Modulation of expression/function of intestinal P-glycoprotein under disease states

References

• Takano M, Yumoto R, Murakami T. Expression and function of efflux drug transporters in the intestine. Pharmacol Ther. 2006;109(1–2):137–161.
   Google Scholar
• Murakami T, Takano M. Intestinal efflux transporters and drug absorption. Expert Opin Drug Metab Toxicol. 2008;4(7):923–939.
   Google Scholar
• Wacher VJ, Wu CY, Benet LZ. Overlapping substrate specificities and tissue distribution of cytochrome P450 3A and P-glycoprotein: implications for drug delivery and activity in cancer chemotherapy. Mol Carcinog. 1995;13(3):129–134.
   Google Scholar
• Mouly S, Paine MF. P-glycoprotein increases from proximal to distal regions of human small intestine. Pharm Res. 2003;20(10):1595–1599.
   Google Scholar
• Paine MF, Khalighi M, Fisher JM, et al. Characterization of interintestinal and intraintestinal variations in human CYP3A-dependent metabolism. J Pharmacol Exp Ther. 1997;283(3):1552–1562.
   Google Scholar
• Paine MF, Ludington SS, Chen ML, et al. Do men and women differ in proximal small intestinal CYP3A or P-glycoprotein expression? Drug Metab Dispos. 2005;33(3):426–433.
   Google Scholar
• Gröer C, Brück S, Lai Y, et al. LC-MS/MS-based quantification of clinically relevant intestinal uptake and efflux transporter proteins. J Pharm Biomed Anal. 2013;85:253–261.
   Google Scholar
• Gröer C, Busch D, Patrzyk M, et al. Absolute protein quantification of clinically relevant cytochrome P450 enzymes and UDP-glucuronosyltransferases by mass spectrometry-based targeted proteomics. J Pharm Biomed Anal. 2014;100:393–401.
   Google Scholar
• Harwood MD, Achour B, Russell MR, et al. Application of an LC-MS/MS method for the simultaneous quantification of human intestinal transporter proteins absolute abundance using a QconCAT technique. J Pharm Biomed Anal. 2015;110:27–33.
   Google Scholar
• Busch D, Fritz A, Partecke LI, et al. LC-MS/MS method for the simultaneous quantification of intestinal CYP and UGT activity. J Pharm Biomed Anal. 2018;155:194–201.
   Google Scholar
• Harwood MD, Zhang M, Pathak SM, et al. The regional-specific relative and absolute expression of gut transporters in adult Caucasians: A meta-analysis. Drug Metab Dispos. 2019;47(8):854–864.
   Google Scholar
• Yumoto R, Murakami T, Nakamoto Y, et al. Transport of rhodamine 123, a P-glycoprotein substrate, across rat intestine and Caco-2 cell monolayers in the presence of cytochrome P-450 3A-related compounds. J Pharmacol Exp Ther. 1999;289(1):149–155.
   Google Scholar
• Wada S, Kano T, Mita S, et al. The role of inter-segmental differences in P-glycoprotein expression and activity along the rat small intestine in causing the double-peak phenomenon of substrate plasma concentration. Drug Metab Pharmacokinet. 2013;28(2):98–103.
   Google Scholar
• Wu CY, Benet LZ. Predicting drug disposition via application of BCS: transport/absorption/elimination interplay and development of a biopharmaceutics drug disposition classification system. Pharm Res. 2005;22(1):11–23.
   Google Scholar
• Debono M, Ghobadi C, Rostami-Hodjegan A, et al. Modified-release hydrocortisone to provide circadian cortisol profiles. J Clin Endocrinol Metab. 2009;94(5):1548–1554.
   Google Scholar
• Chan S, Debono M. Replication of cortisol circadian rhythm: new advances in hydrocortisone replacement therapy. Ther Adv Endocrinol Metab. 2010;1(3):129–138.
   Google Scholar
• Chung S, Son GH, Kim K. Circadian rhythm of adrenal glucocorticoid: its regulation and clinical implications. Biochim Biophys Acta. 2011;1812:581–591.
   Google Scholar
• Savvidis C, Koutsilieris M. Circadian rhythm disruption in cancer biology. Mol Med. 2012;18:1249–1260.
   Google Scholar
• Sephton SE, Lush E, Dedert EA, et al. Diurnal cortisol rhythm as a predictor of lung cancer survival. Brain Behav Immun. 2013;30(Suppl):S163–170.
   Google Scholar
• Lemmer B. Relevance for chronopharmacology in practical medicine. Semin Perinatol. 2000;24(4):280–290.
   Google Scholar
• Ballesta A, Innominato PF, Dallmann R, et al. Systems chronotherapeutics. Pharmacol Rev. 2017;69(2):161–199.
   Google Scholar
• Iwasaki M, Koyanagi S, Suzuki N, et al. Circadian modulation in the intestinal absorption of P-glycoprotein substrates in monkeys. Mol Pharmacol. 2015;88(1):29–37.
   Google Scholar
• Tada H, Satoh S, Iinuma M, et al. Chronopharmacokinetics of tacrolimus in kidney transplant recipients: occurrence of acute rejection. J Clin Pharmacol. 2003;43(8):859–865.
   Google Scholar
• Iwahori T, Takeuchi H, Matsuno N, et al. Pharmacokinetic differences between morning and evening administration of cyclosporine and tacrolimus therapy. Transplant Proc. 2005;37(4):1739–1740.
   Google Scholar
• Baraldo M, Furlanut M. Chronopharmacokinetics of ciclosporin and tacrolimus. Clin Pharmacokinet. 2006;45(8):775–788.
