Quantitative investigation of the role of breast cancer resistance protein (Bcrp/Abcg2) in limiting brain and testis penetration of xenobiotic compounds

Drug Metabolism and Disposition

Volumn 36, Issue 6, 2008, Pages 995-1002

  Enokizono, Junichi ^a   Kusuhara, Hiroyuki ^a   Ose, Atsushi ^a   Schinkel, Alfred H ^b   Sugiyama, Yuichi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; 2 AMINO 3,8 DIMETHYLIMIDAZO[4,5 F]QUINOXALINE; 4' HYDROXYL 2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; BREAST CANCER RESISTANCE PROTEIN; DAIDZEIN; DANTROLENE; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN 1; PRAZOSIN; PROTEIN MDR1A; TRIAMTERENE; XENOBIOTIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD TESTIS BARRIER; BRAIN PERFUSION; CANCER RESISTANCE; CELL TRANSPORT; CONTROLLED STUDY; DRUG ACTIVITY; DRUG CLEARANCE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; TISSUE DISTRIBUTION; XENOBIOTIC METABOLISM;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BRAIN; CELL LINE; DANTROLENE; DOGS; IMIDAZOLES; LLC-PK1 CELLS; MALE; MICE; MICE, KNOCKOUT; P-GLYCOPROTEINS; PRAZOSIN; QUINOXALINES; SWINE; TESTIS; TRIAMTERENE; XENOBIOTICS;

MUS;

EID: 44149086662     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.107.019257     Document Type: Article

References (42)

