The role of organic anion transporting polypeptides in drug absorption, distribution, excretion and drug-drug interactions

References

• Gu Q, Paulose-Ram R, Burt VL, et al. Prescription cholesterol-lowering medication use in adults aged 40 and over: United States, 2003-2012. NCHS Data Brief. 2014;177:1–8.
   PubMedGoogle Scholar
• Wenner Moyer M. The search beyond statins. Nat Med. 2010;16:150–153.
   PubMed Web of Science ®Google Scholar
• Shitara Y, Itoh T, Sato H, et al. Inhibition of transporter-mediated hepatic uptake as a mechanism for drug-drug interaction between cerivastatin and cyclosporin A. J Pharmacol Exp Ther. 2003;304:610–616.
   PubMed Web of Science ®Google Scholar
• Elsby R, Hilgendorf C, Fenner K. Understanding the critical disposition pathways of statins to assess drug-drug interaction risk during drug development: it’s not just about OATP1B1. Clin Pharmacol Ther. 2012;92:584–598.
   PubMed Web of Science ®Google Scholar
• Gong IY, Kim RB. Impact of genetic variation in OATP transporters to drug disposition and response. Drug Metab Pharmacokinet. 2013;28:4–18.
   PubMed Web of Science ®Google Scholar
• Giacomini KM, Huang S, Tweedie DJ, et al. Membrane transporters in drug development. Nature. 2012;9:215–236.
   Web of Science ®Google Scholar
• Huang S-M, Zhang L, Giacomini KM. The international transporter consortium: a collaborative group of scientists from academia, industry, and the FDA. Clin Pharmacol Ther. 2010;87:32–36.
   PubMed Web of Science ®Google Scholar
• Yu J, Ritchie TK, Mulgaonkar A, et al. Drug disposition and drug-drug interaction data in 2013 FDA new drug applications: a systematic review. Drug Metab Dispos. 2014;42:1991–2001.
   PubMed Web of Science ®Google Scholar
• Li L, Meier PJ, Ballatori N. Oatp2 mediates bidirectional organic solute transport: a role for intracellular glutathione. Mol Pharmacol. 2000;58:335–340.
   PubMed Web of Science ®Google Scholar
• Satlin LM, Amin V, Wolkoff AW, et al. Organic anion transporting polypeptide mediates organic anion /HCO3- exchange *. J Biol Chem. 1997;272:26340–26345.
   PubMed Web of Science ®Google Scholar
• Hagenbuch B, Stieger B. The SLCO (former SLC21) superfamily of transporters. Mol Aspects Med. 2013;34:396–412. .
   PubMed Web of Science ®Google Scholar
• Leuthold S, Hagenbuch B, Mohebbi N, et al. Mechanisms of pH-gradient driven transport mediated by organic anion polypeptide transporters. Am J Physiol Cell Physiol. 2009;296:C570–82.
   PubMed Web of Science ®Google Scholar
• Patik I, Kovacsics D, Német O, et al. Functional expression of the 11 human organic anion transporting polypeptides in insect cells reveals that sodium fluorescein is a general OATP substrate. Biochem Pharmacol. 2015;98:649–658.
   PubMed Web of Science ®Google Scholar
• Masuda S, Ibaramoto K, Takeuchi A, et al. Cloning and functional characterization of a new multispecific organic anion transporter, OAT-K2, in rat kidney. Mol Pharmacol. 1999;55:743–752.
   PubMed Web of Science ®Google Scholar
• Roth M, Obaidat A, Hagenbuch B. OATPs, OATs and OCTs: the organic anion and cation transporters of the SLCO and SLC22A gene superfamilies. Br J Pharmacol. 2012;165:1260–1287.
   PubMed Web of Science ®Google Scholar
• Durmus S, Naik J, Buil L, et al. In vivo disposition of doxorubicin is affected by mouse OATP1a/1b and human OATP1A/1B transporters. Int J Cancer. 2014;135:1700–1710.
   PubMed Web of Science ®Google Scholar
• Cheng Z, Liu H, Yu N, et al. Hydrophilic anti-migraine triptans are substrates for OATP1A2, a transporter expressed at human blood-brain barrier. Xenobiotica. 2012;42:880–890.
   PubMed Web of Science ®Google Scholar
• Gozalpour E, Greupink R, Wortelboer HM, et al. Interaction of digitalis-like compounds with liver uptake transporters NTCP, OATP1B1, and OATP1B3. Mol Pharm. 2014;11:1844–1855.
   PubMed Web of Science ®Google Scholar
• Sprowl JA, Sparreboom A. Uptake carriers and oncology drug safety. Drug Metab Dispos. 2014;42:611–622.
   PubMed Web of Science ®Google Scholar
• Chan T, Zhu L, Madigan MC, et al. Human organic anion transporting polypeptide 1A2 (OATP1A2) mediates cellular uptake of all-trans-retinol in human retinal pigmented epithelial cells. Br J Pharmacol. 2015;172:2343–2353.
   PubMed Web of Science ®Google Scholar
• Kullak-Ublick GA, Hagenbuch B, Stieger B, et al. Molecular and functional characterization of an organic anion transporting polypeptide cloned from human liver. Gastroenterology. 1995;109:1274–1282.
   PubMed Web of Science ®Google Scholar
• Gao B, Vavricka SR, Meier PJ, et al. Differential cellular expression of organic anion transporting peptides OATP1A2 and OATP2B1 in the human retina and brain: implications for carrier-mediated transport of neuropeptides and neurosteriods in the CNS. Pflügers Arch Eur J Physiol. 2014;467:1481–1493.
   PubMed Web of Science ®Google Scholar
• Misaka S, Yatabe J, Müller F, et al. Green tea ingestion greatly reduces plasma concentrations of nadolol in healthy subjects. Clin Pharmacol Ther. 2014;95:432–438.
