Precision-cut intestinal slices: alternative model for drug transport, metabolism, and toxicology research

References

• Otto W. Versuche und uberledbeudem carcinomgewebe (methoden). Biochemische Zeitschr. 1923;142:317–333.
   Google Scholar
• Ha K. Untersuchungen über den Stoffwechsel der Aminosäuren im Tierkörper. Hoppe-Seyl Z. 1933;217:191.
   Google Scholar
• Krumdieck CL, Dos Santos J, Ho K-J. A new instrument for the rapid preparation of tissue slices. Anal Biochem. 1980;104(1):118–123.
   PubMed Web of Science ®Google Scholar
• Brendel K, Jay Gandolfi A, Krumdieck CL, et al. Tissue slicing and culturing revisited. Trends Pharmacol Sci. 1987;8(1):11–15.
   Web of Science ®Google Scholar
• Vickers AE, Fischer V, Connors S, et al. Cyclosporin A metabolism in human liver, kidney, and intestine slices. Comparison to rat and dog slices and human cell lines. Drug Metab Dispos. 1992;20(6):802–809.
   PubMed Web of Science ®Google Scholar
• Vickers AE, Fisher RL, Brendel K, et al. Sites of biotransformation for the cyclosporin derivative SDZ IMM 125 using human liver and kidney slices and intestine. Comparison with rat liver slices and cyclosporin A metabolism. Drug Metab Dispos. 1995;23(3):327–333.
   PubMed Web of Science ®Google Scholar
• Smith PF, Gandolfi AJ, Krumdieck CL, et al. Dynamic organ culture of precision liver slices for in vitro toxicology. Life Sci. 1985;36(14):1367–1375.
   PubMed Web of Science ®Google Scholar
• Ruegg CE, Gandolfi AJ, Nagle RB, et al. Preparation of positional renal slices for study of cell-specific toxicity. J Pharmacol Methods. 1987;17(2):111–123.
   PubMedGoogle Scholar
• Van De Bovenkamp M, Groothuis GMM, Draaisma AL, et al. Precision-cut liver slices as a new model to study toxicity-induced hepatic stellate cell activation in a physiologic milieu. Toxicological Sci. 2005;85(1):632–638.
   PubMed Web of Science ®Google Scholar
• Martignoni M, Groothuis G, De Kanter R. Comparison of mouse and rat cytochrome P450-mediated metabolism in liver and intestine. Drug Metab Dispos. 2006;34(6):1047–1054.
   PubMed Web of Science ®Google Scholar
• Groothuis GM, de Graaf IA. Precision-cut intestinal slices as in vitro tool for studies on drug metabolism. Curr Drug Metab. 2012;14(1):112–119.
   Web of Science ®Google Scholar
• Westra IM, Oosterhuis D, Groothuis GMM, et al. The effect of antifibrotic drugs in rat precision-cut fibrotic liver slices. Plos One. 2014;9(4):e95462.
   PubMed Web of Science ®Google Scholar
• Westra IM, Oosterhuis D, Groothuis GMM, et al. Precision-cut liver slices as a model for the early onset of liver fibrosis to test antifibrotic drugs. Toxicol Appl Pharmacol. 2014;274(2):328–338.
   PubMed Web of Science ®Google Scholar
• Van De Bovenkamp M, Groothuis GMM, Meijer DKF, et al. Liver fibrosis in vitro: cell culture models and precision-cut liver slices. Toxicol Vitro. 2007;21(4):545–557.
   PubMed Web of Science ®Google Scholar
• Oenema TA, Maarsingh H, Smit M, et al. Bronchoconstriction induces TGF-β release and airway remodelling in guinea pig lung slices. Plos One. 2013;8(6):e65580.
   Google Scholar
• Schlepütz M, Rieg AD, Seehase S, et al. Neurally mediated airway constriction in human and other species: a comparative study using precision-cut lung slices (PCLS). Plos One. 2012;7(10):e47344.