   Google Scholar
• Park SI, Felipe CR, Pinheiro-Machado PG, et al. Circadian and time-dependent variability in tacrolimus pharmacokinetics. Fundam Clin Pharmacol. 2007;21(2):191–197.
   Google Scholar
• Satoh S, Tada H, Murakami M, et al. Circadian pharmacokinetics of mycophenolic Acid and implication of genetic polymorphisms for early clinical events in renal transplant recipients. Transplantation. 2006;82(4):486–493.
   Google Scholar
• Yokooji T, Kameda Y, Utsumi M, et al. Interaction of hydrophobic components in female urine before and after childbirth with P-glycoprotein in vitro. Pharmazie. 2014;69(6):430–436.
   Google Scholar
• Okyar A, Dressler C, Hanafy A, et al. Circadian variations in exsorptive transport: in situ intestinal perfusion data and in vivo relevance. Chronobiol Int. 2012;29(4):443–453.
   Google Scholar
• Okyar A, Swati A, Kumar SA, et al. Sex-, feeding-, and circadian time-dependency of P-glycoprotein expression and activity - implications for mechanistic pharmacokinetics modeling. Sci Rep. 2019;9:10505.
   Google Scholar
• Ohdo S. Chronotherapeutic strategy: rhythm monitoring, manipulation and disruption. Adv Drug Deliv Rev. 2010;62(9–10):859–875.
   Google Scholar
• Blech S, Ebner T, Ludwig-Schwellinger E, et al. The metabolism and disposition of the oral direct thrombin inhibitor, dabigatran, in humans. Drug Metab Dispos. 2008;36(2):386–399.
   Google Scholar
• Gouin-Thibault I, Delavenne X, Blanchard A, et al. Interindividual variability in dabigatran and rivaroxaban exposure: contribution of ABCB1 genetic polymorphisms and interaction with clarithromycin. J Thromb Haemost. 2017;15(2):273–283.
   Google Scholar
• Zhao Y, Hu ZY. Physiologically based pharmacokinetic modelling and in vivo [I]/K(i) accurately predict P-glycoprotein-mediated drug-drug interactions with dabigatran etexilate. Br J Pharmacol. 2014;171(4):1043–1053.
   Google Scholar
• Härtter S, Koenen-Bergmann M, Sharma A, et al. Decrease in the oral bioavailability of dabigatran etexilate after co-medication with rifampicin. Br J Clin Pharmacol. 2012;74(3):490–500.
   Google Scholar
• Finch CK, Chrisman CR, Baciewicz AM, et al. Rifampin and rifabutin drug interactions an update. Arch Intern Med. 2002;162(9):985–992.
   Google Scholar
• Chen J, Raymond K. Roles of rifampicin in drug-drug interactions: underlying molecular mechanisms involving the nuclear pregnane X receptor. Ann Clin Microbiol Antimicrob. 2006;5:3.
   Google Scholar
• van de Kerkhof EG, de Graaf IA, Ungell AL, 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.
   Google Scholar
• Brueck S, Bruckmueller H, Wegner D, et al. Transcriptional and post-transcriptional regulation of duodenal P-glycoprotein and MRP2 in healthy human subjects after chronic treatment with rifampin and carbamazepine. Mol Pharm. 2019;16(9):3823–3830.
   Google Scholar
• Tan H, Xu C, Zeng H, et al. SUMOylation of pregnane X receptor suppresses rifampicin-induced CYP3A4 and P-gp expression and activity in LS174T cells. J Pharmacol Sci. 2016;130(2):66–71.
   Google Scholar
• Chai F, Sun L, Ding Y, et al. A solid self-nanoemulsifying system of the BCS class IIb drug dabigatran etexilate to improve oral bioavailability. Nanomedicine (Lond). 2016;11(14):1801–1816.
   Google Scholar
• Hu M, Zhang J, Ding R, et al. Improved oral bioavailability and therapeutic efficacy of dabigatran etexilate via Soluplus-TPGS binary mixed micelles system. Drug Dev Ind Pharm. 2017;43(4):687–697.
   Google Scholar
• Ellens H, Deng S, Coleman J, et al. Application of receiver operating characteristic analysis to refine the prediction of potential digoxin drug interactions. Drug Metab Dispos. 2013;41(7):1367–1374.
   Google Scholar
• U.S. Food & Drug Administration. Drug development and drug interactions: table of substrates, inhibitors and inducers. [cited 2016 Sept 26]. https://www.fda.gov/drugs/drug-interactions-labeling/drug-development-and-drug-interactions-table-substrates-inhibitors-and-inducers.
   Google Scholar
• Japan Pharmaceuticals and Medical Devices Agency (PMDA). Guideline on drug interactions for drug development and appropriate provision of information.[cited 2019 Feb 08]. https://www.pmda.go.jp/files/000228122.pdf.
   Google Scholar
• Marcus FI. Pharmacokinetic interactions between digoxin and other drugs. Am Coil Cardio. 1985;5:82A–90A.
   Google Scholar
• Ebner T, Ishiguro N, Taub ME. The use of transporter probe drug cocktails for the assessment of transporter-based drug-drug interactions in a clinical setting-proposal of a four component transporter cocktail. J Pharm Sci. 2015;104(9):3220–3228.
   Google Scholar
• Prueksaritanont T, Tatosian DA, Chu X, et al. Validation of a microdose probe drug cocktail for clinical drug interaction assessments for drug transporters and CYP3A. Clin Pharmacol Ther. 2017;101(4):519–530.