   PubMed Web of Science ®Google Scholar
• Gao B, Hagenbuch B, Kullak-Ublick GA, et al. Organic anion-transporting polypeptides mediate transport of opioid peptides across blood-brain barrier. J Pharmacol Exp Ther. 2000;294:73–79.
   PubMed Web of Science ®Google Scholar
• Kullak-Ublick GA, Ismair MG, Stieger B, et al. Organic anion-transporting polypeptide B (OATP-B) and its functional comparison with three other OATPs of human liver. Gastroenterology. 2001;120:525–533.
   PubMed Web of Science ®Google Scholar
• Iusuf D, Hendrikx JJMA, van Esch A, et al. Human OATP1B1, OATP1B3 and OATP1A2 can mediate the in vivo uptake and clearance of docetaxel. Int J Cancer. 2015;136:225–233.
   PubMed Web of Science ®Google Scholar
• Badagnani I, Castro RA, Taylor TR, et al. Interaction of methotrexate with organic-anion transporting polypeptide 1A2 and its genetic variants. J Pharmacol Exp Ther. 2006;318:521–529.
   Google Scholar
• Glaeser H, Bujok K, Schmidt I, et al. Organic anion transporting polypeptides and organic cation transporter 1 contribute to the cellular uptake of the flavonoid quercetin. Naunyn Schmiedebergs Arch Pharmacol. 2014;387:883–891.
   PubMed Web of Science ®Google Scholar
• Van Montfoort JE1, Müller M, Groothuis GM, et al. Comparison of ‘ Type I ’ and ‘ Type II ’ organic cation transport by organic cation transporters and organic anion- transporting polypeptides. J Pharmacol Exp Ther. 2001;298:110–115.
   PubMed Web of Science ®Google Scholar
• Forster S, Thumser AE, Hood SR, et al. Characterization of rhodamine-123 as a tracer dye for use in in vitro drug transport assays. PLoS One. 2012; 7: e33253.
   Web of Science ®Google Scholar
• Su Y, Zhang X, Sinko PJ. Human organic anion-transporting polypeptide OATP-A (SLC21A3) acts in concert with P-glycoprotein and multidrug resistance protein 2 in the vectorial transport of Saquinavir in Hep G2 cells. Mol Pharm. 2004;1:49–56.
   PubMed Web of Science ®Google Scholar
• Bexten M, Oswald S, Grube M, et al. Expression of drug transporters and drug metabolizing enzymes in the bladder urothelium in man and affinity of the bladder spasmolytic trospium chloride to transporters likely involved in its pharmacokinetics. Mol Pharm. 2015;12:171–178.
   PubMed Web of Science ®Google Scholar
• Hagenbuch B, Meier PJ. The superfamily of organic anion transporting polypeptides. Biochim Biophys Acta. 2003;1609:1–18.
   PubMed Web of Science ®Google Scholar
• Izumi S, Nozaki Y, Komori T, et al. Substrate-dependent inhibition of organic anion transporting polypeptide 1B1: comparative analysis with prototypical probe substrates estradiol-17β-glucuronide, estrone-3-sulfate, and sulfobromophthalein. Drug Metab Dispos. 2013;41:1859–1866.
   PubMed Web of Science ®Google Scholar
• Oshida K, Shimamura M, Seya K, et al. Identification of transporters involved in beraprost sodium transport in vitro. Eur J Drug Metab Pharmacokinet. 2016. DOI:10.1007/s13318-016-0327-4
   PubMedGoogle Scholar
• Izumi S, Nozaki Y, Komori T, et al. Investigation of fluorescein derivatives as substrates of Organic Anion Transporting Polypeptide (OATP) 1B1 to develop sensitive fluorescence-based OATP1B1 inhibition assays. Mol Pharm. 2016;13:438–448.
   PubMed Web of Science ®Google Scholar
• Lee HH, Leake BF, Teft W, et al. Contribution of hepatic organic anion-transporting polypeptides to docetaxel uptake and clearance. Mol Cancer Ther. 2015;14:994–1003.
   PubMed Web of Science ®Google Scholar
• Abe T, Kakyo M, Tokui T, et al. Identification of a novel gene family encoding human liver-specific organic anion transporter LST-1. J Biol Chem. 1999;274:17159–17163.
   PubMed Web of Science ®Google Scholar
• Gui C, Obaidat A, Chaguturu R, et al. Development of a cell-based high-throughput assay to screen for inhibitors of organic anion transporting polypeptides 1B1 and 1B3. Curr Chem Genomics. 2010;4:1–8.
   PubMedGoogle Scholar
• Gui C, Miao Y, Thompson L, et al. Effect of pregnane X receptor ligands on transport mediated by human OATP1B1 and OATP1B3. Eur J Pharmacol. 2008;584:57–65.
   PubMed Web of Science ®Google Scholar
• De Bruyn T, Fattah S, Stieger B, et al. Sodium fluorescein is a probe substrate for hepatic drug transport mediated by OATP1B1 and OATP1B3. J Pharm Sci. 2011;100:5018–5030.
   PubMed Web of Science ®Google Scholar
• Ismair MG, Stieger B, Cattori V, et al. Hepatic uptake of cholecystokinin octapeptide by organic anion-transporting polypeptides OATP4 and OATP8 of rat and human liver. Gastroenterology. 2001;121:1185–1190.
   PubMed Web of Science ®Google Scholar
• Obaidat A, Roth M, Hagenbuch B. The expression and function of organic anion transporting polypeptides in normal tissues and in cancer. Annu Rev Pharmacol Toxicol. 2012;52:135–151.
   PubMed Web of Science ®Google Scholar
• König J, Cui Y, Nies AT, et al. Localization and genomic organization of a new hepatocellular organic anion transporting polypeptide. J Biol Chem. 2000;275:23161–23168.
   PubMed Web of Science ®Google Scholar
• Pizzagalli F, Hagenbuch B, Stieger B, et al. Identification of a novel human organic anion transporting polypeptide as a high affinity thyroxine transporter. Mol Endocrinol. 2002;16:2283–2296.