   Google Scholar
• Lavoie TL, Krishnan R, Siegel HR, et al. Dilatation of the constricted human airway by tidal expansion of lung parenchyma. Am J Respir Crit Care Med. 2012;186(3):225–232.
   PubMed Web of Science ®Google Scholar
• Groothuis GMM, Casini A, Meurs H, et al. Chapter 3 translational research in pharmacology and toxicology using precision-cut tissue slices [Internet]. In: Coleman R, editor. Human-based systems for translational research. London: The Royal Society of Chemistry; 2015. p. 38–65. http://pubs.rsc.org/en/content/ebook/978-1-84973-825-5#!divbookcontent
   Google Scholar
• Fisher RL, Vickers AEM. Preparation and culture of precision-cut organ slices from human and animal. Xenobiotica. 2013;43(1):8–14.
   PubMed Web of Science ®Google Scholar
• De Kanter R, Tuin A, Van De Kerkhof E, et al. A new technique for preparing precision-cut slices from small intestine and colon for drug biotransformation studies. J Pharmacol Toxicol Methods. 2005;51(1):65–72.
   PubMedGoogle Scholar
• Vickers AEM, Zollinger M, Dannecker R, et al. In vitro metabolism of tegaserod in human liver and intestine: assessment of drug interactions. Drug Metab Dispos. 2001;29(10):1269–1276.
   PubMed Web of Science ®Google Scholar
• Malfatti MA, Connors MS, Mauthe RJ, et al. The capability of rat colon tissue slices to metabolize the cooked-food carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Cancer Res. 1996;56(11):2550–2555.
   PubMed Web of Science ®Google Scholar
• De Kanter R, De Jager MH, Draaisma AL, et al. Drug-metabolizing activity of human and rat liver, lung, kidney and intestine slices. Xenobiotica. 2002;32(5):349–362.
   PubMed Web of Science ®Google Scholar
• Lerche-Langrand C, Toutain HJ. Precision-cut liver slices: characteristics and use for in vitro pharmaco-toxicology. Toxicology. 2000;153(1–3):221–253.
   PubMed Web of Science ®Google Scholar
• De Kanter R, Monshouwer M, Meijer DK, et al. Precision-cut organ slices as a tool to study toxicity and metabolism of xenobiotics with special reference to non-hepatic tissues. Curr Drug Metab. 2002 Feb;3(1):39–59.
   PubMed Web of Science ®Google Scholar
• Van De Kerkhof EG, Ungell A-LB, Sjöberg ÅK, et al. Innovative methods to study human intestinal drug metabolism in vitro: precision-cut slices compared with ussing chamber preparations. Drug Metab Dispos. 2006;34(11):1893–1902.
   PubMed Web of Science ®Google Scholar
• Van De Kerkhof EG, de Graaf IAM, Ungell A-LB, et al. Induction of metabolism and transport in human intestine: validation of precision-cut slices as a tool to study induction of drug metabolism in human intestine in vitro. Drug Metab Dispos. 2008;36(3):604–613.
   PubMed Web of Science ®Google Scholar
• Punyadarsaniya D, Winter C, Mork A-K, et al. Precision-cut intestinal slices as a culture system to analyze the infection of differentiated intestinal epithelial cells by avian influenza viruses. J Virol Methods. 2015;212:71–75.
   PubMed Web of Science ®Google Scholar
• de Graaf IAM, Olinga P, De Jager MH, et al. Preparation and incubation of precision-cut liver and intestinal slices for application in drug metabolism and toxicity studies. Nat Protoc. 2010;5(9):1540–1551.
   PubMed Web of Science ®Google Scholar
• Brouwer KLR, Keppler D, Hoffmaster KA, et al. In vitro methods to support transporter evaluation in drug discovery and development. Clin Pharmacol Ther. 2013;94(1):95–112.
