Development of a perfusable 3D liver cell cultivation system via bundling-up assembly of cell-laden microfibers

Dash, 2009, Liver tissue engineering in the evaluation of drug safety, Exp. Opin. Drug Metab. Toxicol., 5, 1159, 10.1517/17425250903160664 Greer, 2010, Cell based approaches for evaluation of drug-induced liver injury, Toxicology, 268, 125, 10.1016/j.tox.2009.08.007 Nakazawa, 2006, Hepatocyte spheroid formation on a titanium dioxide gel surface and hepatocyte long-term culture, J. Mater. Sci. Mater. Med., 17, 359, 10.1007/s10856-006-8237-7 Du, 2007, Identification and characterization of a novel prespheroid 3-dimensional hepatocyte monolayer on galactosylated substratum, Tissue Eng., 13, 1455, 10.1089/ten.2006.0381 Yamada, 2015, Cell-sized condensed collagen microparticles for preparing microengineered composite spheroids of primary hepatocytes, Lab Chip, 15, 3941, 10.1039/C5LC00785B Yajima, 2017, Collagen microparticle-mediated 3D cell organization: a facile route to bottom-up engineering of thick and porous tissues, ACS Biomater. Sci. Eng., 3, 2144, 10.1021/acsbiomaterials.7b00131 Khetani, 2008, Microscale culture of human liver cells for drug development, Nat. Biotechnol., 26, 120, 10.1038/nbt1361 Yamada, 2012, Controlled formation of heterotypic hepatic micro-organoids in anisotropic hydrogel microfibers for long-term preservation of liver-specific functions, Biomaterials, 33, 8304, 10.1016/j.biomaterials.2012.07.068 Ito, 2007, Construction of heterotypic cell sheets by magnetic force-based 3-D coculture of HepG2 and NIH3T3 cells, J. Biosci. Bioeng., 104, 371, 10.1263/jbb.104.371 Kim, 2012, Preserved liver-specific functions of hepatocytes in 3D co-culture with endothelial cell sheets, Biomaterials, 33, 1406, 10.1016/j.biomaterials.2011.10.084 Lee-Montiel, 2017, Control of oxygen tension recapitulates zone-specific functions in human liver microphysiology systems, Exp. Biol. Med., 242, 1617, 10.1177/1535370217703978 Guo, 2017, Physiological oxygen tension reduces hepatocyte dedifferentiation in in vitro culture, Sci. Rep., 7, 5923, 10.1038/s41598-017-06433-3 Kim, 2017, Fabrication of functional 3D hepatic tissues with polarized hepatocytes by stacking endothelial cell sheets in vitro, J. Tissue Eng. Regen. Med., 11, 2071, 10.1002/term.2102 Tilles, 2001, Effects of oxygenation and flow on the viability and function of rat hepatocytes cocultured in a microchannel flat-plate bioreactor, Biotechnol. Bioeng., 73, 379, 10.1002/bit.1071 Allen, 2005, In vitro zonation and toxicity in a hepatocyte bioreactor, Toxicol. Sci., 84, 110, 10.1093/toxsci/kfi052 Domansky, 2010, Perfused multiwell plate for 3D liver tissue engineering, Lab Chip, 10, 51, 10.1039/B913221J Hegde, 2014, Dynamic interplay of flow and collagen stabilizes primary hepatocytes culture in a microfluidic platform, Lab Chip, 14, 2033, 10.1039/C4LC00071D Toh, 2009, A microfluidic 3D hepatocyte chip for drug toxicity testing, Lab Chip, 9, 2026, 10.1039/b900912d Schepers, 2016, Engineering a perfusable 3D human liver platform from iPS cells, Lab Chip, 16, 2644, 10.1039/C6LC00598E Sakai, 2014, Detachably assembled microfluidic device for perfusion culture and post-culture analysis of a spheroid array, Biotechnol. J., 9, 971, 10.1002/biot.201300559 Okuyama, 2010, Preparation of arrays of cell spheroids and spheroid-monolayer cocultures within a microfluidic device, J. Biosci. Bioeng., 110, 572, 10.1016/j.jbiosc.2010.05.013 Lubberstedt, 2015, Serum-free culture of primary human hepatocytes in a miniaturized hollow-fibre membrane bioreactor for pharmacological in vitro studies, J. Tissue Eng. Regen. Med., 9, 1017, 10.1002/term.1652 Takei, 2016, Vascular-like network prepared using hollow hydrogel microfibers, J. Biosci. Bioeng., 121, 336, 10.1016/j.jbiosc.2015.06.018 Ahmed, 2017, Human liver microtissue spheroids