Evaluation of the Usefulness of Breast Cancer Resistance Protein (BCRP) Knockout Mice and BCRP Inhibitor-Treated Monkeys to Estimate the Clinical Impact of BCRP Modulation on the Pharmacokinetics of BCRP Substrates

Pharmaceutical Research

Volumn 32, Issue 5, 2015, Pages 1634-1647

  Karibe, Tsuyoshi ^a   Hagihara Nakagomi, Rie ^a   Abe, Koji ^a   Imaoka, Tomoki ^a   Mikkaichi, Tsuyoshi ^a   Yasuda, Satoru ^a   Hirouchi, Masakazu ^a   Watanabe, Nobuaki ^a   Okudaira, Noriko ^a   Izumi, Takashi ^a  

^a DAIICHI SANKYO CO   (Japan)

Author keywords

ABCG2 421C>A; BCRP; Cynomolgus monkey; Gastrointestinal absorption; Knockout mouse

Indexed keywords

ABC TRANSPORTER; ABCG2 PROTEIN, MOUSE; ACRIDINE DERIVATIVE; ELACRIDAR; FLUINDOSTATIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INDOLE DERIVATIVE; MONOUNSATURATED FATTY ACID; NONSTEROID ANTIINFLAMMATORY AGENT; PITAVASTATIN; QUINOLINE DERIVATIVE; ROSUVASTATIN; SALAZOSULFAPYRIDINE; TETRAHYDROISOQUINOLINE DERIVATIVE;

ANIMAL; ANTAGONISTS AND INHIBITORS; AREA UNDER THE CURVE; BLOOD; CACO 2 CELL LINE; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; INTESTINE ABSORPTION; KNOCKOUT MOUSE; MACACA FASCICULARIS; MALE; METABOLISM;

ACRIDINES; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; AREA UNDER CURVE; ATP-BINDING CASSETTE TRANSPORTERS; CACO-2 CELLS; FATTY ACIDS, MONOUNSATURATED; FEMALE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; INDOLES; INTESTINAL ABSORPTION; MACACA FASCICULARIS; MALE; MICE, KNOCKOUT; QUINOLINES; ROSUVASTATIN CALCIUM; SULFASALAZINE; TETRAHYDROISOQUINOLINES;

EID: 84939991160     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-014-1563-4     Document Type: Article

References (42)