   Google Scholar
• Stopfer P, Giessmann T, Hohl K, et al. Optimization of a drug transporter probe cocktail: potential screening tool for transporter-mediated drug-drug interactions. Br J Clin Pharmacol. 2018;84(9):1941–1949.
   Google Scholar
• Friche E, Jensen PB, Sehested M, et al. The solvents cremophor EL and Tween 80 modulate daunorubicin resistance in the multidrug resistant Ehrlich ascites tumor. Cancer Commun. 1990;2(9):297–303.
   Google Scholar
• Rischin D, Webster LK, Millward MJ, et al. Cremophor pharmacokinetics in patients receiving 3-, 6-, and 24-hour infusions of paclitaxel. J Natl Cancer Inst. 1996;88(18):1297–1301.
   Google Scholar
• Al-Ali AAA, Steffansen B, Holm R, et al. Nonionic surfactants increase digoxin absorption in Caco-2 and MDCKII MDR1 cells: impact on P-glycoprotein inhibition, barrier function, and repeated cellular exposure. Int J Pharm. 2018;551(1–2):270–280.
   Google Scholar
• Hugger ED, Audus KL, Borchardt RT. Effects of poly(ethylene glycol) on efflux transporter activity in Caco-2 cell monolayers. J Pharm Sci. 2002;91(9):1980–1990.
   Google Scholar
• Hodaei D, Baradaran B, Valizadeh H, et al. Effects of polyethylene glycols on intestinal efflux pump expression and activity in Caco-2 cells. Braz J Pharm Sci. 2015;51(3):745–753.
   Google Scholar
• Mai Y, Dou L, Murdan S, et al. An animal’s sex influences the effects of the excipient PEG 400 on the intestinal P-gp protein and mRNA levels, which has implications for oral drug absorption. Eur J Pharm Sci. 2018;120:53–60.
   Google Scholar
• Gurjar R, Chan CYS, Curley P, et al. Inhibitory effects of commonly used excipients on P-glycoprotein in vitro. Mol Pharm. 2018;15(11):4835–4842.
   Google Scholar
• Woodcock DM, Linsenmeyer ME, Chojnowski G, et al. Reversal of multidrug resistance by surfactants. Br J Cancer. 1992;66(1):62–68.
   Google Scholar
• Fatouros DG, Karpf DM, Nielsen FS, et al. Clinical studies with oral lipid based formulations of poorly soluble compounds. Ther Clin Risk Manag. 2007;3(4):591–604.
   Google Scholar
• Zanchetta B, Chaud MV, Santana MHA. Self-emulsifying drug delivery systems (SEDDS) in pharmaceutical development. J Adv Chem Eng. 2015;5:130.
   Google Scholar
• Zhang X, Xing X, Zhao Y, et al. Pharmaceutical dispersion techniques for dissolution and bioavailability enhancement of poorly water-soluble drugs. Pharmaceutics. 2018;10:74.
   Google Scholar
• Loftsson T. Excipient pharmacokinetics and profiling. Int J Pharm. 2015;480(1–2):48–54.
   Google Scholar
• Nakanishi T, Tamai I. Interaction of drug or food with drug transporters in intestine and liver. Curr Drug Metab. 2015;16(9):753–764.
   Google Scholar
• Dewanjee S, Dua TK, Bhattacharjee N, et al. Natural products as alternative choices for P-glycoprotein (P-gp) inhibition. Molecules. 2017;22(6):871.
   Google Scholar
• Meng C, Zhou S-Y, Fabriaga E, et al. Food-drug interactions precipitated by fruit juices other than grapefruit juice: an update review. J Food Drug Anal. 2018;26:ss61–ss71.
   Google Scholar
• Alvarez AI, Real R, Pérez M, et al. Modulation of the activity of ABC transporters (P-glycoprotein, MRP2, BCRP) by flavonoids and drug response. J Pharm Sci. 2010;99(2):598–617.
   Google Scholar
• Edgar B, Bailey D, Bergstrand R, et al. Acute effects of drinking grapefruit juice on the pharmacokinetics and dynamics of felodipine–and its potential clinical relevance. Eur J Clin Pharmacol. 1992;42(3):313–317.
   Google Scholar
• Ducharme MP, Warbasse LH, Edwards DJ. Disposition of intravenous and oral cyclosporine after administration with grapefruit juice. Clin Pharmacol Ther. 1995;57(5):485–491.
   Google Scholar
• Ducharme MP, Provenzano R, Dehoorne-Smith M, et al. Trough concentrations of cyclosporine in blood following administration with grapefruit juice. Br J Clin Pharmacol. 1993;36(5):457–459.
   Google Scholar
• Edwards DJ, Fitzsimmons ME, Schuetz EG, et al. 6ʹ,7ʹ-Dihydroxybergamottin in grapefruit juice and seville orange juice: effects on cyclosporine disposition, enterocyte CYP3A4, and P-glycoprotein. Clin Pharmacol Ther. 1999;65(3):237–244.
   Google Scholar
• Tian R, Koyabu N, Takanaga H, et al. Effects of grapefruit juice and orange juice on the intestinal efflux of P-glycoprotein substrates. Pharm Res. 2002;19(6):802–809.
   Google Scholar
• De Castro WV, Mertens-Talcott S, Derendorf H, et al. Effect of grapefruit juice, naringin, naringenin, and bergamottin on the intestinal carrier-mediated transport of talinolol in rats. J Agric Food Chem. 2008;56(12):4840–4845.
   Google Scholar
• Shirasaka Y, Kuraoka E, Spahn-Langguth H, et al. Species difference in the effect of grapefruit juice on intestinal absorption of talinolol between human and rat. J Pharmacol Exp Ther. 2010;332(1):181–189. Fugh-Berman A. Herb-drug interactions. Lancet. 2000;355(9198):134-138.
