All layers matter: Innovative three-dimensional epithelium-stroma-endothelium intestinal model for reliable permeability outcomes

Kennedy, 1997, Managing the drug discovery/development interface, Drug Discov. Today, 2, 436, 10.1016/S1359-6446(97)01099-4 Li, 2001, Screening for human ADME/Tox drug properties in drug discovery, Drug Discov. Today, 6, 357, 10.1016/S1359-6446(01)01712-3 Dahlgren, 2019, Intestinal permeability and drug absorption: predictive experimental, computational and in vivo approaches, Pharmaceutics, 11, 1, 10.3390/pharmaceutics11080411 Polli, 2008, In vitro studies are sometimes better than conventional human pharmacokinetic in vivo studies in assessing bioequivalence of immediate-release solid oral dosage forms, AAPS J., 10, 289, 10.1208/s12248-008-9027-6 Press, 2008, Permeability for intestinal absorption: Caco-2 assay and related issues, Curr. Drug Metab., 9, 893, 10.2174/138920008786485119 Hilgendorf, 2000, Caco-2 versus Caco-2/HT29-MTX co-cultured cell lines: Permeabilities via diffusion, inside- and outside-directed carrier-mediated transport, J. Pharm. Sci., 89, 63, 10.1002/(SICI)1520-6017(200001)89:1<63::AID-JPS7>3.0.CO;2-6 Chen, 2015, Robust bioengineered 3D functional human intestinal epithelium, Sci. Rep., 5, 13708, 10.1038/srep13708 Fitzgerald, 2015, Life in 3D is never flat: 3D models to optimise drug delivery, J. Control. Release, 215, 39, 10.1016/j.jconrel.2015.07.020 Macedo, 2020, Development of an improved 3D in vitro intestinal model to perform permeability studies of Paracellular compounds, Front. Bioeng. Biotechnol., 8, 10.3389/fbioe.2020.524018 Li, 2013, Development of an improved three-dimensional in vitro intestinal mucosa model for drug absorption evaluation, Tissue Eng. Part C Meth., 19, 708, 10.1089/ten.tec.2012.0463 Madden, 2018, Bioprinted 3D primary human intestinal tissues model aspects of native physiology and ADME/Tox functions, iScience, 2, 156, 10.1016/j.isci.2018.03.015 Pereira, 2015, Dissecting stromal-epithelial interactions in a 3D in vitro cellularized intestinal model for permeability studies, Biomaterials, 56, 36, 10.1016/j.biomaterials.2015.03.054 Yi, 2017, Three-dimensional in vitro gut model on a villi-shaped collagen scaffold, BioChip J., 11, 219, 10.1007/s13206-017-1307-8 Yu, 2014, Three dimensional human small intestine models for ADME-Tox studies, Drug Discov. Today, 19, 1587, 10.1016/j.drudis.2014.05.003 Yu, 2012, In vitro 3D human small intestinal villous model for drug permeability determination, Biotechnol. Bioeng., 109, 2173, 10.1002/bit.24518 Darnell, 2011, Cytochrome P450-dependent metabolism in HepaRG cells cultured in a dynamic three-dimensional bioreactor, Drug Metab. Dispos., 39, 1131, 10.1124/dmd.110.037721 Desrochers, 2014, Tissue-engineered kidney disease models, Adv. Drug Deliv. Rev., 69-70, 67, 10.1016/j.addr.2013.12.002 Pampaloni, 2007, The third dimension bridges the gap between cell culture and live tissue, Nat. Rev. Mol. Cell Biol., 8, 839, 10.1038/nrm2236 Justice, 2009, 3D cell culture opens new dimensions in cell-based assays, Drug Discov. Today, 14, 102, 10.1016/j.drudis.2008.11.006 Chitcholtan, 2013, Differences in growth properties of endometrial cancer in three dimensional (3D) culture and 2D cell monolayer, Exp. Cell Res., 319, 75, 10.1016/j.yexcr.2012.09.012 Basson, 1996, Regulation of human (Caco-2) intestinal epithelial cell