   PubMed Web of Science ®Google Scholar
• Schnell C, Shahmoradi A, Wichert SP, et al. The multispecific thyroid hormone transporter OATP1C1 mediates cell-specific sulforhodamine 101-labeling of hippocampal astrocytes. Brain Struct Funct. 2013;220:193–203.
   PubMed Web of Science ®Google Scholar
• Lu R, Kanai N, Bao Y, et al. Cloning, in vitro expression, and tissue distribution of a human prostaglandin transporter cDNA(hPGT). J Clin Invest. 1996;98:1142–1149.
   PubMed Web of Science ®Google Scholar
• Hagenbuch B, Gui C. Xenobiotic transporters of the human organic anion transporting polypeptides (OATP) family. Xenobiotica. 2008;38:778–801.
   PubMed Web of Science ®Google Scholar
• Nozawa T, Imai K, Nezu J-I, et al. Functional characterization of pH-sensitive organic anion transporting polypeptide OATP-B in human. J Pharmacol Exp Ther. 2004;308:438–445.
   PubMed Web of Science ®Google Scholar
• Tamai I, Nezu J, Uchino H, et al. Molecular identification and characterization of novel members of the human organic anion transporter (OATP) family. Biochem Biophys Res Commun. 2000;273:251–260.
   PubMed Web of Science ®Google Scholar
• Huber RD, Gao B, Sidler Pfändler M-A, et al. Characterization of two splice variants of human organic anion transporting polypeptide 3A1 isolated from human brain. Am J Physiol Cell Physiol. 2007;292:C795–C806.
   PubMed Web of Science ®Google Scholar
• Fujiwara K, Adachi H, Nishio T, et al. Identification of thyroid hormone transporters in humans: different molecules are involved in a tissue-specific manner. Endocrinology. 2001;142:2005–2012.
   PubMed Web of Science ®Google Scholar
• Mikkaichi T, Suzuki T, Onogawa T, et al. Isolation and characterization of a digoxin transporter and its rat homologue expressed in the kidney. Proc Natl Acad Sci U S A. 2004;101:3569–3574.
   PubMed Web of Science ®Google Scholar
• Yamaguchi H, Sugie M, Okada M, et al. Transport of estrone 3-sulfate mediated by organic anion transporter OATP4C1: estrone 3-sulfate binds to the different recognition site for digoxin in OATP4C1. Drug Metab Pharmacokinet. 2010;25:314–317.
   PubMed Web of Science ®Google Scholar
• Chu XY, Bleasby K, Yabut J, et al. Transport of the dipeptidyl peptidase-4 inhibitor sitagliptin by human organic anion transporter 3, organic anion transporting polypeptide 4C1, and multidrug resistance P-glycoprotein. J Pharmacol Exp Ther. 2007;321:673–683.
   PubMed Web of Science ®Google Scholar
• Kato K, Shirasaka Y, Kuraoka E, et al. Intestinal absorption mechanism of tebipenem pivoxil, a novel oral carbapenem: involvement of human OATP family in apical membrane transport. Mol Pharm. 2010;7:1747–1756.
   PubMed Web of Science ®Google Scholar
• Yamakawa Y, Hamada A, Shuto T, et al. Pharmacokinetic impact of SLCO1A2 polymorphisms on imatinib disposition in patients with chronic myeloid leukemia. Clin Pharmacol Ther. 2011;90:157–163.
   PubMed Web of Science ®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;332:181–189.
   PubMed Web of Science ®Google Scholar
• Glaeser H, Bailey DG, Dresser GK, et al. Intestinal drug transporter expression and the impact of grapefruit juice in humans. Clin Pharmacol Ther. 2007;81:362–370.
   PubMed Web of Science ®Google Scholar
• Bailey DG, Dresser GK, Leake BF, et al. Naringin is a major and selective clinical inhibitor of organic anion-transporting polypeptide 1A2 (OATP1A2) in grapefruit juice. Clin Pharmacol Ther. 2007;81:495–502.
   PubMed Web of Science ®Google Scholar
• Shirasaka Y, Suzuki K, Nakanishi T, et al. Intestinal absorption of HMG-CoA reductase inhibitor pravastatin mediated by organic anion transporting polypeptide. Pharm Res. 2010;27:2141–2149.
   PubMed Web of Science ®Google Scholar
• Fischer WJ, Altheimer S, Cattori V, et al. Organic anion transporting polypeptides expressed in liver and brain mediate uptake of microcystin. Toxicol Appl Pharmacol. 2005;203:257–263.
   PubMed Web of Science ®Google Scholar
• König J, Seithel A, Gradhand U, et al. Pharmacogenomics of human OATP transporters. Naunyn Schmiedebergs Arch Pharmacol. 2006;372:432–443.
   PubMed Web of Science ®Google Scholar
• Dresser GK, Bailey DG, Leake BF, et al. Fruit juices inhibit organic anion transporting polypeptide-mediated drug uptake to decrease the oral availability of fexofenadine. Clin Pharmacol Ther. 2002;71:11–20.
   PubMed Web of Science ®Google Scholar
• Parvez MM, Jung J-A, Shin H-J, et al. Characterization of 22 anti-tuberculosis drugs for the inhibitory interaction potential on organic anionic transporter polypeptides (OATPs) mediated uptake. Antimicrob Agents Chemother. 2016;60:3096–3105.
   Google Scholar
• Karlgren M, Vildhede A, Norinder U, et al. Classi fi cation of inhibitors of hepatic Organic Anion Transporting Polypeptides (OATPs): in fl uence of protein expression on drug − drug interactions. J Med Chem. 2012;55:4740–4763.
   PubMed Web of Science ®Google Scholar
• Brenner S, Riha J, Giessrigl B, et al. The effect of organic anion-transporting polypeptides 1B1, 1B3 and 2B1 on the antitumor activity of flavopiridol in breast cancer cells. Int J Oncol. 2015;46:324–332.
