The role of cellular interactions in the induction of hepatocyte polarity and functional maturation in stem cell-derived hepatic cells

Agarwal, 2008, Efficient differentiation of functional hepatocytes from human embryonic stem cells, Stem Cell., 26, 1117, 10.1634/stemcells.2007-1102 Anada, 2012, An oxygen-permeable spheroid culture system for the prevention of central hypoxia and necrosis of spheroids, Biomaterials, 33, 8430, 10.1016/j.biomaterials.2012.08.040 Bedossa, 2003, Liver extracellular matrix in health and disease, J. Pathol., 200, 504, 10.1002/path.1397 Behrens, 1985, Dissociation of Madin-Darby canine kidney epithelial cells by the monoclonal antibody anti-arc-1: mechanistic aspects and identification of the antigen as a component related to uvomorulin, J. Cell Biol., 101, 1307, 10.1083/jcb.101.4.1307 Bissell, 1980, Phenotypic stability of adult rat hepatocytes in primary monolayer culture, Ann. N. Y. Acad. Sci., 349, 85, 10.1111/j.1749-6632.1980.tb29518.x Boyer, 2013, Bile formation and secretion, Comp. Physiol., 3, 1035, 10.1002/cphy.c120027 Carpentier, 2009, Artificial and bioartificial liver devices: present and future, Gut, 58, 1690, 10.1136/gut.2008.175380 Dawson, 2010, Liver disease without flipping: new functions of ATP8B1, the protein affected in familial intrahepatic cholestasis type 1, Hepatology, 51, 1885, 10.1002/hep.23662 Demetriou, 2004, Prospective, randomized, multicenter, controlled trial of a bioartificial liver in treating acute liver failure, Ann. Surg., 239, 660, 10.1097/01.sla.0000124298.74199.e5 Ding, 2010, Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration, Nature, 468, 310, 10.1038/nature09493 Dixon, 2013, Kupffer cells in the liver, Comp. Physiol., 3, 785, 10.1002/cphy.c120026 Duncan, 1994, Expression of transcription factor HNF-4 in the extraembryonic endoderm, gut, and nephrogenic tissue of the developing mouse embryo: HNF-4 is a marker for primary endoderm in the implanting blastocyst, Proc. Natl. Acad. Sci. U. S. A., 91, 7598, 10.1073/pnas.91.16.7598 Dunn, 1991, Long-term in vitro function of adult hepatocytes in a collagen sandwich configuration, Biotechnol. Prog., 7, 237, 10.1021/bp00009a007 Fabris, 2008, Epithelial expression of angiogenic growth factors modulate arterial vasculogenesis in human liver development, Hepatology, 47, 719, 10.1002/hep.22015 Feldman, 2005, Occludin: structure, function and regulation, Adv. Drug Deliv. Rev., 57, 883, 10.1016/j.addr.2005.01.009 Fraslin, 1985, Dependence of hepatocyte-specific gene expression on cell-cell interactions in primary culture, EMBO J., 4, 2487, 10.1002/j.1460-2075.1985.tb03960.x Friedman, 2008, Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver, Physiol. Rev., 88, 125, 10.1152/physrev.00013.2007 Gebhardt, 1997, Cell-cell interactions in the regulation of the expression of hepatic enzymes, Cell Biol. Toxicol., 13, 263, 10.1023/A:1007431307300 Gerlach, 1993, Hepatocyte aggregate culture technique for bioreactors in hybrid liver support systems, Int. J. Artif. Organs, 16, 843, 10.1177/039139889301601210 Gerlach, 2003, Use of primary human liver cells originating from discarded grafts in a bioreactor for liver support therapy and the prospects of culturing adult liver stem cells in bioreactors: a morphologic study, Transplantation, 76, 781, 10.1097/01.TP.0000083319.36931.32 Gerlach, 1995, Improved hepatocyte in vitro maintenance in a culture model with woven multicompartment capillary systems: electron microscopy studies, Hepatology, 22, 546 Gissen, 2015, Structural and functional hepatocyte polarity and liver disease, J. Hepatol., 63, 1023, 10.1016/j.jhep.2015.06.015 Glicklis, 2004, Modeling mass transfer in