differentiation by extracellular matrix proteins, Exp. Cell Res., 225, 301, 10.1006/excr.1996.0180 Hewes, 2020, In vitro models of the small intestine: engineering challenges and engineering solutions, Tissue Eng. B Rev., 26, 313, 10.1089/ten.teb.2019.0334 Snyder, 2020, Materials and microenvironments for engineering the intestinal epithelium, Ann. Biomed. Eng., 48, 1916, 10.1007/s10439-020-02470-8 Castano, 2019, Dynamic photopolymerization produces complex microstructures on hydrogels in a moldless approach to generate a 3D intestinal tissue model, Biofabrication, 11, 10.1088/1758-5090/ab0478 Zhang, 2020, Development of a novel in vitro 3D intestinal model for permeability evaluations, Int. J. Food Sci. Nutr., 71, 549, 10.1080/09637486.2019.1700940 Li, 2018, A fast screening model for drug permeability assessment based on native small intestinal extracellular matrix, RSC Adv., 8, 34514, 10.1039/C8RA05992F Sun, 2002, Comparison of human duodenum and Caco-2 gene expression profiles for 12,000 gene sequences tags and correlation with permeability of 26 drugs, Pharm. Res., 19, 1400, 10.1023/A:1020483911355 Cardoso, 2014, Macrophages stimulate gastric and colorectal cancer invasion through EGFR Y(1086), c-Src, Erk1/2 and Akt phosphorylation and smallGTPase activity, Oncogene, 33, 2123, 10.1038/onc.2013.154 Roulis, 2016, Fibroblasts and myofibroblasts of the intestinal lamina propria in physiology and disease, Differentiation, 92, 116, 10.1016/j.diff.2016.05.002 Olson, 1993, Contraction of collagen gels by intestinal epithelial cells depends on microfilament function, Dig. Dis. Sci., 38, 388, 10.1007/BF01316489 Deanfield, 2007, Endothelial function and dysfunction: testing and clinical relevance, Circulation, 115, 1285, 10.1161/CIRCULATIONAHA.106.652859 Szulcek, 2015, Transient intervals of hyper-gravity enhance endothelial barrier integrity: impact of mechanical and gravitational forces measured electrically, PLoS One, 10, 10.1371/journal.pone.0144269 Mio, 1998, Human bronchial epithelial cells modulate collagen gel contraction by fibroblasts, Am. J. Phys., 274, 119 Montesano, 1988, Transforming growth factor beta stimulates collagen-matrix contraction by fibroblasts: implications for wound healing, Proc. Natl. Acad. Sci. U. S. A., 85, 4894, 10.1073/pnas.85.13.4894 Drygiannakis, 2013, Proinflammatory cytokines induce crosstalk between colonic epithelial cells and subepithelial myofibroblasts: implication in intestinal fibrosis, J. Crohn’s Colitis, 7, 286, 10.1016/j.crohns.2012.04.008 Finesmith, 1990, Fibroblasts from wounds of different stages of repair vary in their ability to contract a collagen gel in response to growth factors, J. Cell. Physiol., 144, 99, 10.1002/jcp.1041440113 Ishikawa, 2017, A 3D epithelial-mesenchymal co-culture model of human bronchial tissue recapitulates multiple features of airway tissue remodeling by TGF-beta1 treatment, Respir. Res., 18, 195, 10.1186/s12931-017-0680-0 Knowles, 2012, Endothelin-1 stimulates colon cancer adjacent fibroblasts, Int. J. Cancer, 130, 1264, 10.1002/ijc.26090 Kurosaka, 1998, Transforming growth factor-beta 1 promotes contraction of collagen gel by bovine corneal fibroblasts through differentiation of myofibroblasts, Invest. Ophthalmol. Vis. Sci., 39, 699 Kowalczyk, 2015, The role of endothelin-1 and endothelin receptor antagonists in inflammatory response and sepsis, Arch. Immunol. Ther. Exp., 