   PubMedGoogle Scholar
• Borenstein JT, Weinberg EJ, Orrick BK, Sundback C, Kaazempur-Mofrad MR, Vacanti JP. Microfabrication of three-dimensional engineered scaffolds. Tissue Eng. 2007;13:1837–44.
   PubMedGoogle Scholar
• Fidkowski C, Kaazempur-Mofrad MR, Borenstein J, Vacanti JP, Langer R, Wang Y. Endothelialized microvasculature based on a biodegradable elastomer. Tissue Eng. 2005;11:302–9.
   PubMedGoogle Scholar
• Khademhosseini A, Langer R, Borenstein J, Vacanti JP. Microscale technologies for tissue engineering and biology. Proc Natl Acad Sci USA. 2006;103:2480–7.
   PubMed Web of Science ®Google Scholar
• Murray CD. The physiological principle of minimum work. I. The vascular system and the cost of blood volume. Proc Natl Acad Sci USA. 1926;12:207–14.
   PubMedGoogle Scholar
• Zhou Y, Kassab GS, Molloi S. On the design of the coronary arterial tree: a generalization of Murray's law. Phys Med Biol. 1999;44:2929–45.
   PubMed Web of Science ®Google Scholar
• Kassab GS. Scaling laws of vascular trees: of form and function. Am J Physiol Heart Circ Physiol. 2006;290:H894–903.
   PubMed Web of Science ®Google Scholar
• Hoganson DM, Pryor HI 2nd, Vacanti JP. Tissue engineering and organ structure: a vascularized approach to liver and lung. Pediatr Res. 2008;63:520–6.
   PubMed Web of Science ®Google Scholar