   PubMed Web of Science ®Google Scholar
• Lancaster CS, Sprowl1 JA, Walker AL, et al., Sparreboom and AS. Modulation of OATP1B-type transporter function alters cellular uptake and disposition of platinum chemotherapeutics. Mol Cancer Ther. 2013;12:1537–1544.
   PubMed Web of Science ®Google Scholar
• Zimmerman EI, Hu S, Roberts JL, et al. Contribution of OATP1B1 and OATP1B3 to the disposition of sorafenib and sorafenib-glucuronide. Clin Cancer Res. 2013;19:1458–1466.
   PubMed Web of Science ®Google Scholar
• Treiber A, Schneiter R, Häusler S, et al. Bosentan is a substrate of human OATP1B1 and OATP1B3: inhibition of hepatic uptake as the common mechanism of its interactions with cyclosporin A, rifampicin, and sildenafil. Drug Metab Dispos. 2007;35:1400–1407.
   PubMed Web of Science ®Google Scholar
• Yamashiro W, Maeda K, Hirouchi M, et al. Involvement of transporters in the hepatic uptake and biliary excretion of valsartan, a selective antagonist of the angiotensin II AT1-receptor, in humans. Drug Metab Dispos. 2006;34:1247–1254.
   PubMed Web of Science ®Google Scholar
• König J, Glaeser H, Keiser M, et al. Role of organic anion-transporting polypeptides for cellular mesalazine (5-aminosalicylic acid) uptake. Drug Metab Dispos. 2011;39:1097–1102.
   PubMed Web of Science ®Google Scholar
• Shitara Y, Hirano M, Sato H, et al. Gemfibrozil and Its glucuronide inhibit the organic anion transporting polypeptide 2 (OATP2/OATP1B1: SLC21A6)-mediated hepatic uptake and cyp2c8-mediated metabolism of cerivastatin: analysis of the mechanism of the clinically relevant drug-drug interactio. J Pharmacol Exp Ther. 2004;311:228–236.
   PubMed Web of Science ®Google Scholar
• Monks NR, Liu S, Xu Y, et al. Potent cytotoxicity of the phosphatase inhibitor microcystin LR and microcystin analogues in OATP1B1- and OATP1B3-expressing HeLa cells. Mol Cancer Ther. 2007;6:587–598.
   PubMed Web of Science ®Google Scholar
• Karlgren M, Ahlin G, Bergström CAS, et al. In vitro and in silico strategies to identify OATP1B1 inhibitors and predict clinical drug-drug interactions. Pharm Res. 2012;29:411–426.
   PubMed Web of Science ®Google Scholar
• Prueksaritanont T, Chu X, Evers R, et al. Pitavastatin is a more sensitive and selective organic anion-transporting polypeptide 1B clinical probe than rosuvastatin. Br J Clin Pharmacol. 2014;78:587–598.
   PubMed Web of Science ®Google Scholar
• Smith NF, Marsh S, Scott-Horton TJ, et al. Variants in the SLCO1B3 gene: interethnic distribution and association with paclitaxel pharmacokinetics. Clin Pharmacol Ther. 2007;81:76–82.
   PubMed Web of Science ®Google Scholar
• Nambu T, Hamada A, Nakashima R, et al. Association of SLCO1B3 polymorphism with intracellular accumulation of imatinib in leukocytes in patients with chronic myeloid leukemia. Biol Pharm Bull. 2011;34:114–119.
   PubMed Web of Science ®Google Scholar
• Mandery K, Bujok K, Schmidt I, et al. Influence of cyclooxygenase inhibitors on the function of the prostaglandin transporter organic anion-transporting polypeptide 2A1 expressed in human gastroduodenal mucosa. J Pharmacol Exp Ther. 2010;332:345–351.
   PubMed Web of Science ®Google Scholar
• Kraft ME, Glaeser H, Mandery K, et al. The prostaglandin transporter OATP2A1 is expressed in human ocular tissues and transports the antiglaucoma prostanoid latanoprost. Invest Ophthalmol Vis Sci. 2010;51:2504–2511.
   PubMed Web of Science ®Google Scholar
• Scialis RJ, Manautou JE. Elucidation of the mechanisms through which the reactive metabolite diclofenac acyl glucuronide can mediate toxicity. J Pharmacol Exp Ther. 2016;357:167–176.
   PubMed Web of Science ®Google Scholar
• Knauer MJ, Urquhart BL, Meyer Zu Schwabedissen HE, et al. Human skeletal muscle drug transporters determine local exposure and toxicity of statins. Circ Res. 2010;106:297–306.
   PubMed Web of Science ®Google Scholar
• Wei SC, Tan YY, Weng MT, et al. SLCO3A1, a novel Crohn’s disease-associated gene, regulates NF-kB activity and associates with intestinal perforation. PLoS One. 2014;9.e100515.
   Web of Science ®Google Scholar
• He J, Yu Y, Prasad B, et al. Mechanism of an unusual, but clinically significant, digoxin-bupropion drug interaction. Biopharm Drug Dispos. 2014;35:253–263.
   PubMed Web of Science ®Google Scholar
• Toyohara T, Suzuki T, Morimoto R, et al. SLCO4C1 transporter eliminates uremic toxins and attenuates hypertension and renal inflammation. Ther Res. 2010;31:1221–1223.
   Google Scholar
• Hamilton U, Olszewski M, Svoboda M, et al. Organic anion transporting polypeptide 5A1 (OATP5A1) in Small Cell Lung Cancer (SCLC) cells: possible involvement in chemoresistance to satraplatin. Biomark Cancer. 2011;3:31–40.
   PubMedGoogle Scholar
• Shimada H, Nakamura Y, Nakanishi T, et al. OATP2A1/SLCO2A1-mediated prostaglandin E2 loading into intracellular acidic compartments of macrophages contributes to exocytotic secretion. Biochem Pharmacol. 2015;98:629–638.