   Google Scholar
• Glaeser H, Bailey DG, Dresser, et al. Intestinal drug transporter expression and the impact of grapefruit juice in humans. Clin Pharmacol Ther. 2007;81(3):362−370.
   Google Scholar
• Oswald S, Gröer C, Drozdzik M, et al. Mass spectrometry-based targeted proteomics as a tool to elucidate the expression and function of intestinal drug transporters. Aaps J. 2013;15(4):1128–1140.
   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.
   Google Scholar
• Drozdzik M, Busch D, Lapczuk J, et al. Protein abundance of clinically relevant drug transporters in the human liver and intestine: A comparative analysis in paired tissue specimens. Clin Pharmacol Ther. 2019;105(5):1204–1212.
   Google Scholar
• Fugh-Berman A. Herb-drug interactions. Lancet. 2000;68(6):598–604.
   Google Scholar
• Dürr D, Stieger B, Kullak-Ublick GA, et al. St John’s Wort induces intestinal P-glycoprotein/MDR1 and intestinal and hepatic CYP3A4. Clin Pharmacol Ther. 2000;68(6):598–604.
   Google Scholar
• Matheny CJ, Ali RY, Yang X, et al. Effect of prototypical inducing agents on P-glycoprotein and CYP3A expression in mouse tissues. Drug Metab Dispos. 2004;32(9):1008–1014.
   Google Scholar
• Mannel M. Drug interactions with St John’s wort: mechanisms and clinical implications. Drug Saf. 2004;27(11):773–797.
   Google Scholar
• Tian R, Koyabu N, Morimoto S, et al. Functional induction and de-induction of P-glycoprotein by St. John’s wort and its ingredients in a human colon adenocarcinoma cell line. Drug Metab Dispos. 2005;33(4):547–554.
   Google Scholar
• Chrubasik-Hausmann S, Vlachojannis J, McLachlan AJ. Understanding drug interactions with St. John’s wort (Hypericum perforatum L.): impact of hyperforin content. J Pharm Pharmacol. 2019;71(1):129–138.
   Google Scholar
• Sehirli AO, Cetinei S, Ozkan N, et al. St.John’s Wort may ameliorate 2,4,6-trinitrobenzenesulfonic acid colitis of rats through the induction of pregnane X receptors and/or p-glycoproteins. J Physiol Pharmacol. 2015;66(2):203–214.
   Google Scholar
• Jodoin J, Demeule M, Beliveau R. Inhibition of the multidrug resistance P-glycoprotein activity by green tea polyphenols. Biochim Biophys Acta. 2002;1542(1–3):149–159.
   Google Scholar
• Chung JH, Choi DH, Choi JS. Effects of oral epigallocatechin gallate on the oral pharmacokinetics of verapamil in rats. Biopharm Drug Dispos. 2009;30(2):90–93.
   Google Scholar
• Dash RP, Ellendula B, Agarwal M, et al. Increased intestinal P-glycoprotein expression and activity with progression of diabetes and its modulation by epigallocatechin-3-gallate: evidence from pharmacokinetic studies. Eur J Pharmacol. 2015;767:67–76.
   Google Scholar
• Fan L, Tao GY, Wang G, et al. Effects of Ginkgo biloba extract ingestion on the pharmacokinetics of talinolol in healthy Chinese volunteers. Ann Pharmacother. 2009;43(5):944–949.
   Google Scholar
• Okura T, Ibe M, Umegaki K, et al. Effects of dietary ingredients on function and expression of P-glycoprotein in human intestinal epithelial cells. Biol Pharm Bull. 2010;33(2):255–259.
   Google Scholar
• Xiao CQ, Chen R, Lin J, et al. Effect of genistein on the activities of cytochrome P450 3A and P-glycoprotein in Chinese healthy participants. Xenobiotica. 2012;42(2):173–178.
   Google Scholar
• Saksena S, Goyal S, Raheja G, et al. Upregulation of P-glycoprotein by probiotics in intestinal epithelial cells and in the dextran sulfate sodium model of colitis in mice. Am J Physiol Gastrointest Liver Physiol. 2011;300(6):G1115–1123.
   Google Scholar
• St Sauver JL, Olson JE, Roger VL, et al. CYP2D6 phenotypes are associated with adverse outcomes related to opioid medications. Pharmgenomics Pers Med. 2017;10:217–227.
   Google Scholar
• von Ahsen N, Richter M, Grupp C, et al. No influence of the MDR-1 C3435T polymorphism or a CYP3A4 promoter polymorphism (CYP3A4-V allele) on dose-adjusted cyclosporin A trough concentrations or rejection incidence in stable renal transplant recipients. Clin Chem. 2001;47(6):1048–1052.
   Google Scholar
• Morita N, Yasumori T, Nakayama K. Human MDR1 polymorphism: G2677T/A and C3435T have no effect on MDR1 transport activities. Biochem Pharmacol. 2003;65(11):1843–1852.
   Google Scholar
• Tsuchiya N, Satoh S. Influence of CYP3A5 and MDR1 (ABCB1) Polymorphisms on the pharmacokinetics of tacrolimus in renal transplant recipients. Transplantation. 2004;78(8):1182–1187.
   Google Scholar
• Chowbay B, Li H, David M, et al. Meta-analysis of the influence of MDR1 C3435T polymorphism on digoxin pharmacokinetics and MDR1 gene expression. Br J Clin Pharmacol. 2005;60(2):159–171.