   PubMed Web of Science ®Google Scholar
• Kis O, Zastre J, Hoque MT, et al. Role of drug efflux and uptake transporters in atazanavir intestinal permeability and drug-drug interactions. Pharm Res. 2013;30(4):1050–1064.
   PubMed Web of Science ®Google Scholar
• Rozehnal V, Nakai D, Hoepner U, et al. Human small intestinal and colonic tissue mounted in the Ussing chamber as a tool for characterizing the intestinal absorption of drugs. Eur J Pharm Sci. 2012;46(5):367–373.
   PubMed Web of Science ®Google Scholar
• Ellis LCJ, Hawksworth GM, Weaver RJ. ATP-dependent transport of statins by human and rat MRP2/Mrp2. Toxicol Appl Pharmacol. 2013;269(2):187–194.
   PubMed Web of Science ®Google Scholar
• Li M, Si L, Pan H, et al. Excipients enhance intestinal absorption of ganciclovir by P-gp inhibition: assessed in vitro by everted gut sac and in situ by improved intestinal perfusion. Int J Pharm. 2011;403(1–2):37–45.
   PubMed Web of Science ®Google Scholar
• The International Transporter Consortium. Membrane transporters in drug development. Nat Rev Drug Discov. 2010;9(3):215–236.
   PubMed Web of Science ®Google Scholar
• Hu M, Ling J, Lin H, et al. Use of caco-2 cell monolayers to study drug absorption and metabolism. In: Yan Z, Caldwell G, editors. Optimization in drug discovery. New York: Humana Press; 2004. p. 19–35.
   Google Scholar
• Kamiyama E, Sugiyama D, Nakai D, et al. Culture period-dependent change of function and expression of ATP-binding cassette transporters in caco-2 cells. Drug Metab Dispos. 2009;37(9):1956–1962.
   PubMed Web of Science ®Google Scholar
• Siissalo S, Zhang H, Stilgenbauer E, et al. The expression of most udp-glucuronosyltransferases (UGTs) is increased significantly during caco-2 cell differentiation, whereas UGT1A6 is highly expressed also in undifferentiated cells. Drug Metab Dispos. 2008;36(11):2331–2336.
   PubMed Web of Science ®Google Scholar
• Sato T, Vries RG, Snippert HJ, et al. Single Lgr5 stem cells build crypt–villus structures in vitro without a mesenchymal niche. Nature. 2009;459(7244):262–265.
   PubMed Web of Science ®Google Scholar
• Pham BT, Van Haaften WT, Oosterhuis D, et al. Precision-cut rat, mouse, and human intestinal slices as novel models for the early-onset of intestinal fibrosis. Physiol Rep. 2015;3(4):e12323.
   Google Scholar
• Russell WMS, Burch RL The principles of humane experimental technique. Hertfordshire: Universities Federation for Animal Welfare Wheathampstead. 1959.
   Google Scholar
• Van Der Logt EMJ, Blokzijl T, Van Der Meer R, et al. Westernized high-fat diet accelerates weight loss in dextran sulfate sodium-induced colitis in mice, which is further aggravated by supplementation of heme. J Nutr Biochem. 2013;24(6):1159–1165.
   PubMed Web of Science ®Google Scholar
• Wang WP, Guo X, Koo MWL, et al. Protective role of heme oxygenase-1 on trinitrobenzene sulfonic acid-induced colitis in rats. Am J Physiol Gastrointest Liver Physiol. 2001 Aug;281(2):G586–G594.
   Google Scholar
• Bertrand B, Stefan L, Pirrotta M, et al. Caffeine-based gold(I) N-heterocyclic carbenes as possible anticancer agents: synthesis and biological properties. Inorg Chem. 2014;53(4):2296–2303.
   PubMed Web of Science ®Google Scholar
• De Kanter R, Monshouwer M, Draaisma AL, et al. Prediction of whole-body metabolic clearance of drugs through the combined use of slices from rat liver, lung, kidney, small intestine and colon. Xenobiotica. 2004;34(3):229–241.