   PubMed Web of Science ®Google Scholar
• Kindla J, Rau TT, Jung R, et al. Expression and localization of the uptake transporters OATP2B1, OATP3A1 and OATP5A1 in non-malignant and malignant breast tissue. Cancer Biol Ther. 2011;11:584–591.
   PubMed Web of Science ®Google Scholar
• Mk P, Neuvonen M, Neuvonen PJNM. SLCO1B1 polymorphism markedly affects the pharmacokinetics of simvastatin acid. Pharmacogenet Genomics. 2006;16:873–879.
   PubMed Web of Science ®Google Scholar
• Maeda K. Organic anion transporting polypeptide (OATP)1B1 and OATP1B3 as important regulators of the pharmacokinetics of substrate drugs. Biol Pharm Bull. 2015;38:155–168.
   PubMed Web of Science ®Google Scholar
• Shitara Y, Maeda K, Ikejiri K, et al. Clinical significance of organic anion transporting polypeptides (OATPs) in drug disposition: their roles in hepatic clearance and intestinal absorption. Biopharm Drug Dispos. 2013;34:45–78.
   PubMed Web of Science ®Google Scholar
• Kunze A, Huwyler J, Camenisch G, et al. Prediction of organic anion-transporting polypeptide 1B1- and 1B3- mediated hepatic uptake of statins based on transporter protein expression and activity data. Drug Metab Dispos. 2014;42:1514–1521.
   PubMed Web of Science ®Google Scholar
• Masereeuw R, Mutsaers HAM, Toyohara T, et al. The kidney and uremic toxin removal: glomerulus or tubule? semin. Nephrol. 2014;34:191–208.
   Web of Science ®Google Scholar
• Knauer MJ, Girdwood AJ, Kim RB, et al. Transport function and transcriptional regulation of a liver-enriched human organic anion transporting polypeptide 2B1 transcriptional start site variant. Mol Pharmacol. 2013;83:1218–1228.
   PubMed Web of Science ®Google Scholar
• Meier Y, Eloranta J, Darimont J. Regional distribution of solute carrier mRNA expression along the human intestinal tract. Drug Metab. 2007;35:590–594.
   Web of Science ®Google Scholar
• Kobayashi D, Nozawa T, Imai K, et al. Involvement of human organic anion transporting polypeptide OATP-B (SLC21A9) in pH-dependent transport across intestinal apical membrane. J Pharmacol Exp Ther. 2003;306:703–708.
   PubMed Web of Science ®Google Scholar
• Urquhart BL, Kim RB. Blood-brain barrier transporters and response to CNS-active drugs. Eur J Clin Pharmacol. 2009;65:1063–1070.
   PubMed Web of Science ®Google Scholar
• Su L, Mruk DD, Lee WM, et al. Drug transporters and blood–testis barrier function. J Endocrinol. 2015;2:337–351.
   Google Scholar
• Gao B, Huber RD, Wenzel A, et al. Localization of organic anion transporting polypeptides in the rat and human ciliary body epithelium. Exp Eye Res. 2005;80:61–72.
   PubMed Web of Science ®Google Scholar
• Wang H, Yan Z, Dong M, et al. Alteration in placental expression of bile acids transporters OATP1A2, OATP1B1, OATP1B3 in intrahepatic cholestasis of pregnancy. Arch Gynecol Obstet. 2012;285:1535–1540.
   PubMed Web of Science ®Google Scholar
• Grube M, Reuther S, Meyer Zu Schwabedissen H, et al. Organic anion transporting polypeptide 2B1 and breast cancer resistance protein interact in the transepithelial transport of steroid sulfates in human placenta. Drug Metab Dispos. 2007;35:30–35.
   PubMed Web of Science ®Google Scholar
• Hagenbuch B. Cellular entry of thyroid hormones by organic anion transporting polypeptides. Best Pract Res Clin Endocrinol Metab. 2007;21:209–221.
   PubMed Web of Science ®Google Scholar
• Memon N, Weinberger BI, Hegyi T, et al. Inherited disorders of bilirubin clearance. Pediatr Res. 2016;79:378–386.
   PubMed Web of Science ®Google Scholar
• Van De Steeg E, Stránecký V, Hartmannová H, et al. Complete OATP1B1 and OATP1B3 deficiency causes human Rotor syndrome by interrupting conjugated bilirubin reuptake into the liver. J Clin Invest. 2012;122:519–528.
   PubMed Web of Science ®Google Scholar
• Van De Steeg E, Wagenaar E, van der Kruijssen CMM, et al. Organic anion transporting polypeptide 1a/1b-knockout mice provide insights into hepatic handling of bilirubin, bile acids, and drugs. J Clin Invest. 2010;120:2942–2952.
   PubMed Web of Science ®Google Scholar
• Isidor B, Pichon O, Redon R, et al. Mesomelia-synostoses syndrome results from deletion of sulf1 and slco5a1 genes at 8q13. Am J Hum Genet. 2010;87:95–100.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Xia W, He J, et al. Exome sequencing identifies SLCO2A1 mutations as a cause of primary hypertrophic osteoarthropathy. Am J Hum Genet. 2012;90:125–132.
   PubMed Web of Science ®Google Scholar
• Umeno J, Hisamatsu T, Esaki M, et al. a hereditary enteropathy caused by mutations in the SLCO2A1 gene, encoding a prostaglandin transporter. PLoS Genet. 2015;11:1–15.
   Web of Science ®Google Scholar
• Nakanishi T, Hasegawa Y, Mimura R, et al. Prostaglandin transporter (PGT/SLCO2A1) protects the lung from bleomycin-induced fibrosis. PLoS One. 2015;10:1–19.
   Web of Science ®Google Scholar
• Höglinger GU, Melhem NM, Dickson DW, et al. Identification of common variants influencing risk of the tauopathy progressive supranuclear palsy. Nat Genet. 2011;43:699–705.