   Google Scholar
• Chen Z, Zhang L, Yang C, et al. Effect of MDR1 C1236T Polymorphism on Cyclosporine pharmacokinetics: A systematic review and meta-analysis medicine (Baltimore). 2017;96(47):e8700.
   Google Scholar
• Verstuyft C, Schwab M, Schaeffeler E, et al. Digoxin pharmacokinetics and MDR1 genetic polymorphisms. Eur J Clin Pharmacol. 2003;58(12):809–812.
   Google Scholar
• Tufan A, Babaoglu MO, Akdogan A, et al. Association of drug transporter gene ABCB1 (MDR1) 3435C to T polymorphism with colchicine response in familial Mediterranean fever. J Rheumatol. 2007;34(7):1540–1544.
   Google Scholar
• Adeagbo BA, Bolaji OO, Olugbade TA, et al. Influence of CYP3A5*3 and ABCB1 C3435T on clinical outcomes and trough plasma concentrations of imatinib in Nigerians with chronic myeloid leukaemia. J Clin Pharm Ther. 2016;41(5):546–551.
   Google Scholar
• Sharaki O, Zeid M, Moez P, et al. Impact of CYP3A4 and MDR1 gene (G2677T) polymorphisms on dose requirement of the cyclosporine in renal transplant Egyptian recipients. Mol Biol Rep. 2015;42(1):105–117.
   Google Scholar
• Lovrić M, Božina N, Hajnšek S, et al. Association between lamotrigine concentrations and ABCB1 polymorphisms in patients with epilepsy. Ther Drug Monit. 2012;34(5):518–525.
   Google Scholar
• Hanley MJ, Abernethy DR, Greenblatt DJ. Effect of obesity on the pharmacokinetics of drugs in humans. Clin Pharmacokinet. 2010;49(2):71–87.
   Google Scholar
• Sugioka N, Haraya K, Fukushima K, et al. Effects of obesity induced by high-fat diet on the pharmacokinetics of nelfinavir, a HIV protease inhibitor, in laboratory rats. Biopharm Drug Dispos. 2009;30(9):532–541.
   Google Scholar
• Nawa A, Fujita-Hamabe W, Tokuyama S. Altered intestinal P-glycoprotein expression levels in a monosodium glutamate-induced obese mouse model. Life Sci. 2011;89(23–24):834–838.
   Google Scholar
• Lloret-Linares C, Miyauchi E, Luo H, et al. Oral morphine pharmacokinetic in obesity: the role of P-glycoprotein, MRP2, MRP3, UGT2B7, and CYP3A4 jejunal contents and obesity-associated biomarkers. Mol Pharm. 2016;13(3):766–773.
   Google Scholar
• De Hoogd S, Välitalo PAJ, Dahan A, et al. Influence of morbid obesity on the pharmacokinetics of morphine, Morphine-3-glucuronide, and morphine-6-glucuronide. Clin Pharmacokinet. 2017;56(12):1577–1587.
   Google Scholar
• Ulvestad M, Skottheim IB, Jakobsen GS, et al. Impact of OATP1B1, MDR1, and CYP3A4 expression in liver and intestine on interpatient pharmacokinetic variability of atorvastatin in obese subjects. Clin Pharmacol Ther. 2013;93(3):275–282.
   Google Scholar
• Sawamoto K, Huong TT, Sugimoto N, et al. Mechanisms of lower maintenance dose of tacrolimus in obese patients. Drug Metab Pharmacokinet. 2014;29(4):341–347.
   Google Scholar
• Huang ZH, Murakami T, Okochi A, et al. Expression and function of P-glycoprotein in rats with glycerol-induced acute renal failure. Eur J Pharmacol. 2000;406(3):453–460.
   Google Scholar
• Huang ZH, Murakami T, Okochi A, et al. Expression and function of P-glycoprotein in rats with carbon tetrachloride-induced acute hepatic failure. J Pharm Pharmacol. 2001;53(6):873–881.
   Google Scholar
• Murakami T, Yumoto R, Nagai J, et al. Factors affecting the expression and function of P-glycoprotein in rats: drug treatments and diseased states. Pharmazie. 2002;57(2):102–107.
   Google Scholar
• Evers R, Piquette-Miller M, Polli JW, et al. Disease-associated changes in drug transporters may impact the pharmacokinetics and/or toxicity of drugs: a white paper from the international transporter consortium. Clin Pharmacol Ther. 2018;104(5):900–915.
   Google Scholar
• Mizoguchi T, Yamada K, Furukawa T, et al. Expression of the MDR1 gene in human gastric and colorectal carcinomas. J Natl Cancer Inst. 1990;82(21):1679–1683.
   Google Scholar
• Hinoshita E, Uchiumi T, Taguchi K, et al. Increased expression of an ATP-binding cassette superfamily transporter, multidrug resistance protein 2, in human colorectal carcinomas. Clin Cancer Res. 2000;6(6):2401–2407.
   Google Scholar
• Canaparo R, Nordmark A, Finnström N, et al. Expression of cytochromes P450 3A and P-glycoprotein in human large intestine in paired tumour and normal samples. Basic Clin Pharmacol Toxicol. 2007;100(4):240–348.
   Google Scholar
• Andersen V, Vogel U, Godiksen S, et al. Low ABCB1 gene expression is an early event in colorectal carcinogenesis. PLoS One. 2013;8(8):e72119.
   Google Scholar
• Andersen V, Vogel LK, Kopp TI, et al. High ABCC2 and low ABCG2 gene expression are early events in the colorectal adenoma-carcinoma sequence. PLoS One. 2015;10(3):e0119255.
