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Articles

Construction of polysaccharide scaffold-based perfusion bioreactor supporting liver cell aggregates for drug screening

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Pages 2249-2269 | Received 12 May 2022, Accepted 14 Jul 2022, Published online: 26 Jul 2022

References

  • Ware BR, Khetani SR. Engineered liver platforms for different phases of drug development. Trends Biotechnol. 2017;35(2):172–183.
  • Kola I, Landis J. Can the pharmaceutical industry reduce attrition rates? Nat Rev Drug Discov. 2004;3(8):711–715.
  • Kaplowitz N. Idiosyncratic drug hepatotoxicity. Nat Rev Drug Discov. 2005;4(6):489–499.
  • Bunchorntavakul C, Reddy KR. Drug hepatotoxicity: Newer agents. Clin Liver Dis. 2017;21(1):115–134.
  • European Association for the Study of the Liver. Electronic address, e.e.e., et al. EASL clinical practice guidelines: Drug-induced liver injury. J Hepatol. 2019;70(6):1222–1261.
  • Rushmore TH, Kong AN. Pharmacogenomics, regulation and signaling pathways of phase I and II drug metabolizing enzymes. Curr Drug Metab. 2002;3(5):481–490.
  • Gomez-Lechon MJ, et al. Competency of different cell models to predict human hepatotoxic drugs. Expert Opin Drug Metab Toxicol. 2014;10(11):1553–1568.
  • Godoy P, Hewitt NJ, Albrecht U, et al. Recent advances in 2D and 3D in vitro systems using primary hepatocytes, alternative hepatocyte sources and non-parenchymal liver cells and their use in investigating mechanisms of hepatotoxicity, cell signaling and ADME. Arch Toxicol. 2013;87(8):1315–1530.
  • Meng Q. Three-dimensional culture of hepatocytes for prediction of drug-induced hepatotoxicity. Expert Opin Drug Metab Toxicol. 2010;6(6):733–746.
  • Bale SS, Golberg I, Jindal R, et al. Long-term coculture strategies for primary hepatocytes and liver sinusoidal endothelial cells. Tissue Eng Part C Methods. 2015;21(4):413–422.
  • Levy G, Bomze D, Heinz S, et al. Long-term culture and expansion of primary human hepatocytes. Nat Biotechnol. 2015;33(12):1264–1271.
  • Huang G, Li F, Zhao X, et al. Functional and biomimetic materials for engineering of the Three-Dimensional cell microenvironment. Chem Rev. 2017;117(20):12764–12850.
  • Xia L, Arooz T, Zhang S, et al. Hepatocyte function within a stacked double sandwich culture plate cylindrical bioreactor for bioartificial liver system. Biomaterials. 2012;33(32):7925–7932.
  • Ginai M, Elsby R, Hewitt CJ, et al. The use of bioreactors as in vitro models in pharmaceutical research. Drug Discov Today. 2013;18(19-20):922–935.
  • Chang R, Emami K, Wu H, et al. Biofabrication of a three-dimensional liver micro-organ as an in vitro drug metabolism model. Biofabrication. 2010;2(4):045004.
  • Breslin S, O'Driscoll L. Three-dimensional cell culture: the missing link in drug discovery. Drug Discov Today. 2013;18(5-6):240–249.
  • Grayson WL, Marolt D, Bhumiratana S, et al. Optimizing the medium perfusion rate in bone tissue engineering bioreactors. Biotechnol Bioeng. 2011;108(5):1159–1170.
  • Schmelzer E, Triolo F, Turner ME, et al. Three-dimensional perfusion bioreactor culture supports differentiation of human fetal liver cells. Tissue Eng Part A. 2010;16(6):2007–2016.
  • Abeille F, Mittler F, Obeid P, et al. Continuous microcarrier-based cell culture in a benchtop microfluidic bioreactor. Lab Chip. 2014;14(18):3510–3518.
  • Sibuea CV, Pawitan J, Antarianto R, et al. 3D Co-Culture of hepatocyte, a hepatic stellate cell line, and stem cells for developing a bioartificial liver prototype. IJTech. 2020;11(5):951–962.
  • Goral VN, Hsieh Y-C, Petzold ON, et al. Perfusion-based microfluidic device for three-dimensional dynamic primary human hepatocyte cell culture in the absence of biological or synthetic matrices or coagulants. Lab Chip. 2010;10(24):3380–3386.
  • Zhang J, Zhao X, Liang L, et al. A decade of progress in liver regenerative medicine. Biomaterials. 2018;157:161–176.
  • Li Z, Cui Z. Three-dimensional perfused cell culture. Biotechnol Adv. 2014;32(2):243–254.