   PubMed Web of Science ®Google Scholar
• Kenny EE, Pe’er I, Karban A, et al. A genome-wide scan of Ashkenazi Jewish Crohn’s disease suggests novel susceptibility loci. PLoS Genet. 2012;8:e1002559.
   PubMed Web of Science ®Google Scholar
• Lee W, Glaeser H, Smith LH, et al. Polymorphisms in human organic anion-transporting polypeptide 1A2 (OATP1A2): implications for altered drug disposition and central nervous system drug entry. J Biol Chem. 2005;280:9610–9617.
   PubMed Web of Science ®Google Scholar
• Bronger H, Konig J, Kopplow K, et al. ABCC drug efflux pumps and organic anion uptake transporters in human gliomas and the blood-tumor barrier. Cancer Res. 2005;65:11419–11428.
   PubMed Web of Science ®Google Scholar
• Wlcek K, Svoboda M, Thalhammer T, et al. Altered expression of organic anion transporter polypeptide (OATP) genes in human breast carcinoma. Cancer Biol Ther. 2008;7:1450–1455.
   PubMed Web of Science ®Google Scholar
• Ballestero MR, Monte MJ, Briz O, et al. Expression of transporters potentially involved in the targeting of cytostatic bile acid derivatives to colon cancer and polyps. Biochem Pharmacol. 2006;72:729–738.
   PubMed Web of Science ®Google Scholar
• Liedauer R, Svoboda M, Wlcek K, et al. Different expression patterns of organic anion transporting polypeptides in osteosarcomas, bone metastases and aneurysmal bone cysts. Oncol Rep. 2009;22:1485–1492.
   PubMed Web of Science ®Google Scholar
• Meyer Zu Schwabedissen HE, Tirona RG, Yip CS, et al. Interplay between the nuclear receptor pregnane X receptor and the uptake transporter organic anion transporter polypeptide 1A2 selectively enhances estrogen effects in breast cancer. Cancer Res. 2008;68:9338–9347.
   PubMed Web of Science ®Google Scholar
• Arakawa H, Nakanishi T, Yanagihara C, et al. Enhanced expression of organic anion transporting polypeptides (OATPs) in androgen receptor-positive prostate cancer cells: possible role of OATP1A2 in adaptive cell growth under androgen-depleted conditions. Biochem Pharmacol. 2012;84:1070–1077.
   PubMed Web of Science ®Google Scholar
• Thakkar N, Lockhart AC, Lee W. Role of organic anion-transporting polypeptides (OATPs) in cancer therapy. AAPS J. 2015;17:535–545.
   PubMed Web of Science ®Google Scholar
• Zu Schwabedissen HEM, Boettcher K, Steiner T, et al. OATP1B3 is expressed in pancreatic b-islet cells and enhances the insulinotropic effect of the sulfonylurea derivative glibenclamide. Diabetes. 2014;63:775–784.
   PubMed Web of Science ®Google Scholar
• Furihata T, Sun YCK. Cancer-type organic anion transporting polypeptide 1B3: current knowledge of the gene structure, expression profile, functional implications and future perspectives. Curr Drug Metab. 2015;16:474–485.
   PubMed Web of Science ®Google Scholar
• Kang J, Chapdelaine P, Parent J, et al. Expression of human prostaglandin transporter in the human endometrium across the menstrual cycle. J Clin Endocrinol Metab. 2005;90:2308–2313.
   PubMed Web of Science ®Google Scholar
• Choi K, Zhuang H, Crain BDS. Expression and localization of prostaglandin transporter in Alzheimer disease brains and age-matched controls. J Neuroimmunol. 2008;195:81–87.
   PubMed Web of Science ®Google Scholar
• Wlcek K, Svoboda M, Riha J, et al. The analysis of organic anion transporting polypeptide (OATP) mRNA and protein patterns in primary and metastatic liver cancer. Cancer Biol Ther. 2011;11:801–811.
   PubMed Web of Science ®Google Scholar
• Al Sarakbi W, Mokbel R, Salhab M, et al. The role of STS and OATP-B mRNA expression in predicting the clinical outcome in human breast cancer. Anticancer Res. 2006;26:4985–4990.
   PubMed Web of Science ®Google Scholar
• Nozawa T, Suzuki M, Takahashi K, et al. Involvement of estrone-3-sulfate transporters in proliferation of hormone-dependent breast cancer cells. J Pharmacol Exp Ther. 2004;311:1032–1037.
   PubMed Web of Science ®Google Scholar
• Pizzagalli F, Varga Z, Huber RD, et al. Identification of steroid sulfate transport processes in the human mammary gland. J Clin Endocrinol Metab. 2003;88:3902–3912.
   PubMed Web of Science ®Google Scholar
• Nozawa T, Suzuki M, Yabuuchi H, et al. Suppression of cell proliferation by inhibition of estrone-3-sulfate transporter in estrogen-dependent breast cancer cells. Pharm Res. 2005;22:1634–1641.
   PubMed Web of Science ®Google Scholar
• Sato K, Sugawara J, Sato T, et al. Expression of organic anion transporting polypeptide E (OATP-E) in human placenta. Placenta. 2003;24:144–148.
   PubMed Web of Science ®Google Scholar
• Brenner S, Klameth L, Riha J, et al. Specific expression of OATPs in primary small cell lung cancer (SCLC) cells as novel biomarkers for diagnosis and therapy. Cancer Lett. 2015;356:517–524.
   PubMed Web of Science ®Google Scholar
• Okabe M, Szakács G, Reimers MA, et al. Profiling SLCO and SLC22 genes in the NCI-60 cancer cell lines to identify drug uptake transporters. Mol Cancer Ther. 2008;7:3081–3091.
   PubMed Web of Science ®Google Scholar
• Lee S-Y, Williamson B, Caballero OL, et al. Identification of the gonad-specific anion transporter SLCO6A1 as a cancer/testis (CT) antigen expressed in human lung cancer. Cancer Immun. 2004;4:13.