1. Mao Q, Unadkat JD. Role of the breast cancer resistance protein (ABCG2) in drug transport. AAPS J. 2005;7:E118-33.
2. Maliepaard M, Scheffer GL, Faneyte IF, van Gastelen MA, Pijnenborg AC, Schinkel AH, et al. Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res. 2001;61:3458-64.
3. Wright JA, Haslam IS, Coleman T, Simmons NL. Breast cancer resistance protein BCRP (ABCG2)-mediated transepithelial nitrofurantoin secretion and its regulation in human intestinal epithelial (Caco-2) layers. Eur J Pharmacol. 2011;672:70-6.
4. Jani M, Szabó P, Kis E, Molnár E, Glavinas H, Krajcsi P. Kinetic characterization of sulfasalazine transport by human ATP-binding cassette G2. Biol Pharm Bull. 2009;32:497-9.
5. Kitamura S, Maeda K, Wang Y, Sugiyama Y. Involvement of multiple transporters in the hepatobiliary transport of rosuvastatin. Drug Metab Dispos. 2008;36:2014-23.
6. Hirano M, Maeda K, Matsushima S, Nozaki Y, Kusuhara H, Sugiyama Y. Involvement of BCRP (ABCG2) in the biliary excretion of pitavastatin. Mol Pharmacol. 2005;68:800-7.
7. Li J, Volpe DA, Wang Y, Zhang W, Bode C, Owen A, et al. Use of transporter knockdown Caco-2 cells to investigate the in vitro efflux of statin drugs. Drug Metab Dispos. 2011;39:1196-202.
8. Yamasaki Y, Ieiri I, Kusuhara H, Sasaki T, Kimura M, Tabuchi H, et al. Pharmacogenetic characterization of sulfasalazine disposition based on NAT2 and ABCG2 (BCRP) gene polymorphisms in humans. Clin Pharmacol Ther. 2008;84:95-103.
9. Urquhart BL, Ware JA, Tirona RG, Ho RH, Leake BF, Schwarz UI, et al. Breast cancer resistance protein (ABCG2) and drug disposition: intestinal expression, polymorphisms and sulfasalazine as an in vivo probe. Pharmacogenet Genomics. 2008;18:439-48.
10. Adkison KK, Vaidya SS, Lee DY, Koo SH, Li L, Mehta AA, et al. Oral sulfasalazine as a clinical BCRP probe substrate: pharmacokinetic effects of genetic variation (C421A) and pantoprazole coadministration. J Pharm Sci. 2010;99:1046-62.
11. Zhang W, Yu BN, He YJ, Fan L, Li Q, Liu ZQ, et al. Role of BCRP 421C>A polymorphism on rosuvastatin pharmacokinetics in healthy Chinese males. Clin Chim Acta. 2006;373:99-103.
12. Keskitalo JE, Zolk O, Fromm MF, Kurkinen KJ, Neuvonen PJ, Niemi M. ABCG2 polymorphism markedly affects the pharmacokinetics of atorvastatin and rosuvastatin. Clin Pharmacol Ther. 2009;86:197-203.
13. Keskitalo JE, Pasanen MK, Neuvonen PJ, Niemi M. Different effects of the ABCG2 c.421C>A SNP on the pharmacokinetics of fluvastatin, pravastatin and simvastatin. Pharmacogenomics. 2009;10:1617-24.
14. Imai Y, Nakane M, Kage K, Tsukahara S, Ishikawa E, Tsuruo T, et al. C421A polymorphism in the human breast cancer resistance protein gene is associated with low expression of Q141K protein and low-level drug resistance. Mol Cancer Ther. 2002;1:611-6.
15. Kobayashi D, Ieiri I, Hirota T, Takane H, Maegawa S, Kigawa J, et al. Functional assessment of ABCG2 (BCRP) gene polymorphisms to protein expression in human placenta. Drug Metab Dispos. 2005;33:94-101.
16. Zamber CP, Lamba JK, Yasuda K, Farnum J, Thummel K, Schuetz JD, et al. Natural allelic variants of breast cancer resistance protein (BCRP) and their relationship to BCRP expression in human intestine. Pharmacogenetics. 2003;13:19-28.
17. Mizuno T, Fukudo M, Terada T, Kamba T, Nakamura E, Ogawa O, et al. Impact of Genetic Variation in Breast Cancer Resistance Protein (BCRP/ABCG2) on Sunitinib Pharmacokinetics. Drug Metab Pharmacokinet. 2012;27:631-9.
18. Adkison KK, Vaidya SS, Lee DY, Koo SH, Li L, Mehta AA, et al. The ABCG2 C421A polymorphism does not affect oral nitrofurantoin pharmacokinetics in healthy Chinese male subjects. Br J Clin Pharmacol. 2008;66:233-9.
19. Ieiri I, Suwannakul S, Maeda K, Uchimaru H, Hashimoto K, Kimura M, et al. SLCO1B1 (OATP1B1, an uptake transporter) and ABCG2 (BCRP, an efflux transporter) variant alleles and pharmacokinetics of pitavastatin in healthy volunteers. Clin Pharmacol Ther. 2007;82:541-7.
20. Zaher H, Khan AA, Palandra J, Brayman TG, Yu L, Ware JA. Breast cancer resistance protein (Bcrp/abcg2) is a major determinant of sulfasalazine absorption and elimination in the mouse. Mol Pharm. 2006;3:55-61.
21. Selvakumar S, Bhutani P, Ghosh K, Krishnamurthy P, Kallipatti S, Selvam S, et al. Expression and characterization of cynomolgus monkey cytochrome CYP3A4 in a novel human embryonic kidney cell-based mammalian system. Drug Metab Dispos. 2014;42:369-76.
22. Ward KW, Azzarano LM. Preclinical pharmacokinetic properties of the P-glycoprotein inhibitor GF120918A (HCl salt of GF120918, 9,10-dihydro-5-methoxy-9-oxo-N-[4-[2-(1,2,3,4-tetrahydro-6,7-dimethoxy-2-isoquinolinyl)ethyl]phenyl]-4-acridine-carboxamide) in the mouse, rat, dog, and monkey. J Pharmacol Exp Ther. 2004;310:703-9.