  • Cho CS, Seo SJ, Park IK, et al. Galactose-carrying polymers as extracellular matrices for liver tissue engineering. Biomaterials. 2006;27(4):576–585.
  • Antarianto RD, Pragiwaksana A, Septiana WL, et al. Hepatocyte differentiation from iPSCs or MSCs in decellularized liver scaffold: Cell-ECM adhesion, spatial distribution, and hepatocyte maturation profile. Organogenesis. 2022;18(1):2061263.
  • Weng YS, et al. Scaffold-Free Liver-On-A-Chip with multiscale organotypic cultures. Adv Mater. 2017;29(36):1701545..
  • Kim M, Lee JY, Jones CN, et al. Heparin-based hydrogel as a matrix for encapsulation and cultivation of primary hepatocytes. Biomaterials. 2010;31(13):3596–3603.
  • Lewis PL, Green RM, Shah RN. 3D-printed gelatin scaffolds of differing pore geometry modulate hepatocyte function and gene expression. Acta Biomater. 2018;69:63–70.
  • Xiao Y, Zhou M, Zhang M, et al. Hepatocyte culture on 3D porous scaffolds of PCL/PMCL. Colloids Surf B Biointerfaces. 2019;173:185–193.
  • Kukla DA, Stoppel WL, Kaplan DL, et al. Assessing the compatibility of primary human hepatocyte culture within porous silk sponges. RSC Adv. 2020;10(62):37662–37674.
  • Cheng N, Wauthier E, Reid LM. Mature human hepatocytes from ex vivo differentiation of alginate-encapsulated hepatoblasts. Tissue Eng Part A. 2008;14(1):1–7.
  • Lee KY, Mooney DJ. Alginate: properties and biomedical applications. Prog Polym Sci. 2012;37(1):106–126.
  • Janani G, Mandal BB. Mimicking physiologically relevant hepatocyte zonation using immunomodulatory silk liver extracellular matrix scaffolds toward a bioartificial liver platform. ACS Appl Mater Interfaces. 2021;13(21):24401–24421.
  • Shehata EMM, Gowayed MA, El-Ganainy SO, et al. Pectin coated nanostructured lipid carriers for targeted piperine delivery to hepatocellular carcinoma. Int J Pharm. 2022;619:121712.
  • Munarin F, Tanzi MC, Petrini P. Advances in biomedical applications of pectin gels. Int J Biol Macromol. 2012;51(4):681–689.
  • Markov PA, Krachkovsky NS, Durnev EA, et al. Mechanical properties, structure, bioadhesion, and biocompatibility of pectin hydrogels. J Biomed Mater Res A. 2017;105(9):2572–2581.
  • Hh A, et al. Freeze-printing of pectin/alginate scaffolds with high resolution, overhang structures and interconnected porous network. Additive Manufacturing, 2021.
  • Seglen PO. Preparation of isolated rat liver cells. Methods Cell Biol. 1976;13:29–83.
  • Morita M, Watanabe Y, Akaike T. Protective effect of hepatocyte growth factor on interferon-gamma-induced cytotoxicity in mouse hepatocytes. Hepatology. 1995;21(6):1585–1593.
  • Bale SS, Geerts S, Jindal R, et al. Isolation and co-culture of rat parenchymal and non-parenchymal liver cells to evaluate cellular interactions and response. Sci Rep. 2016;6:25329.
  • Li Z, Leung M, Hopper R, et al. Feeder-free self-renewal of human embryonic stem cells in 3D porous natural polymer scaffolds. Biomaterials. 2010;31(3):404–412.
  • Wang C-C, Yang K-C, Lin K-H, et al. A highly organized three-dimensional alginate scaffold for cartilage tissue engineering prepared by microfluidic technology. Biomaterials. 2011;32(29):7118–7126.
  • Powers MJ, Domansky K, Kaazempur-Mofrad MR, et al. A microfabricated array bioreactor for perfused 3D liver culture. Biotechnol Bioeng. 2002;78(3):257–269.
  • Chen JP, Lin CT. Dynamic seeding and perfusion culture of hepatocytes with galactosylated vegetable sponge in packed-bed bioreactor. J Biosci Bioeng. 2006;102(1):41–45.
  • Jauregui HO, Ng SF, Gann KL, et al. Xenobiotic induction of P-450 PB-4 (IIB1) and P-450c (IA1) and associated monooxygenase activities in primary cultures of adult rat hepatocytes. Xenobiotica. 1991;21(9):1091–1106.
  • Lau YY, Sapidou E, Cui X, et al. Development of a novel in vitro model to predict hepatic clearance using fresh, cryopreserved, and sandwich-cultured hepatocytes. Drug Metab Dispos. 2002;30(12):1446–1454.