   PubMedGoogle Scholar
• Muto M, Onogawa T, Suzuki T, et al. Human liver-specific organic anion transporter-2 is a potent prognostic factor for human breast carcinoma. Cancer Sci. 2007;98:1570–1576.
   PubMed Web of Science ®Google Scholar
• Wright JL, Kwon EM, Ostrander EA, et al. Expression of SLCO transport genes in castration-resistant prostate cancer and impact of genetic variation in SLCO1B3 and SLCO2B1 on prostate cancer outcomes. Cancer Epidemiol Biomarkers Prev. 2011;20:619–627.
   PubMed Web of Science ®Google Scholar
• Hamada A, Sissung T, Price DK, et al. Effect of SLCO1B3 haplotype on testosterone transport and clinical outcome in caucasian patients with androgen-independent prostatic cancer. Clin Cancer Res. 2008;14:3312–3318.
   PubMed Web of Science ®Google Scholar
• Yamaguchi H, Okada M, Akitaya S, et al. Transport of fluorescent chenodeoxycholic acid via the human organic anion transporters OATP1B1 and OATP1B3. J Lipid Res. 2006;47:1196–1202.
   PubMed Web of Science ®Google Scholar
• de Waart DR, Häusler S, Vlaming MLH, et al. Hepatic transport mechanisms of cholyl-L-lysyl-fluorescein. J Pharmacol Exp Ther. 2010;334:78–86.
   PubMed Web of Science ®Google Scholar
• Kopplow K, Letschert K, König J, et al. Human hepatobiliary transport of organic anions analyzed by quadruple-transfected cells. Mol Pharmacol. 2005;68:1031–1038.
   PubMed Web of Science ®Google Scholar
• Sun D, Lennernas H, Welage LS, et al. 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. 2002;19:1400–1416.
   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;459:262–265.
   PubMed Web of Science ®Google Scholar
• Li M, de Graaf IAM, Groothuis GMM. Precision-cut intestinal slices: alternative model for drug transport, metabolism, and toxicology research. Expert Opin Drug Metab Toxicol. 2016;5255:1–16.
   Google Scholar
• Soldatow VVY, Lecluyse EEL, Griffith LLG, et al. In vitro models for liver toxicity testing. Toxicol Res (Camb). 2013;2:23–39.
   PubMed Web of Science ®Google Scholar
• Herzog N, Hansen M, Miethbauer S, et al. Primary-like human hepatocytes genetically engineered to obtain proliferation competence display hepatic differentiation characteristics in monolayer and organotypical spheroid cultures. Cell Biol Int. 2016;40:341–353.
   PubMed Web of Science ®Google Scholar
• Godoy P, Hewitt NJ, Albrecht U, et al. 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. 2013;87:1315–1530.
   Web of Science ®Google Scholar
• Evers R, Chu XY. Role of the murine organic anion-transporting polypeptide 1b2 (OATP1b2) in drug disposition and hepatotoxicity. Mol Pharmacol. 2008;74:309–311.
   PubMed Web of Science ®Google Scholar
• Shen H, Dai J, Liu T, et al. Coproporphyrins I and III as functional markers of OATP1B activity: in vitro and in vivo evaluation in preclinical species. J Pharmacol Exp Ther. 2016.357:382–393.
   Web of Science ®Google Scholar
• Lu H, Choudhuri S, Ogura K, et al. Characterization of organic anion transporting polypeptide 1b2-null mice: essential role in hepatic uptake/toxicity of phalloidin and microcystin-LR. Toxicol Sci. 2008;103:35–45.
   PubMed Web of Science ®Google Scholar
• Zaher H, Meyer Zu Schwabedissen HE, Tirona RG, et al. Targeted disruption of murine organic anion-transporting polypeptide 1b2 (OATP1b2/SLCO1b2) significantly alters disposition of prototypical drug substrates pravastatin and rifampin. Mol Pharmacol. 2008;74:320–329.
   PubMed Web of Science ®Google Scholar
• Kuo K-L, Zhu H, McNamara PJ, et al. Localization and functional characterization of the Rat OATP4c1 Transporter in an in vitro cell system and rat tissues. PLoS One. 2012;7:e39641.
   PubMed Web of Science ®Google Scholar
• van de Steeg E, van der Kruijssen CM, Wagenaar E, et al. Methotrexate pharmacokinetics in transgenic mice with liver-specific expression of human organic anion-transporting polypeptide 1B1 (SLCO1B1). Drug Metab Dispos. 2009;37:277–281.
   PubMed Web of Science ®Google Scholar
• van de Steeg E, van Esch A, Wagenaar E, et al. Influence of human OATP1B1, OATP1B3, and OATP1A2 on the pharmacokinetics of methotrexate and paclitaxel in humanized transgenic mice. Clin Cancer Res. 2013;19:821–832.
   PubMed Web of Science ®Google Scholar
• Durmus S, Lozano-Mena G, van Esch A, et al. Preclinical mouse models to study human OATP1B1- and OATP1B3-mediated drug-drug interactions in vivo. Mol Pharm. 2015;12:4259–4269.
   PubMed Web of Science ®Google Scholar
• List AF, Spier C, Greer J, et al. Phase I/II trial of cyclosporine as a chemotherapy-resistance modifier in acute leukemia. J Clin Oncol. 1993;11:1652–1660.
   PubMed Web of Science ®Google Scholar
• Khurana V, Minocha M, Pal D, et al. Role of OATP-1B1 and/or OATP-1B3 in hepatic disposition of tyrosine kinase inhibitors. Drug Metabol Drug Interact. 2014;29:179–190.
   PubMedGoogle Scholar
• Nozawa T, Minami H, Sugiura S, et al. Role of organic anion transporter OATP1B1 (OATP-C) in hepatic uptake of irinotecan and its active metabolite, 7-ethyl-10-hydroxycamptothecin: in vitro evidence and effect of single nucleotide polymorphisms. Drug Metab Dispos. 2005;33:434–439.