hepatocyte spheroids via cell viability, spheroid size, and hepatocellular functions, Biotechnol. Bioeng., 86, 672, 10.1002/bit.20086 Godoy, 2013, 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, 87, 1315, 10.1007/s00204-013-1078-5 Gonzalez-Mariscal, 1985, Tight junction formation in cultured epithelial cells (MDCK), J. Membr. Biol., 86, 113, 10.1007/BF01870778 Gualdi, 1996, Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control, Genes Dev., 10, 1670, 10.1101/gad.10.13.1670 Guguen-Guillouzo, 1983, Maintenance and reversibility of active albumin secretion by adult rat hepatocytes co-cultured with another liver epithelial cell type, Exp. Cell Res., 143, 47, 10.1016/0014-4827(83)90107-6 Guguen-Guillouzo, 1983, Modulation of functional activities in cultured rat hepatocytes, Mol. Cell. Biochem., 53–54, 35 Hay, 2008, Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo, Stem Cell., 26, 894, 10.1634/stemcells.2007-0718 Hazard, 2007, Sterolins ABCG5 and ABCG8: regulators of whole body dietary sterols, Pflügers Archiv, 453, 745, 10.1007/s00424-005-0040-7 Jauregui, 1992, Long-term cultures of adult mammalian hepatocytes in hollow fibers as the cellular component of extracorporeal (hybrid) liver assist devices, Artif. Organs, 16, 209, 10.1111/j.1525-1594.1992.tb00296.x Jung, 1999, Initiation of mammalian liver development from endoderm by fibroblast growth factors, Science, 284, 1998, 10.1126/science.284.5422.1998 Kamiya, 1999, Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer, EMBO J., 18, 2127, 10.1093/emboj/18.8.2127 Keppler, 2000, Hepatic secretion of conjugated drugs and endogenous substances, Semin. Liver Dis., 20, 265, 10.1055/s-2000-9391 Kojima, 2009, Gap and tight junctions in liver: composition, regulation, and function, 201 Konopka, 2007, Junctional adhesion molecule-A is critical for the formation of pseudocanaliculi and modulates E-cadherin expression in hepatic cells, J. Biol. Chem., 282, 28137, 10.1074/jbc.M703592200 Kubitz, 2012, The bile salt export pump (BSEP) in health and disease, Clin. Res. Hepatol. Gastroenterol., 36, 536, 10.1016/j.clinre.2012.06.006 Kuo, 1991, Evidence that interaction of hepatocytes with the collecting (hepatic) veins triggers position-specific transcription of the glutamine synthetase and ornithine aminotransferase genes in the mouse liver, Mol. Cell Biol., 11, 6050, 10.1128/MCB.11.12.6050 LeCluyse, 2012, Organotypic liver culture models: meeting current challenges in toxicity testing, Crit. Rev. Toxicol, 42, 501, 10.3109/10408444.2012.682115 Li, 2000, Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha, Genes Dev., 14, 464, 10.1101/gad.14.4.464 Li, 1997, Alagille syndrome is caused by mutations in human Jagged 1, which encodes a ligand for Notch 1, Nat. Genet., 16, 243, 10.1038/ng0797-243 Ma, 2013, Highly efficient differentiation of functional hepatocytes from human induced pluripotent stem cells, Stem Cells Transl. Med., 2, 409, 10.5966/sctm.2012-0160 Mallanna, 2013, Differentiation of hepatocytes from pluripotent stem cells, Curr. Protoc. Stem Cell Biol., 26, 10.1002/9780470151808.sc01g04s26 Martinez-Hernandez, 1993, The hepatic extracellular matrix. I. Components and distribution in normal liver, Virchows Arch. A Pathol. Anat. Histopathol., 423, 1, 10.1007/BF01606425 Martinez Barbera, 2000, The homeobox gene Hex is required in definitive endodermal tissues for normal forebrain, liver and thyroid formation, Development, 127, 2433, 10.1242/dev.127.11.2433 Matsui, 2002, K-Ras mediates cytokine-induced formation of E-cadherin-based adherens junctions during liver development, EMBO J., 21, 1021, 10.1093/emboj/21.5.1021 Matsumoto, 2001, Liver organogenesis promoted by