  • Yang J, Goto M, Ise H, et al. Galactosylated alginate as a scaffold for hepatocytes entrapment. Biomaterials. 2002;23(2):471–479.
  • Kim SH, Kim JH, Akaike T. Regulation of cell adhesion signaling by synthetic glycopolymer matrix in primary cultured hepatocyte. FEBS Lett. 2003;553(3):433–439.
  • Chua K-N, Lim W-S, Zhang P, et al. Stable immobilization of rat hepatocyte spheroids on galactosylated nanofiber scaffold. Biomaterials. 2005;26(15):2537–2547.
  • Seo S-J, Kim I-Y, Choi Y-J, et al. Enhanced liver functions of hepatocytes cocultured with NIH 3T3 in the alginate/galactosylated chitosan scaffold. Biomaterials. 2006;27(8):1487–1495.
  • Lee S-A, No DY, Kang E, et al. Spheroid-based three-dimensional liver-on-a-chip to investigate hepatocyte-hepatic stellate cell interactions and flow effects. Lab Chip. 2013;13(18):3529–3537.
  • Martin I, Wendt D, Heberer M. The role of bioreactors in tissue engineering. Trends Biotechnol. 2004;22(2):80–86.
  • Kidambi S, Yarmush RS, Novik E, et al. Oxygen-mediated enhancement of primary hepatocyte metabolism, functional polarization, gene expression, and drug clearance. Proc Natl Acad Sci U S A. 2009;106(37):15714–15719.
  • Alvarez-Dominguez JR, Melton DA. Cell maturation: Hallmarks, triggers, and manipulation. Cell. 2022;185(2):235–249.
  • Nahmias Y, Berthiaume F, Yarmush ML. Integration of technologies for hepatic tissue engineering. Adv Biochem Eng Biotechnol. 2007;103:309–329.
  • Balis UJ, Behnia K, Dwarakanath B, et al. Oxygen consumption characteristics of porcine hepatocytes. Metab Eng. 1999;1(1):49–62.
  • Rotem A, Toner M, Tompkins RG, et al. Oxygen uptake rates in cultured rat hepatocytes. Biotechnol Bioeng. 1992;40(10):1286–1291.
  • Park W-J, Park J-W, Erez-Roman R, et al. Protection of a ceramide synthase 2 null mouse from drug-induced liver injury: role of gap junction dysfunction and connexin 32 mislocalization. J Biol Chem. 2013;288(43):30904–30916.
  • Luther J, Khan S, Gala MK, et al. Hepatic gap junctions amplify alcohol liver injury by propagating cGAS-mediated IRF3 activation. Proc Natl Acad Sci U S A. 2020;117(21):11667–11673.
  • Maitre JL, Heisenberg CP. Three functions of cadherins in cell adhesion. Curr Biol. 2013;23(14):R626–33.
  • Treyer A, Musch A. Hepatocyte polarity. Compr Physiol. 2013;3(1):243–287.
  • Martin-Belmonte F, Perez-Moreno M. Epithelial cell polarity, stem cells and cancer. Nat Rev Cancer. 2011;12(1):23–38.
  • Gissen P, Arias IM. Structural and functional hepatocyte polarity and liver disease. J Hepatol, 2015;63(4):1023–1037.
  • Ho RH, Tirona RG, Leake BF, et al. Drug and bile acid transporters in rosuvastatin hepatic uptake: function, expression, and pharmacogenetics. Gastroenterology. 2006;130(6):1793–1806.
  • Pedersen JM, Matsson P, Bergström CAS, et al. Early identification of clinically relevant drug interactions with the human bile salt export pump (BSEP/ABCB11). Toxicol Sci. 2013;136(2):328–343.
  • Bessems JG, Vermeulen NP. Paracetamol (acetaminophen)-induced toxicity: molecular and biochemical mechanisms, analogues and protective approaches. Crit Rev Toxicol. 2001;31(1):55–138.
  • Zand R, Nelson SD, Slattery JT, et al. Inhibition and induction of cytochrome P4502E1-catalyzed oxidation by isoniazid in humans. Clin Pharmacol Ther. 1993;54(2):142–149.
  • Getachew Y, James L, Lee WM, et al. Susceptibility to acetaminophen (APAP) toxicity unexpectedly is decreased during acute viral hepatitis in mice. Biochem Pharmacol. 2010;79(9):1363–1371.
  • Huang Y-S, Chern H-D, Su W-J, et al. Cytochrome P450 2E1 genotype and the susceptibility to antituberculosis drug-induced hepatitis. Hepatology. 2003;37(4):924–930.
  • Park KS, Sohn DH, Veech RL, et al. Translational activation of ethanol-inducible cytochrome P450 (CYP2E1) by isoniazid. Eur J Pharmacol. 1993;248(1):7–14.
  • Griffin SJ, Houston JB. Prediction of in vitro intrinsic clearance from hepatocytes: comparison of suspensions and monolayer cultures. Drug Metab Dispos. 2005;33(1):115–120.

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