   PubMed Web of Science ®Google Scholar
• Oswald S, König J, Lütjohann D, et al. Disposition of ezetimibe is influenced by polymorphisms of the hepatic uptake carrier OATP1B1. Pharmacogenet Genomics. 2008;18:559–568.
   PubMed Web of Science ®Google Scholar
• Kalliokoski A, Neuvonen M, Neuvonen PJ, et al. Different effects of SLCO1B1 polymorphism on the pharmacokinetics and pharmacodynamics of repaglinide and nateglinide. J Clin Pharmacol. 2008;48:311–321.
   PubMed Web of Science ®Google Scholar
• Giannakopoulou E, Ragia G, Kolovou V, et al. No impact of SLCO1B1 521T>C, 388A>G and 411G>A polymorphisms on response to statin therapy in the Greek population. Mol Biol Rep. 2014;41:4631–4638.
   PubMed Web of Science ®Google Scholar
• Tirona RG, Leake BF, Merino G, et al. Polymorphisms in OATP-C: identification of multiple allelic variants associated with altered transport activity among European- and African-Americans. J Biol Chem. 2001;276:35669–35675.
   PubMed Web of Science ®Google Scholar
• Niemi M, Pasanen MK, Neuvonen PJ. Organic anion transporting polypeptide 1B1: a genetically polymorphic transporter of major importance for hepatic drug uptake. Pharmacol Rev. 2011;63:157–181.
   PubMed Web of Science ®Google Scholar
• Link E, Parish S, Armitage J, et al.; SEARCH Collaborative Group. SLCO1B1 variants and statin-induced myopathy — A genomewide study. N Engl J Med. 2008;359:789–799.
   PubMed Web of Science ®Google Scholar
• Tornio A, Vakkilainen J, Neuvonen M, et al. SLCO1B1 polymorphism markedly affects the pharmacokinetics of lovastatin acid. Pharmacogenet Genomics. 2015;25:382–387.
   PubMed Web of Science ®Google Scholar
• Gerloff T, Schaefer M, Mwinyi J, et al. Influence of the SLCO1Bl*1b and *5 haplotypes on pravastatin’s cholesterol lowering capabilities and basal sterol serum levels. Naunyn Schmiedebergs Arch Pharmacol. 2006;373:45–50.
   PubMed Web of Science ®Google Scholar
• Li LM, Chen L, Deng GH, et al. SLCO1B1*15 haplotype is associated with rifampin-induced liver injury. Mol Med Rep. 2012;6:75–82.
   PubMed Web of Science ®Google Scholar
• Letschert K, Keppler D, Konig J. Mutations in the SLCO1B3 gene affecting the substrate specificity of the hepatocellular uptake transporter OATP1B3 (OATP8). Pharmacogenetics. 2004;14:441–452.
   PubMedGoogle Scholar
• Yamakawa Y, Hamada A, Nakashima R, et al. Association of genetic polymorphisms in the influx transporter SLCO1B3 and the efflux transporter ABCB1 with imatinib pharmacokinetics in patients with chronic myeloid leukemia. Ther Drug Monit. 2011;33:244–250.
   PubMed Web of Science ®Google Scholar
• Chew SC, Sandanaraj E, Singh O, et al. Influence of SLCO1B3 haplotype-tag SNPs on docetaxel disposition in Chinese nasopharyngeal cancer patients. Br J Clin Pharmacol. 2012;73:606–618.
   PubMed Web of Science ®Google Scholar
• Fujimoto N, Kubo T, Inatomi H, et al. Polymorphisms of the androgen transporting gene SLCO2B1 may influence the castration resistance of prostate cancer and the racial differences in response to androgen deprivation. Prostate Cancer Prostatic Dis. 2013;16:336–340.
   PubMed Web of Science ®Google Scholar
• Mougey EB, Feng H, Castro M, et al. Absorption of montelukast is transporter mediated: a common variant of OATP2B1 is associated with reduced plasma concentrations and poor response. Pharmacogenet Genomics. 2009;19:129–138.
   PubMed Web of Science ®Google Scholar
• Nozawa T, Nakajima M, Tamai I, et al. Genetic polymorphisms of human organic anion transporters OATP-C (SLC21A6) and OATP-B (SLC21A9): allele frequencies in the Japanese population and functional analysis. J Pharmacol Exp Ther. 2002;302:804–813.
   PubMed Web of Science ®Google Scholar
• Deepak V, Svati HS, Spasojevic I, et al. The SLCO1B1* 5 genetic variant is associated with statin-induced side effects. J Am Coll Cardiol. 2009;54:1609–1616.
   PubMed Web of Science ®Google Scholar
• Donnelly LA, Doney a SF, Tavendale R, et al. Common nonsynonymous substitutions in SLCO1B1 predispose to statin intolerance in routinely treated individuals with type 2 diabetes: a go-DARTS study. Clin Pharmacol Ther. 2011;89:210–216.
   PubMed Web of Science ®Google Scholar
• Pasanen MK, Fredrikson H, Neuvonen PJ, et al. Different effects of SLCO1B1 polymorphism on the pharmacokinetics of atorvastatin and rosuvastatin. Clin Pharmacol Ther. 2007;82:726–733.
   PubMed Web of Science ®Google Scholar
• Generaux GT, Bonomo FM, Johnson M, et al. Impact of SLCO1B1 (OATP1B1) and ABCG2 (BCRP) genetic polymorphisms and inhibition on LDL-C lowering and myopathy of statins. Xenobiotica. 2011;41:639–651.
   PubMed Web of Science ®Google Scholar
• Tamai I. Oral drug delivery utilizing intestinal OATP transporters. Adv Drug Deliv Rev. 2012;64:508–514.
   PubMed Web of Science ®Google Scholar
• Solon EG. Use of radioactive compounds and autoradiography to determine drug tissue distribution. Chem Res Toxicol. 2012;25:543–555.
   PubMed Web of Science ®Google Scholar