   Google Scholar
• Micsik T, Lőrincz A, Mersich T, et al. Decreased functional activity of multidrug resistance protein in primary colorectal cancer. Diagn Pathol. 2015;10:26.
   Google Scholar
• Murakami T. Absorption sites of orally administered drugs in the small intestine. Expert Opin Drug Discov. 2017;12(12):1219–1232.
   Google Scholar
• Greig E, Sandle GI. Diarrhea in ulcerative colitis. The role of altered colonic sodium transport. Ann N Y Acad Sci. 2000;915:327–332.
   Google Scholar
• Asano T, Nishimoto K, Hayakawa M. Increased tacrolimus trough levels in association with severe diarrhea, a case report. Transplant Proc. 2004;36(7):2096–2097.
   Google Scholar
• Lemahieu W, Maes B, Verbeke K, et al. Cytochrome P450 3A4 and P-glycoprotein activity and assimilation of tacrolimus in transplant patients with persistent diarrhea. Am J Transplant. 2005;5(6):1383–1391.
   Google Scholar
• Abdel Halim M, Al-Otaibi T, Gheith O, et al. Toxic tacrolimus blood levels with rifampin administration in a renal transplant recipient. Ann Transplant. 2010;15(1):57–60.
   Google Scholar
• Nakamura A, Amada N, Haga I, et al. Effects of elevated tacrolimus trough levels in association with infectious enteritis on graft function in renal transplant recipients. Transplant Proc. 2014;46(2):592–594.
   Google Scholar
• Dietrich CG, Geier A, Salein N, et al. Consequences of bile duct obstruction on intestinal expression and function of multidrug resistance-associated protein 2. Gastroenterology. 2004;126(4):1044–1053.
   Google Scholar
• Yumoto R, Murakami T, Takano M. Differential effect of acute hepatic failure on in vivo and in vitro P-glycoprotein functions in the intestine. Pharm Res. 2003;20(5):765–771.
   Google Scholar
• Dilger K, Hohenester S, Winkler-Budenhofer U, et al. Effect of ursodeoxycholic acid on bile acid profiles and intestinal detoxification machinery in primary biliary cirrhosis and health. J Hepatol. 2012;57(1):133–140.
   Google Scholar
• Zhang YZ, Li YY. Inflammatory bowel disease: pathogenesis. World J Gastroenterol. 2014;20(1):91–99.
   Google Scholar
• Magnusson KE, Sundqvist T, Sjödahl R, et al. Altered intestinal permeability to low-molecular-weight polyethyleneglycols (PEG 400) in patients with Crohn’s disease. Acta Chir Scand. 1983;149(3):323–327.
   Google Scholar
• Petryszyn PW, Wiela-Hojeńska A. The importance of the polymorphisms of the ABCB1 gene in disease susceptibility, behavior and response to treatment in inflammatory bowel disease: A literature review. Adv Clin Exp Med. 2018;27(10):1459–1463.
   Google Scholar
• Shaffer JA, Williams SE, Turnberg LA, et al. Absorption of prednisolone in patients with Crohn’s disease. Gut. 1983;24(3):182–186.
   Google Scholar
• Brynskov J, Freund L, Campanini MC, et al. Cyclosporin pharmacokinetics after intravenous and oral administration in patients with Crohn’s disease. Scand J Gastroenterol. 1992;27(11):961–967.
   Google Scholar
• Sandborn WJ. Preliminary report on the use of oral tacrolimus (FK506) in the treatment of complicated proximal small bowel and fistulizing Crohn’s disease. Am J Gastroenterol. 1997;92(5):876–879.
   Google Scholar
• Farrell RJ, Murphy A, Long A, et al. High multidrug resistance (P-glycoprotein 170) expression in inflammatory bowel disease patients who fail medical therapy. Gastroenterology. 2000;118(2):279–288.
   Google Scholar
• Langmann T, Moehle C, Mauerer R, et al. Loss of detoxification in inflammatory bowel disease: dysregulation of pregnane X receptor target genes. Gastroenterology. 2004;127(1):26–40.
   Google Scholar
• Blokzijl H, Vander Borght S, Bok LI, et al. Decreased P-glycoprotein (P-gp/MDR1) expression in inflamed human intestinal epithelium is independent of PXR protein levels. Inflamm Bowel Dis. 2007;13(6):710–720.
   Google Scholar
• Englund G, Jacobson A, Rorsman F, et al. Efflux transporters in ulcerative colitis: decreased expression of BCRP (ABCG2) and Pgp (ABCB1). Inflamm Bowel Dis. 2007;13(3):291–297.
   Google Scholar
• Fakhoury M, Lecordier J, Medard Y, et al. Impact of inflammation on the duodenal mRNA expression of CYP3A and P-glycoprotein in children with Crohn’s disease. Inflamm Bowel Dis. 2006;12(8):745–749.
   Google Scholar
• Buchman AL, Paine MF, Wallin A, et al. A higher dose requirement of tacrolimus in active Crohn’s disease may be related to a high intestinal P-glycoprotein content. Dig Dis Sci. 2005;50(12):2312–2315.
   Google Scholar
• Gutmann H, Hruz P, Zimmermann C, et al. Breast cancer resistance protein and P-glycoprotein expression in patients with newly diagnosed and therapy-refractory ulcerative colitis compared with healthy controls. Digestion. 2008;78(2–3):154–162.
   Google Scholar
• Ufer M, Häsler R, Jacobs G, et al. Decreased sigmoidal ABCB1 (P-glycoprotein) expression in ulcerative colitis is associated with disease activity. Pharmacogenomics. 2009;10(12):1941–1953.