63, 41, 10.1007/s00005-014-0310-1 Sawicki, 2005, Interaction of keratinocytes and fibroblasts modulates the expression of matrix metalloproteinases-2 and -9 and their inhibitors, Mol. Cell. Biochem., 269, 209, 10.1007/s11010-005-3178-x Gullberg, 1990, Beta 1 integrin-mediated collagen gel contraction is stimulated by PDGF, Exp. Cell Res., 186, 264, 10.1016/0014-4827(90)90305-T Lagente, 2005, Role of matrix metalloproteinases in the development of airway inflammation and remodeling, Braz. J. Med. Biol. Res., 38, 1521, 10.1590/S0100-879X2005001000009 Nagase, 1999, Matrix metalloproteinases, J. Biol. Chem., 274, 21491, 10.1074/jbc.274.31.21491 Visse, 2003, Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry, Circ. Res., 92, 827, 10.1161/01.RES.0000070112.80711.3D Lopez-Avila, 2008, Methods for detection of matrix metalloproteinases as biomarkers in cardiovascular disease, Clin. Med. Insights: Cardiol., 2, 75 Lijnen, 2001, Plasmin and matrix metalloproteinases in vascular remodeling, Thromb. Haemost., 86, 324, 10.1055/s-0037-1616230 Hinnebusch, 2004, Enterocyte differentiation marker intestinal alkaline phosphatase is a target gene of the gut-enriched Kruppel-like factor, Am. J. Phys., 286, 23 Alpers, 1994, The secretion of intestinal alkaline phosphatase (IAP) from the enterocyte, J. Gastroenterol., 29, 63 Artursson, 1991, Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells, Biochem. Biophys. Res. Commun., 175, 880, 10.1016/0006-291X(91)91647-U Traber, 1992, Sucrase-isomaltase gene expression along crypt-villus axis of human small intestine is regulated at level of mRNA abundance, Am. J. Phys., 262, G123 Suh, 1996, An intestine-specific homeobox gene regulates proliferation and differentiation, Mol. Cell. Biol., 16, 619, 10.1128/MCB.16.2.619 Sato, 2011, Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium, Gastroenteroloy, 141, 1762, 10.1053/j.gastro.2011.07.050 Wikman-Larhed, 1995, Co-cultures of human intestinal goblet (HT29-H) and absorptive (Caco-2) cells for studies of drug and peptide absorption, Eur. J. Pharm. Sci., 3, 171, 10.1016/0928-0987(95)00007-Z Chen, 2010, Defining conditions for the co-culture of Caco-2 and HT29-MTX cells using Taguchi design, J. Pharmacol. Toxicol. Methods, 61, 334, 10.1016/j.vascn.2010.02.004 Cohen, 2016, The clinical consequences of sucrase-isomaltase deficiency, Mol. Cell. Pediatr., 3, 5, 10.1186/s40348-015-0028-0 Gericke, 2016, The multiple roles of sucrase-isomaltase in the intestinal physiology, Mol. Cell. Pediatr., 3, 2, 10.1186/s40348-016-0033-y Estudante, 2013, Intestinal drug transporters: an overview, Adv. Drug Deliv. Rev., 65, 1340, 10.1016/j.addr.2012.09.042 Liu, 2013, The transporters of intestinal tract and techniques applied to evaluate interactions between drugs and transporters, Asian J. Pharmaceut. Sci., 8, 151 Chan, 2004, The ABCs of drug transport in intestine and liver: efflux proteins limiting drug absorption and bioavailability, Eur. J. Pharm. Sci., 21, 25, 10.1016/j.ejps.2003.07.003 Varma, 2010, Targeting intestinal transporters for optimizing oral drug absorption, Curr. Drug Metab., 11, 730, 10.2174/138920010794328850 Muller, 2011, Transporter-mediated drug-drug interactions, Pharmacogenomics, 12, 1017, 10.2217/pgs.11.44 Kunta, 2004, Intestinal drug transporters: in vivo function and clinical importance, Curr. Drug Metab., 5, 109, 