   PubMed Web of Science ®Google Scholar
• Martignoni M, Groothuis GM, De Kanter R. Species differences between mouse, rat, dog, monkey and human CYP-mediated drug metabolism, inhibition and induction. Expert Opin Drug Metab Toxicol. 2006;2(6):875–894.
   PubMed Web of Science ®Google Scholar
• Van De Kerkhof EG, de Graaf IA, Groothuis GM. In vitro methods to study intestinal drug metabolism. Curr Drug Metab. 2007;8(7):658–675.
   PubMed Web of Science ®Google Scholar
• Van Midwoud PM, Merema MT, Verpoorte E, et al. A microfluidic approach for in vitro assessment of interorgan interactions in drug metabolism using intestinal and liver slices. Lab Chip. 2010;10(20):2778–2786.
   PubMed Web of Science ®Google Scholar
• Li M, Si LQ, Pan HP, et al. Excipients enhance intestinal absorption of ganciclovir by P-gp inhibition: assessed in vitro by everted gut sac and in situ by improved intestinal perfusion. Int J Pharm. 2011;403(12):37–45.
   PubMed Web of Science ®Google Scholar
• Parsa A, Saadati R, Abbasian Z, et al. Enhanced permeability of etoposide across everted sacs of rat small intestine by vitamin E-TPGS. Iran J Pharm Res. 2013; Winter 12(Suppl):37–46.
   PubMedGoogle Scholar
• Van De Kerkhof EG, de Graaf IAM, De Jager MH, et al. Induction of phase I and II drug metabolism in rat small intestine and colon in vitro. Drug Metab Dispos. 2007;35(6):898–907.
   PubMed Web of Science ®Google Scholar
• Van De Kerkhof EG, de Graaf IAM, De Jager MH, et al. Characterization of rat small intestinal and colon precision-cut slices as an in vitro system for drug metabolism and induction studies. Drug Metab Dispos. 2005;33(11):1613–1620.
   PubMed Web of Science ®Google Scholar
• Roskott AM, Nieuwenhuijs VB, Leuvenink HG, et al. Reduced ischemia-reoxygenation injury in rat intestine after luminal preservation with a tailored solution. Transplantation. 2010;90(6):622–629.
   PubMed Web of Science ®Google Scholar
• Li M, de Graaf IAM, De Jager MH, et al. Rat precision-cut intestinal slices to study P-gp activity and the potency of its inhibitors ex vivo. Toxicol Vitro. 2015;29(5):1070–1078.
   PubMed Web of Science ®Google Scholar
• Possidente M, Dragoni S, Franco G, et al. Rat intestinal precision-cut slices as an in vitro model to study xenobiotic interaction with transporters. Eur J Pharmaceutics Biopharmaceutics. 2011;79(2):343–348.
   PubMed Web of Science ®Google Scholar
• Khan AA, Chow ECY, Porte RJ, et al. Expression and regulation of the bile acid transporter, OSTα-OSTβ in rat and human intestine and liver. Biopharm Drug Dispos. 2009;30(5):241–258.
   PubMed Web of Science ®Google Scholar
• Khan AA, Chow ECY, Van Loenen-Weemaes A-M, et al. Comparison of effects of VDR versus PXR, FXR and GR ligands on the regulation of CYP3A isozymes in rat and human intestine and liver. Eur J Pharm Sci. 2009;37(2):115–125.
   PubMed Web of Science ®Google Scholar
• Khan AA, Dragt BS, Porte RJ, et al. Regulation of VDR expression in rat and human intestine and liver – consequences for CYP3A expression. Toxicol Vitro. 2010;24(3):822–829.
   PubMed Web of Science ®Google Scholar
• Khan AA, Chow ECY, Porte RJ, et al. The role of lithocholic acid in the regulation of bile acid detoxication, synthesis, and transport proteins in rat and human intestine and liver slices. Toxicol Vitro. 2011;25(1):80–90.