in hollow fiber membrane bioreactor, Colloids Surf. B Biointerfaces, 160, 272, 10.1016/j.colsurfb.2017.09.024 Mazza, 2015, Decellularized human liver as a natural 3D-scaffold for liver bioengineering and transplantation, Sci. Rep., 5, 13079, 10.1038/srep13079 Kobayashi, 2013, Preparation of stripe-patterned heterogeneous hydrogel sheets using microfluidic devices for high-density coculture of hepatocytes and fibroblasts, J. Biosci. Bioeng., 116, 761, 10.1016/j.jbiosc.2013.05.034 Duffy, 1998, Rapid prototyping of microfluidic systems in poly(dimethylsiloxane), Anal. Chem., 70, 4974, 10.1021/ac980656z Andersen, 2004, Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets, Cancer Res., 64, 5245, 10.1158/0008-5472.CAN-04-0496 Tanaka, 1988, Preparation of stable alginate gel beads in electrolyte solutions using Ba2+ and Sr2+, Biotechnol. Tech., 2, 115, 10.1007/BF01876161 Provin, 2009, Low O2 metabolism of HepG2 cells cultured at high density in a 3D microstructured scaffold, Biomed. Microdevices, 11, 485, 10.1007/s10544-008-9254-8 Mueller, 2011, Organotypic cultures of Hepg2 cells for in vitro toxicity studies, J. Bioeng. Biomed. Sci., 10.4172/2155-9538.S2-002 Bustin, 2009, The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments, Clin. Chem., 55, 611, 10.1373/clinchem.2008.112797 Anada, 2010, Three-dimensional cell culture device utilizing thin membrane deformation by decompression, Sens. Actuators B Chem., 147, 376, 10.1016/j.snb.2010.01.065 Tamayol, 2015, Hydrogel templates for rapid manufacturing of bioactive fibers and 3D constructs, Adv. Healthcare Mater., 4, 2146, 10.1002/adhm.201500492 Onoe, 2013, Metre-long cell-laden microfibres exhibit tissue morphologies and functions, Nat. Mater., 12, 584, 10.1038/nmat3606 Onoe, 2015, Cell-laden microfibers for bottom-up tissue engineering, Drug Discov. Today, 20, 236, 10.1016/j.drudis.2014.10.018 Cho, 2007, Oxygen uptake rates and liver-specific functions of hepatocyte and 3T3 fibroblast co-cultures, Biotechnol. Bioeng., 97, 188, 10.1002/bit.21225 Kidambi, 2009, Oxygen-mediated enhancement of primary hepatocyte metabolism, functional polarization, gene expression, and drug clearance, Proc. Natl. Acad. Sci. USA, 106, 15714, 10.1073/pnas.0906820106 Nahmias, 2006, A novel formulation of oxygen-carrying matrix enhances liver-specific function of cultured hepatocytes, FASEB J., 20, 2531, 10.1096/fj.06-6192fje Braet, 2002, Structural and functional aspects of liver sinusoidal endothelial cell fenestrae: a review, Comp. Hepatol., 1, 1, 10.1186/1476-5926-1-1 Kietzmann, 2017, Metabolic zonation of the liver: the oxygen gradient revisited, Red. Biol., 11, 622, 10.1016/j.redox.2017.01.012 Camp, 2007, Induction of zone-like liver function gradients in HepG2 cells by varying culture medium height, Biotechnol. Prog., 23, 1485, 10.1021/bp070308v Inamori, 2010, Investigation of medium perfusion through scaffold-free tissue constructs using endothelial cell-covered spheroids in vitro, Biochem. Eng. J., 50, 116, 10.1016/j.bej.2010.04.004 Bruzewicz, 2008, Fabrication of a modular tissue construct in a microfluidic chip, Lab Chip, 8, 663, 10.1039/b719806j Miller, 2012, Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues, Nat. Mater., 11, 768, 10.1038/nmat3357 Moya, 2013, In vitro perfused human capillary networks, Tissue Eng. C Methods, 19, 730, 10.1089/ten.tec.2012.0430 Osaki, 2015, Acceleration of vascular sprouting from fabricated perfusable vascular-like structures, PLoS One, 10, e0123735, 10.1371/journal.pone.0123735 Takei, 2016, In vitro formation of vascular-like networks using hydrogels, J. Biosci. Bioeng., 122, 519, 10.1016/j.jbiosc.2016.03.023 Wilkening, 2003, Comparison of primary human hepatocytes and hepatoma cell line HepG2 with regard to their biotransformation properties, Drug Metab. Dispos., 31, 1035, 10.1124/dmd.31.8.1035