   Google Scholar
• Cario E. P-glycoprotein multidrug transporter in inflammatory bowel diseases: more questions than answers. World J Gastroenterol. 2017;23(9):1513–1520.
   Google Scholar
• Tseng JC, Kung AL. In vivo imaging method to distinguish acute and chronic inflammation. J Vis Exp. 2013;78:50690.
   Google Scholar
• Iizasa H, Genda N, Kitano T, et al. Altered expression and function of P-glycoprotein in dextran sodium sulfate-induced colitis in mice. J Pharm Sci. 2003;92(3):569–576.
   Google Scholar
• Kawauchi S, Nakamura T, Miki I, et al. Downregulation of CYP3A and P-glycoprotein in the secondary inflammatory response of mice with dextran sulfate sodium-induced colitis and its contribution to cyclosporine A blood concentrations. J Pharmacol Sci. 2014;124(2):180–191.
   Google Scholar
• Kawase A, Yoshida I, Tsunokuni Y, et al. Decreased PXR and CAR inhibit transporter and CYP mRNA Levels in the liver and intestine of mice with collagen-induced arthritis. Xenobiotica. 2007;37(4):366–374.
   Google Scholar
• Uno S, Kawase A, Tsuji A, et al. Decreased intestinal CYP3A and P-glycoprotein activities in rats with adjuvant arthritis. Drug Metab Pharmacokinet. 2007;22(4):313–321.
   Google Scholar
• Kawase A, Norikane S, Okada A, et al. Distinct alterations in ATP-binding cassette transporter expression in liver, kidney, small intestine, and brain in adjuvant-induced arthritic rats. J Pharm Sci. 2014;103(8):2556–2564.
   Google Scholar
• Iida A, Ouchi S, Oda T, et al. Changes of absorptive and secretory transporting system of (1 → 3) β-D-glucan based on efflux transporter in indomethacin-induced rat. Eur J Drug Metab Pharmacokinet. 2015;40(1):29–38.
   Google Scholar
• Omae T, Goto M, Shimomura M, et al. Transient up-regulation of P-glycoprotein reduces tacrolimus absorption after ischemia-reperfusion injury in rat ileum. Biochem Pharmacol. 2005;69(4):561–568.
   Google Scholar
• Ogura J, Kobayashi M, Itagaki S, et al. Alteration of Mrp2 and P-gp expression, including expression in remote organs, after intestinal ischemia-reperfusion. Life Sci. 2008;82(25–26):1242–1248.
   Google Scholar
• Tomita M, Takizawa Y, Kishimoto H, et al. Assessment of ileal epithelial P-glycoprotein dysfunction induced by ischemia/reperfusion using in vivo animal model. Drug Metab Pharmacokinet. 2008;23(5):356–363.
   Google Scholar
• Tomita M, Takizawa Y, Kishimoto H, et al. Effect of intestinal ischaemia/reperfusion on P-glycoprotein-mediated ileal excretion of rhodamine 123 in the rat. J Pharm Pharmacol. 2009;61(10):1319–1324.
   Google Scholar
• Ikemura K, Urano K, Matsuda H, et al. Decreased oral absorption of cyclosporine A after liver ischemia-reperfusion injury in rats: the contribution of CYP3A and P-glycoprotein to the first-pass metabolism in intestinal epithelial cells. J Pharmacol Exp Ther. 2009;328(1):249–255.
   Google Scholar
• Terada Y, Ogura J, Tsujimoto T, et al. Intestinal P-glycoprotein expression is multimodally regulated by intestinal ischemia-reperfusion. J Pharm Pharm Sci. 2014;17(2):266–276.
   Google Scholar
• Sukkummee W, Jittisak P, Wonganan P, et al. The prominent impairment of liver/intestinal cytochrome P450 and intestinal drug transporters in sepsis-induced acute kidney injury over acute and chronic renal ischemia, a mouse model comparison. Ren Fail. 2019;41(1):314–325.
   Google Scholar
• Moini M, Schilsky ML, Tichy EM. Review on immunosuppression in liver transplantation. World J Hepatol. 2015;7(10):1355–1368.
   Google Scholar
• Kaplan B, Lown K, Craig R, et al. Low bioavailability of cyclosporine microemulsion and tacrolimus in a small bowel transplant recipient: possible relationship to intestinal P-glycoprotein activity. Transplantation. 1999;67(2):333–335.
   Google Scholar
• Masuda S, Uemoto S, Hashida T, et al. Effect of intestinal P-glycoprotein on daily tacrolimus trough level in a living-donor small bowel recipient. Clin Pharmacol Ther. 2000;68(1):98–103.
   Google Scholar
• Masuda S, Uemoto S, Goto M, et al. Tacrolimus therapy according to mucosal MDR1 levels in small-bowel transplant recipients. Clin Pharmacol Ther. 2004;75(4):352–361.
   Google Scholar
• Hashida T, Masuda S, Uemoto S, et al. Pharmacokinetic and prognostic significance of intestinal MDR1 expression in recipients of living-donor liver transplantation. Clin Pharmacol Ther. 2001;69(5):308–316.
   Google Scholar
• Masuda S, Goto M, Kiuchi T, et al. Enhanced expression of enterocyte P-glycoprotein depresses cyclosporine bioavailability in a recipient of living donor liver transplantation. Liver Transpl. 2003;9(10):1108–1113.
   Google Scholar
• Fukudo M, Yano I, Yoshimura A, et al. Impact of MDR1 and CYP3A5 on the oral clearance of tacrolimus and tacrolimus-related renal dysfunction in adult living-donor liver transplant patients. Pharmacogenet Genomics. 2008;18(5):413–423.