   PubMed Web of Science ®Google Scholar
• Niu X. Precision-cut intestinal slices as an ex vivo model to study NSAID-induced intestinal toxicity (chapter 6). Groningen: University of Groningen; 2014.
   Google Scholar
• Takano M, Yumoto R, Murakami T. Expression and function of efflux drug transporters in the intestine. Pharmacol Ther. 2006;109(1–2):137–161.
   PubMed Web of Science ®Google Scholar
• MacLean C, Moenning U, Reichel A, et al. Closing the gaps: A full scan of the intestinal expression of P-glycoprotein, breast cancer resistance protein, and multidrug resistance-associated protein 2 in male and female rats. Drug Metab Dispos. 2008;36(7):1249–1254.
   PubMed Web of Science ®Google Scholar
• Sekine S, Ito K, Saeki J, et al. Interaction of Mrp2 with radixin causes reversible canalicular Mrp2 localization induced by intracellular redox status. Biochimica Biophysica Acta (BBA) Molecular Basis Disease. 2011;1812(11):1427–1434.
   PubMed Web of Science ®Google Scholar
• Knutson T, Fridblom P, Ahlström H, et al. Increased understanding of intestinal drug permeability determined by the LOC-I-GUT approach using multislice computed tomography. Mol Pharm. 2009;6(1):2–10.
   PubMed Web of Science ®Google Scholar
• Fisher MB, Labissiere G. The role of the intestine in drug metabolism and pharmacokinetics: an industry perspective. Curr Drug Metab. 2007 Oct;8(7):694–699.
   PubMed Web of Science ®Google Scholar
• Laffont CM, Toutain P-L, Alvinerie M, et al. Intestinal secretion is a major route for parent ivermectin elimination in the rat. Drug Metab Dispos. 2002;30(6):626–630.
   PubMed Web of Science ®Google Scholar
• Chosidow O, Delchier J-C, Chaumette M-T, et al. Intestinal involvement in drug-induced toxic epidermal necrolysis. The Lancet. 1991;337(8746):928.
   PubMed Web of Science ®Google Scholar
• Niu X, De Graaf IAM, Groothuis GMM. Evaluation of the intestinal toxicity and transport of xenobiotics utilizing precision-cut slices. Xenobiotica. 2013;43(1):73–83.
   PubMed Web of Science ®Google Scholar
• Li M, Vokral I, de Graaf IAM, et al. Precision-cut intestinal slices as ex vivo model to study the uptake of bile acids by ASBT in the intestine. ISSX Online Abstracts 2015;10(Suppl 1):37.
   Google Scholar
• Drozdzik M, Gröer C, Penski J, et al. Protein abundance of clinically relevant multidrug transporters along the entire length of the human intestine. Mol Pharm. 2014;11(10):3547–3555.
   PubMed Web of Science ®Google Scholar
• Sugimoto H, Hirabayashi H, Kimura Y, et al. Quantitative investigation of the impact of P-glycoprotein inhibition on drug transport across blood-brain barrier in rats. Drug Metab Dispos. 2011;39(1):8–14.
   PubMed Web of Science ®Google Scholar
• Li M, de Graaf I, De Jager M, et al. Human PCIS as ex vivo model to study the interplay between P-gp and CYP3A4 in the intestine. ISSX Online Abstracts. 2014;2(Supplement 9):P268.
   Google Scholar
• Niu X, de Graaf IAM, Van Der Bij HA, et al. Precision cut intestinal slices are an appropriate ex vivo model to study NSAID-induced intestinal toxicity in rats. Toxicol Vitro. 2014;28(7):1296–1305.
   PubMed Web of Science ®Google Scholar
• Niu X, De Graaf IAM, Van De Vegte D, et al. Consequences of Mrp2 deficiency for diclofenac toxicity in the rat intestine ex vivo. Toxicol Vitro. 2015;29(1):168–175.