10.2174/1389200043489144 Giacomini, 2010, Membrane transporters in drug development, Nat. Rev. Drug Discov., 9, 215, 10.1038/nrd3028 Bruck, 2017, Caco-2 cells - expression, regulation and function of drug transporters compared with human jejunal tissue, Biopharm. Drug Dispos., 38, 115, 10.1002/bdd.2025 Beduneau, 2014, A tunable Caco-2/HT29-MTX co-culture model mimicking variable permeabilities of the human intestine obtained by an original seeding procedure, Eur. J. Pharm. Biopharm., 87, 290, 10.1016/j.ejpb.2014.03.017 Bohets, 2001, Strategies for absorption screening in drug discovery and development, Curr. Top. Med. Chem., 1, 367, 10.2174/1568026013394886 Gerk, 2002, Regulation of expression of the multidrug resistance-associated protein 2 (MRP2) and its role in drug disposition, J. Pharmacol. Exp. Ther., 302, 407, 10.1124/jpet.102.035014 Maubon, 2007, Analysis of drug transporter expression in human intestinal Caco-2 cells by real-time PCR, Fundam. Clin. Pharmacol., 21, 659, 10.1111/j.1472-8206.2007.00550.x Hilgendorf, 2007, Expression of thirty-six drug transporter genes in human intestine, liver, kidney, and organotypic cell lines, Drug Metab. Dispos., 35, 1333, 10.1124/dmd.107.014902 Ogihara, 1999, Peptide transporter in the rat small intestine: ultrastructural localization and the effect of starvation and administration of amino acids, Histochem. J., 31, 169, 10.1023/A:1003515413550 Shu, 2011, Research progress in the organic cation transporters, Zhong Nan Da Xue Xue Bao Yi Xue Ban, 36, 913 Söderholm, 1998, Integrity and metabolism of human ileal mucosa in vitro in the Ussing chamber, Acta Physiol. Scand., 162, 47, 10.1046/j.1365-201X.1998.0248f.x Artursson, 2001, Caco-2 monolayers in experimental and theoretical predictions of drug transport, Adv. Drug Deliv. Rev., 46, 27, 10.1016/S0169-409X(00)00128-9 Sun, 2008, The Caco-2 cell monolayer: usefulness and limitations, Expert Opin. Drug Metab. Toxicol., 4, 395, 10.1517/17425255.4.4.395 Schneider, 2018, Study of mucin turnover in the small intestine by in vivo labeling, Sci. Rep., 8, 5760, 10.1038/s41598-018-24148-x Kim, 2010, Intestinal goblet cells and mucins in health and disease: recent insights and progress, Curr. Gastroenterol. Rep., 12, 319, 10.1007/s11894-010-0131-2 Pontier, 2001, HT29-MTX and Caco-2/TC7 monolayers as predictive models for human intestinal absorption: role of the mucus layer, J. Pharm. Sci., 90, 1608, 10.1002/jps.1111 Wang, 2006, A kinetic study of Rhodamine123 pumping by P-glycoprotein, Biochim. Biophys. Acta Biomembr., 1758, 1671, 10.1016/j.bbamem.2006.06.004 Versantvoort, 2002, Monolayers of IEC-18 cells as an in vitro model for screening the passive transcellular and paracellular transport across the intestinal barrier: comparison of active and passive transport with the human colon carcinoma Caco-2 cell line, Environ. Toxicol. Pharmacol., 11, 335, 10.1016/S1382-6689(01)00122-3 Ruiz, 2009, Induction of intestinal multidrug resistance-associated protein 2 (Mrp2) by spironolactone in rats, Eur. J. Pharmacol., 623, 103, 10.1016/j.ejphar.2009.09.014 Dahan, 2009, Grapefruit juice and its constituents augment colchicine intestinal absorption: potential hazardous interaction and the role of p-glycoprotein, Pharm. Res., 26, 883, 10.1007/s11095-008-9789-7 Lozoya-Agullo, 2015, In situ perfusion model in rat colon for drug absorption studies: comparison with small