endothelial cells prior to vascular function, Science, 294, 559, 10.1126/science.1063889 McClelland, 2008, Ex vivo conditions for self-replication of human hepatic stem cells, Tissue Eng. C Methods, 14, 341, 10.1089/ten.tec.2008.0073 McDaniell, 2006, NOTCH2 mutations cause Alagille syndrome, a heterogeneous disorder of the notch signaling pathway, Am. J. Hum. Genet., 79, 169, 10.1086/505332 Mesnil, 1987, Cell contact but not junctional communication (dye coupling) with biliary epithelial cells is required for hepatocytes to maintain differentiated functions, Exp. Cell Res., 173, 524, 10.1016/0014-4827(87)90292-8 Messner, 2013, Multi-cell type human liver microtissues for hepatotoxicity testing, Arch. Toxicol, 87, 209, 10.1007/s00204-012-0968-2 Miki, 2011, Hepatic differentiation of human embryonic and induced pluripotent stem cells for regenerative medicine Miki, 2011, Hepatic differentiation of human embryonic stem cells is promoted by three-dimensional dynamic perfusion culture conditions, Tissue Eng. C Methods, 17, 557, 10.1089/ten.tec.2010.0437 Miyazawa, 2005, Effect of mechanical stress imposition on co-culture of hepatic parenchymal and nonparenchymal cells: possibility of stimulating production of regenerating factor, Transplant. Proc., 37, 2398, 10.1016/j.transproceed.2005.03.103 Nejsum, 2007, A molecular mechanism directly linking E-cadherin adhesion to initiation of epithelial cell surface polarity, J. Cell Biol., 178, 323, 10.1083/jcb.200705094 Oude Elferink, 2007, Function and pathophysiological importance of ABCB4 (MDR3 P-glycoprotein), Pflügers Archiv, 453, 601, 10.1007/s00424-006-0062-9 Parviz, 2003, Hepatocyte nuclear factor 4alpha controls the development of a hepatic epithelium and liver morphogenesis, Nat. Genet., 34, 292, 10.1038/ng1175 Reid, 1992, Extracellular matrix gradients in the space of Disse: relevance to liver biology, Hepatology, 15, 1198, 10.1002/hep.1840150635 Rossi, 2001, Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm, Genes Dev., 15, 1998, 10.1101/gad.904601 Roth, 2012, OATPs, OATs and OCTs: the organic anion and cation transporters of the SLCO and SLC22A gene superfamilies, Br. J. Pharmacol., 165, 1260, 10.1111/j.1476-5381.2011.01724.x Rozga, 1993, Development of a hybrid bioartificial liver, Ann. Surg., 217, 502, 10.1097/00000658-199305010-00010 Ruebner, 1990, Development and transformation of the ductal plate in the developing human liver, Pediatr. Pathol., 10, 55, 10.3109/15513819009067096 Sakai, 2010, Comparative analysis of gene expression in rat liver tissue and monolayer- and spheroid-cultured hepatocytes, Cells Tissues Organs, 191, 281, 10.1159/000272316 Sakiyama, 2017, Clinical translation of bioartificial liver support systems with human pluripotent stem cell-derived hepatic cells, World J. Gastroenterol., 23, 1974, 10.3748/wjg.v23.i11.1974 Sakiyama, 2018, Evaluation of the mass transfer rate using computer simulation in a three-dimensional interwoven hollow fiber-type bioartificial liver, Biotechnol. Lett., 40, 1567, 10.1007/s10529-018-2609-1 Sasagawa, 2010, Design of prevascularized three-dimensional cell-dense tissues using a cell sheet stacking manipulation technology, Biomaterials, 31, 1646, 10.1016/j.biomaterials.2009.11.036 Sauer, 2002, Primary human liver cells as source for modular extracorporeal liver support-a preliminary report, Int. J. Artif. Organs, 25, 1001, 10.1177/039139880202501015 Schrode, 1990, Induction of glutamine synthetase in periportal hepatocytes by cocultivation with a liver epithelial cell line, Eur. J. Cell Biol., 53, 35 Schuppan, 1990, Structure of the extracellular matrix in normal and fibrotic liver: collagens and glycoproteins, Semin. Liver