23. Ogasawara A, Kume T, Kazama E. Effect of oral ketoconazole on intestinal first-pass effect of midazolam and fexofenadine in cynomolgus monkeys. Drug Metab Dispos. 2007;35:410-8.
24. Shen H, Yang Z, Mintier G, Han YH, Chen C, Balimane P, et al. Cynomolgus monkey as a potential model to assess drug interactions involving hepatic organic anion transporting polypeptides: in vitro, in vivo, and in vitro-to-in vivo extrapolation. J Pharmacol Exp Ther. 2013;344:673-85.
25. Takahashi T, Ohtsuka T, Yoshikawa T, Tatekawa I, Uno Y, Utoh M, et al. Pitavastatin as an in vivo probe for studying hepatic organic anion transporting polypeptide-mediated drug-drug interactions in cynomolgus monkeys. Drug Metab Dispos. 2013;41:1875-82.
26. Kamiyama E, Sugiyama D, Nakai D, Miura S, Okazaki O. Culture period-dependent change of function and expression of ATP-binding cassette transporters in Caco-2 cells. Drug Metab Dispos. 2009;37:1956-62.
27. Imaoka T, Mikkaichi T, Abe K, Hirouchi M, Okudaira N, Izumi T. Integrated approach of in vivo and in vitro evaluation of the involvement of hepatic uptake organic anion transporters in the drug disposition in rats using rifampicin as an inhibitor. Drug Metab Dispos. 2013;41:1442-9.
28. Ward KW, Smith BR. A comprehensive quantitative and qualitative evaluation of extrapolation of intravenous pharmacokinetic parameters from rat, dog, and monkey to humans. II. Volume of distribution and mean residence time. Drug Metab Dispos. 2004;32:612-9.
29. Ward KW, Smith BR. A comprehensive quantitative and qualitative evaluation of extrapolation of intravenous pharmacokinetic parameters from rat, dog, and monkey to humans. I Clearance. Drug Metab Dispos. 2004;32:603-11.
30. Neuvonen PJ. Drug interactions with HMG-CoA reductase inhibitors (statins): the importance of CYP enzymes, transporters and pharmacogenetics. Curr Opin Investig Drugs. 2010;11:323-32.
31. US FDA. Drug approval package: Crestor (Rosuvastatin Calcium) Tablets. Pharmacology Review(s) [Internet]. Available from: http://www.accessdata.fda.gov/drugsatfda-docs/nda/2003/21-366-Crestor.cfm.
32. US FDA. Drug approval package: Livalo (Pitavastatin) Tablets. Pharmacology Review(s) [Internet]. Available from: http://www.accessdata.fda.gov/drugsatfda-docs/nda/2009/022363s000TOC.cfm.
33. Reinoso RF, Sánchez Navarro A, García MJ, Prous JR. Preclinical pharmacokinetics of statins. Methods Find Exp Clin Pharmacol. 2002;24:593-613.
34. Zheng W, Winter SM, Mayersohn M, Bishop JB, Sipes IG. Toxicokinetics of sulfasalazine (salicylazosulfapyridine) and its metabolites in B6C3F1 mice. Drug Metab Dispos. 1993;21:1091-7.
35. Das KM, Chowdhury JR, Zapp B, Fara JW. Small bowel absorption of sulfasalazine and its hepatic metabolism in human beings, cats, and rats. Gastroenterology. 1979;77:280-4.
36. Karlgren M, Vildhede A, Norinder U, Wisniewski JR, Kimoto E, Lai Y, et al. Classification of inhibitors of hepatic organic anion transporting polypeptides (OATPs): influence of protein expression on drug-drug interactions. J Med Chem. 2012;55:4740-63.
37. US FDA. Label and Approval History: Azulfidine (Sulfasalazine) Tablets. [Internet]. Available from: http://www.accessdata.fda.gov/drugsatfda-docs/label/2014/007073s128lbl.pdf.
38. Sjöquist B, Ahnfelt NO, Andersson S. d'Argy R, Fjellner G, Hatsuoka M, et al. Pharmacokinetics of Salazosulfapyridine (Sulfasalazine, SASP). V. Pharmacokinetics of SASP after a single intravenous or oral administration in the dog. Drug Metab Pharmacokinet. 1991;6:491-507.
39. Huang L, Be X, Tchaparian EH, Colletti AE, Roberts J, Langley M, et al. Deletion of Abcg2 has differential effects on excretion and pharmacokinetics of probe substrates in rats. J Pharmacol Exp Ther. 2012;343:316-24.
40. Kruijtzer CMF, Beijnen JH, Rosing H, ten Bokkel Huinink WW, Schot M, Jewell RC, et al. Increased oral bioavailability of topotecan in combination with the breast cancer resistance protein and P-glycoprotein inhibitor GF120918. J Clin Oncol. 2002;20:2943-50.
41. Kuppens IELM, Witteveen EO, Jewell RC, Radema SA, Paul EM, Mangum SG, et al. A phase I, randomized, open-label, parallel-cohort, dose-finding study of elacridar (GF120918) and oral topotecan in cancer patients. Clin Cancer Res. 2007;13:3276-85.
42. Matsson P, Pedersen JM, Norinder U, Bergström CAS, Artursson P. Identification of novel specific and general inhibitors of the three major human ATP-binding cassette transporters P-gp, BCRP and MRP2 among registered drugs. Pharm Res. 2009;26:1816-31.