   PubMed Web of Science ®Google Scholar
• Niu X, de Graaf IM, Langelaar-Makkinje M, et al. Diclofenac toxicity in human intestine ex vivo is not related to the formation of intestinal metabolites. Arch Toxicol. 2015;89(1):107–119.
   PubMed Web of Science ®Google Scholar
• Siissalo S, De Waard H, De Jager MH, et al. Nanoparticle formulation of a poorly soluble cannabinoid receptor 1 antagonist improves absorption by rat and human intestine. Drug Metab Dispos. 2013 Aug 1;41(8):1557–1565
   PubMed Web of Science ®Google Scholar
• Benet LZ. The drug transporter-metabolism alliance: uncovering and defining the interplay. Mol Pharm. 2009;6(6):1631–1643.
   PubMed Web of Science ®Google Scholar
• Chassany O, Michaux A, Bergmann J. Drug-induced diarrhoea. Drug-Safety. 2000;22(1):53–72.
   PubMed Web of Science ®Google Scholar
• Graham DY, Opekun AR, Willingham FF, et al. Visible small-intestinal mucosal injury in chronic NSAID users. Clin Gastroenterol Hepatol. 2005;3(1):55–59.
   PubMed Web of Science ®Google Scholar
• Maiden L, Thjodleifsson B, Theodors A, et al. A quantitative analysis of nsaid-induced small bowel pathology by capsule enteroscopy. Gastroenterology. 2005;128(5):1172–1178.
   PubMed Web of Science ®Google Scholar
• Lim YJ, Yang C-H. Non-steroidal anti-inflammatory drug-induced enteropathy. Clin Endosc. 2012;45(2):138–144.
   PubMedGoogle Scholar
• De Kanter R. Human and rat organ slices: a tool to study drug metabolism and toxicity. Groningen: University of Groningen; 2002.
   Google Scholar
• Zusman I, Zimber A. Ultrastructural changes in rat colorectal epithelium and tumors after treatment with N-methyl-N’-nitro-N-nitrosoguanidine and secondary bile acids. Acta Anat. 1991;141(3):282–288.
   PubMedGoogle Scholar
• Van Haaften WT, Pham BT, Oosterhuis D, et al. Tu1238 fibrotic human precision-cut intestinal slices: a new ex vivo model for established intestinal fibrosis. Gastroenterology. 2014;146(5, Supplement 1):S791.
   Google Scholar
• Trapecar M, Goropevsek A, Gorenjak M, et al. A co-culture model of the developing small intestine offers new insight in the early immunomodulation of enterocytes and macrophages by Lactobacillus spp. through stat1 and nf-kb p65 translocation. Plos One. 2014;9(1):e86297.
   Google Scholar
• Vickers AEM, Fisher RL. Evaluation of drug-induced injury and human response in precision-cut tissue slices. Xenobiotica. 2013;43(1):29–40.
   PubMed Web of Science ®Google Scholar
• Roskott AMC, Nieuwenhuijs VB, Dijkstra G, et al. Small bowel preservation for intestinal transplantation: a review. Transpl Int. 2011;24(2):107–131.
   PubMed Web of Science ®Google Scholar
• Grabinger T, Luks L, Kostadinova F, et al. Ex vivo culture of intestinal crypt organoids as a model system for assessing cell death induction in intestinal epithelial cells and enteropathy. Cell Death Dis. 2014;5:e1228.
   PubMed Web of Science ®Google Scholar
• Kent TH, Cardelli RM, Stamler FW. Small intestinal ulcers and intestinal flora in rats given indomethacin. Am J Pathol. 1969;54(2):237–249.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Ingber DE. Gut-on-a-chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr Biol. 2013;5(9):1130–1140.
   Google Scholar
• Kim HJ, Huh D, Hamilton G, et al. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip. 2012;12(12):2165–2174.
   PubMed Web of Science ®Google Scholar