Dis., 10, 1, 10.1055/s-2008-1040452 Scott, 2005, Hepatocytes enhance effects of lipopolysaccharide on liver nonparenchymal cells through close cell interactions, Shock, 23, 453, 10.1097/01.shk.0000160939.08385.f1 Shin, 2013, Cellular and molecular basis of liver development, Comp. Physiol., 3, 799, 10.1002/cphy.c120022 Si-Tayeb, 2010, Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells, Hepatology, 51, 297, 10.1002/hep.23354 Song, 2009, Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells, Cell Res., 19, 1233, 10.1038/cr.2009.107 Sorensen, 2015, Liver sinusoidal endothelial cells, Comp. Physiol., 5, 1751, 10.1002/cphy.c140078 Spath, 1998, Hepatocyte nuclear factor 4 provokes expression of epithelial marker genes, acting as a morphogen in dedifferentiated hepatoma cells, J. Cell Biol., 140, 935, 10.1083/jcb.140.4.935 Spray, 1987, Proteoglycans and glycosaminoglycans induce gap junction synthesis and function in primary liver cultures, J. Cell Biol., 105, 541, 10.1083/jcb.105.1.541 Stieger, 2011, The role of the sodium-taurocholate cotransporting polypeptide (NTCP) and of the bile salt export pump (BSEP) in physiology and pathophysiology of bile formation, Handb. Exp. Pharmacol., 205, 10.1007/978-3-642-14541-4_5 Sullivan, 2010, Generation of functional human hepatic endoderm from human induced pluripotent stem cells, Hepatology, 51, 329, 10.1002/hep.23335 Szkolnicka, 2013, Pluripotent stem cell-derived hepatocytes: potential and challenges in pharmacology, Annu. Rev. Pharmacol. Toxicol., 53, 147, 10.1146/annurev-pharmtox-011112-140306 Takayama, 2012, Efficient generation of functional hepatocytes from human embryonic stem cells and induced pluripotent stem cells by HNF4alpha transduction, Mol. Ther., 20, 127, 10.1038/mt.2011.234 Takebe, 2013, Vascularized and functional human liver from an iPSC-derived organ bud transplant, Nature, 499, 481, 10.1038/nature12271 Theard, 2007, Cell polarity development and protein trafficking in hepatocytes lacking E-cadherin/beta-catenin-based adherens junctions, Mol. Biol. Cell, 18, 2313, 10.1091/mbc.e06-11-1040 Thiebaut, 1987, Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues, Proc. Natl. Acad. Sci. U. S. A., 84, 7735, 10.1073/pnas.84.21.7735 Thompson, 2018, Extracorporeal cellular therapy (ELAD) in severe alcoholic hepatitis: a multinational, prospective, controlled, randomized trial, Liver Transplant., 24, 380, 10.1002/lt.24986 Touboul, 2010, Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development, Hepatology, 51, 1754, 10.1002/hep.23506 Tremblay, 2005, Distinct populations of endoderm cells converge to generate the embryonic liver bud and ventral foregut tissues, Dev. Biol., 280, 87, 10.1016/j.ydbio.2005.01.003 Treyer, 2013, Hepatocyte polarity, Comp. Physiol., 3, 243, 10.1002/cphy.c120009 Umeda, 2006, ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation, Cell, 126, 741, 10.1016/j.cell.2006.06.043 Vasconcellos, 2016, Exploring the cell signalling in hepatocyte differentiation, Cell. Signal., 28, 1773, 10.1016/j.cellsig.2016.08.011 Vega-Salas, 1988, Exocytosis of vacuolar apical compartment (VAC): a cell-cell contact controlled mechanism for the establishment of the apical plasma membrane domain in epithelial cells, J. Cell Biol., 107, 1717, 10.1083/jcb.107.5.1717 Wang, 1990, Steps in the morphogenesis of a polarized epithelium. I. Uncoupling the roles of cell-cell and cell-substratum contact in establishing plasma membrane polarity in multicellular epithelial (MDCK) cysts, J. Cell Sci., 95, 137, 10.1242/jcs.95.1.137 Willebrords, 2015, Structure, regulation and function of gap junctions in liver, Cell Commun. Adhes., 22, 29, 10.3109/15419061.2016.1151875