   Google Scholar
• Chen YK, Han LZ, Xue F, et al. Personalized tacrolimus dose requirement by CYP3A5 but not ABCB1 or ACE genotyping in both recipient and donor after pediatric liver transplantation. PLoS One. 2014;9(10):e109464.
   Google Scholar
• Lemahieu WP, Maes BD, Verbeke K, et al. CYP3A4 and P-glycoprotein activity in healthy controls and transplant patients on cyclosporin vs. tacrolimus vs. sirolimus. Am J Transplant. 2004;4(9):1514–1522.
   Google Scholar
• Lemahieu WP, Maes BD, Verbeke K. Alterations of CYP3A4 and P-glycoprotein activity in vivo with time in renal graft recipients. Kidney Int. 2004;66(1):433–440.
   Google Scholar
• Sun H, Frassetto L, Benet LZ. Effects of renal failure on drug transport and metabolism. Pharmacol Ther. 2006;109(1–2):1–11.
   Google Scholar
• Fujii H, Goto S, Fukagawa M. Role of uremic toxins for kidney, cardiovascular, and bone dysfunction. Toxins (Basel). 2018 May 16;10(5):ii: E202.
   Google Scholar
• Shibata N, Morimoto J, Hoshino N, et al. Factors that affect absorption behavior of cyclosporin a in gentamicin-induced acute renal failure in rats. Ren Fail. 2000;22(2):181–194.
   Google Scholar
• Veau C, Leroy C, Banide H, et al. Effect of chronic renal failure on the expression and function of rat intestinal P-glycoprotein in drug excretion. Nephrol Dial Transplant. 2001;16(8):1607–1614.
   Google Scholar
• Naud J, Michaud J, Boisvert C, et al. Down-regulation of intestinal drug transporters in chronic renal failure in rats. J Pharmacol Exp Ther. 2007;320(3):978–985.
   Google Scholar
• Mathias AA, Maggio-Price L, Lai Y, et al. Changes in pharmacokinetics of anti-HIV protease inhibitors during pregnancy: the role of CYP3A and P-glycoprotein. J Pharmacol Exp Ther. 2006;316(3):1202–1209.
   Google Scholar
• Santana Machado T, Poitevin S, Paul P, et al. Indoxyl sulfate upregulates liver P-glycoprotein expression and activity through aryl hydrocarbon receptor signaling. J Am Soc Nephrol. 2018;29(3):906–918.
   Google Scholar
• Burk O, Brenner SS, Hofmann U, et al. The impact of thyroid disease on the regulation, expression, and function of ABCB1 (MDR1/P glycoprotein) and consequences for the disposition of digoxin. Clin Pharmacol Ther. 2010;88(5):685–694.
   Google Scholar
• De Rosa MF, Robillard KR, Kim CJ, et al. Expression of membrane drug efflux transporters in the sigmoid colon of HIV-infected and uninfected men. J Clin Pharmacol. 2013;53(9):934–945.
   Google Scholar
• Crowe A. The role of P-glycoprotein and breast cancer resistance protein (BCRP) in bacterial attachment to human gastrointestinal cells. J Crohns Colitis. 2011;5(6):531–542.
   Google Scholar
• Afonso-Pereira F, Dou L, Trenfield SJ, et al. Sex differences in the gastrointestinal tract of rats and the implications for oral drug delivery. Eur J Pharm Sci. 2018;115(3):339–344.
   Google Scholar
• Aros CA, Ardiles LG, Schneider HO, et al. No gender-associated differences of cyclosporine pharmacokinetics in stable renal transplant patients treated with diltiazem. Transplant Proc. 2005;37(8):3364–3366.
   Google Scholar
• Dahan A, Amidon GL. Grapefruit juice and its constituents augment colchicine intestinal absorption: potential hazardous interaction and the role of p-glycoprotein. Pharm Res. 2009;26(4):883–892.
   Google Scholar
• Yang CY, Chao PD, Hou YC, et al. Marked decrease of cyclosporin bioavailability caused by coadministration of ginkgo and onion in rats. Food Chem Toxicol. 2006;44(9):1572–1578.
   Google Scholar
• Oltra-Noguera D, Mangas-Sanjuan V, González-Álvarez I, et al. Drug gastrointestinal absorption in rat: strain and gender differences. Eur J Pharm Sci. 2015;78:198–203.
   Google Scholar
• Oswald S, Terhaag B, Siegmund W. In vivo probes of drug transport: commonly used probe drugs to assess function of intestinal P-glycoprotein (ABCB1) in humans. Handb Exp Pharmacol. 2011;201:403–447.
   Google Scholar
• Stopfer P, Giessmann T, Hohl K, et al. Pharmacokinetic evaluation of a drug transporter cocktail consisting of digoxin, furosemide, metformin, and rosuvastatin. Clin Pharmacol Ther. 2016;100(3):259–267.
   Google Scholar
• Tubic M, Wagner D, Spahn-Langguth H, et al. Effects of controlled-release on the pharmacokinetics and absorption characteristics of a compound undergoing intestinal efflux in humans. Eur J Pharm Sci. 2006;29(3–4):231–239.
   Google Scholar
• Weitschies W, Bernsdorf A, Giessmann T, et al. The talinolol double-peak phenomenon is likely caused by presystemic processing after uptake from gut lumen. Pharm Res. 2005;22(5):728–735.
   Google Scholar
• Gramatté T, Oertel R, Terhaag B, et al. Direct demonstration of small intestinal secretion and site-dependent absorption of the beta-blocker talinolol in humans. Clin Pharmacol Ther. 1996;59(5):541–549.
   Google Scholar