intestine and Caco-2 cell model, J. Pharm. Sci., 104, 3136, 10.1002/jps.24447 Ben-Chetrit, 2018, 729 DiMarco, 2017, Improvement of paracellular transport in the Caco-2 drug screening model using protein-engineered substrates, Biomaterials, 129, 152, 10.1016/j.biomaterials.2017.03.023 Artursson, 1993, Selective paracellular permeability in two models of intestinal absorption: cultured monolayers of human intestinal epithelial cells and rat intestinal segments, Pharm. Res., 10, 1123, 10.1023/A:1018903931777 Lozoya-Agullo, 2016, Segmental-dependent permeability throughout the small intestine following oral drug administration: single-pass vs Doluisio approach to in-situ rat perfusion, Int. J. Pharm., 515, 201, 10.1016/j.ijpharm.2016.09.061 Lozoya-Agullo, 2017, Investigating drug absorption from the colon: single-pass vs doluisio approaches to in-situ rat large-intestinal perfusion, Int. J. Pharm., 527, 135, 10.1016/j.ijpharm.2017.05.018 Youhanna, 2021, The past, present and future of intestinal in vitro cell Systems for Drug Absorption Studies, J. Pharm. Sci., 110, 50, 10.1016/j.xphs.2020.07.001 Skolnik, 2010, Towards prediction of in vivo intestinal absorption using a 96-well Caco-2 assay, J. Pharm. Sci., 99, 3246, 10.1002/jps.22080 Lozoya-Agullo, 2015, In-situ intestinal rat perfusions for human Fabs prediction and BCS permeability class determination: investigation of the single-pass vs. the Doluisio experimental approaches, Int. J. Pharm., 480, 1, 10.1016/j.ijpharm.2015.01.014 Dahan, 2009, Multiple efflux pumps are involved in the transepithelial transport of colchicine: combined effect of p-glycoprotein and multidrug resistance-associated protein 2 leads to decreased intestinal absorption throughout the entire small intestine, Drug Metab. Dispos., 37, 2028, 10.1124/dmd.109.028282 Varma, 2012, pH-dependent solubility and permeability criteria for provisional biopharmaceutics classification (BCS and BDDCS) in early drug discovery, Mol. Pharm., 9, 1199, 10.1021/mp2004912 Dahlgren, 2015, Direct in vivo human intestinal permeability (Peff) determined with different clinical perfusion and intubation methods, J. Pharm. Sci., 104, 2702, 10.1002/jps.24258 Sun, 2013, Structure-based prediction of human intestinal membrane permeability for rapid in silico BCS classification, Biopharm. Drug Dispos., 34, 321, 10.1002/bdd.1848 Ruiz-Picazo, 2017, Comparison of segmental-dependent permeability in human and in situ perfusion model in rat, Eur. J. Pharm. Sci., 107, 191, 10.1016/j.ejps.2017.06.033 Irvine, 1999, MDCK (Madin-Darby canine kidney) cells: a tool for membrane permeability screening, J. Pharm. Sci., 88, 28, 10.1021/js9803205 Cheng, 2007, Development of in vitro pharmacokinetic screens using Caco-2, human hepatocyte, and Caco-2/human hepatocyte hybrid systems for the prediction of oral bioavailability in humans, J. Biomol. Screen., 12, 1084, 10.1177/1087057107308892 Yazdanian, 1998, Correlating partitioning and Caco-2 cell permeability of structurally diverse small molecular weight compounds, Pharm. Res., 15, 1490, 10.1023/A:1011930411574 Yang, 2007, Biopharmaceutics classification of selected beta-blockers: solubility and permeability class membership, Mol. Pharm., 4, 608, 10.1021/mp070028i Shugarts, 2009, The role of transporters in the pharmacokinetics of orally administered drugs, Pharm. Res., 26, 2039, 10.1007/s11095-009-9924-0