1. Adachi Y, Suzuki H, Schinkel AH, and Sugiyama Y (2005) Role of breast cancer resistance protein (Bcrp1/Abcg2) in the extrusion of glucuronide and sulfate conjugates from enterocytes to intestinal lumen. Mol Pharmacol 67:923-928.
2. Adachi Y, Suzuki H, and Sugiyama Y (2001) Comparative studies on in vitro methods for evaluating in vivo function of MDR1 P-glycoprotein. Pharmacol Res 18:1660-1668.
3. Ando T, Kusuhara H, Merino G, Alvarez AI, Schinkel AH, and Sugiyama Y (2007) Involvement of breast cancer resistance protein (ABCG2) in the biliary excretion mechanism of fluoroquinolones. Drug Metab Dispos 35:1873-1879.
4. Augustine LM, Markelewicz RJ, Jr., Boekelheide K, and Cherrington NJ (2005) Xenobiotic and endobiotic transporter mRNA expression in the blood-testis barrier. Drug Metab Dispos 33:182-189.
5. Bai J, Lai L, Yeo HC, Goh BC, and Tan TM (2004) Multidrug resistance protein 4 (MRP4/ABCC4) mediates efflux of bimane-glutathione. Int J Biochem Cell Biol 36:247-257.
6. Bart J, Groen HJ, van der Graaf WT, Hollema H, Hendrikse NH, Vaalburg W, Sleijfer DT, and de Vries EG (2002) An oncological view on the blood-testis barrier. Lancet Oncol 3:357-363.
7. Bart J, Hollema H, Groen HJ, de Vries EG, Hendrikse NH, Sleijfer DT, Wegman TD, Vaalburg W, and van der Graaf WT (2004) The distribution of drug-efflux pumps, P-gp, BCRP, MRP1 and MRP2, in the normal blood-testis barrier and in primary testicular tumours. Eur J Cancer 40:2064-2070.
8. Bihorel S, Camenisch G, Lemaire M, and Scherrmann JM (2007) Influence of breast cancer resistance protein (Abcg2) and p-glycoprotein (Abcb1a) on the transport of imatinib mesylate (Gleevec) across the mouse blood-brain barrier. J Neurochem 102:1749-1757.
9. Breedveld P, Pluim D, Cipriani G, Wielinga P, van Tellingen O, Schinkel AH, and Schellens JH (2005) The effect of Bcrp1 (Abcg2) on the in vivo pharmacokinetics and brain penetration of imatinib mesylate (Gleevec): implications for the use of breast cancer resistance protein and P-glycoprotein inhibitors to enable the brain penetration of imatinib in patients. Cancer Res 65:2577-2582.
10. Burger H, van Tol H, Boersma AW, Brok M, Wiemer EA, Stoter G, and Nooter K (2004) Imatinib mesylate (STI571) is a substrate for the breast cancer resistance protein (BCRP)/ABCG2 drug pump. Blood 104:2940-2942.
11. Cisternino S, Mercier C, Bourasset F, Roux F, and Scherrmann JM (2004) Expression, upregulation, and transport activity of the multidrug-resistance protein Abcg2 at the mouse blood-brain barrier. Cancer Res 64:3296-3301.
12. Dagenais C, Rousselle C, Pollack GM, and Scherrmann JM (2000) Development of an in situ mouse brain perfusion model and its application to mdr1a P-glycoprotein-deficient mice. J Cereb Blood Flow Metab 20:381-386.
13. de Lange EC, Marchand S, van den Berg D, van der Sandt IC, de Boer AG, Delon A, Bouquet S, and Couet W (2000) In vitro and in vivo investigations on fluoroquinolones; effects of the P-glycoprotein efflux transporter on brain distribution of sparfloxacin. Eur J Pharm Sci 12:85-93.
14. Dietrich CG, de Waart DR, Ottenhoff R, Bootsma AH, van Gennip AH, and Elferink RP (2001) Mrp2-deficiency in the rat impairs biliary and intestinal excretion and influences metabolism and disposition of the food-derived carcinogen 2-amino-1-methyl-6-phenylimidazo. Carcinogenesis 22:805-811.
15. Enokizono J, Kusuhara H, and Sugiyama Y (2007a) Involvement of breast cancer resistance protein (BCRP/ABCG2) in the biliary excretion and intestinal efflux of troglitazone sulfate, the major metabolite of troglitazone with a cholestatic effect. Drug Metab Dispos 35:209-214.
16. Enokizono J, Kusuhara H, and Sugiyama Y (2007b) Role of breast cancer resistance protein (Bcrp/Abcg2) in the disposition of phytoestrogens: the importance of Bcrp in the efflux transport in the blood-brain and -testis barriers. Mol Pharmacol 72:967-975.
17. Hirano M, Maeda K, Matsushima S, Nozaki Y, Kusuhara H, and Sugiyama Y (2005) Involvement of BCRP (ABCG2) in the biliary excretion of pitavastatin. Mol Pharmacol 68:800-807.
18. Jonker JW, Buitelaar M, Wagenaar E, Van Der Valk MA, Scheffer GL, Scheper RJ, Plosch T, Kuipers F, Elferink RP, Rosing H, et al. (2002) The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci U S A 99:15649-15654.
19. Jonker JW, Merino G, Musters S, van Herwaarden AE, Bolscher E, Wagenaar E, Mesman E, Dale TC, and Schinkel AH (2005) The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat Med 11:127-129.
20. Kim D and Guengerich FP (2005) Cytochrome P450 activation of arylamines and heterocyclic amines. Annu Rev Pharmacol Toxicol 45:27-49.
21. Kondo C, Onuki R, Kusuhara H, Suzuki H, Suzuki M, Okudaira N, Kojima M, Ishiwata K, Jonker JW, and Sugiyama Y (2005) Lack of improvement of oral absorption of ME3277 by prodrug formation is ascribed to the intestinal efflux mediated by breast cancer resistant protein (BCRP/ABCG2). Pharmacol Res 22:613-618.
22. Kondo C, Suzuki H, Itoda M, Ozawa S, Sawada J, Kobayashi D, Ieiri I, Mine K, Ohtsubo K, and Sugiyama Y (2004) Functional analysis of SNPs variants of BCRP/ABCG2. Pharmacol Res 21:1895-1903.
23. Kusuhara H and Sugiyama Y (2005) Active efflux across the blood-brain barrier: role of the solute carrier family. NeuroRx 2:73-85.
24. Kusuhara H and Sugiyama Y (2007) ATP-binding cassette, subfamily G (ABCG family). Pflugers Arch 453:735-744.
25. Kusuhara H, Suzuki H, Naito M, Tsuruo T, and Sugiyama Y (1998) Characterization of efflux transport of organic anions in a mouse brain capillary endothelial cell line. J Pharmacol Exp Ther 285:1260-1265.
26. Lee YJ, Kusuhara H, Jonker JW, Schinkel AH, and Sugiyama Y (2005) Investigation of efflux transport of dehydroepiandrosterone sulfate and mitoxantrone at the mouse blood-brain barrier: a minor role of breast cancer resistance protein. J Pharmacol Exp Ther 312:44-52.
27. Leggas M, Adachi M, Scheffer GL, Sun D, Wielinga P, Du G, Mercer KE, Zhuang Y, Panetta JC, Johnston B, et al. (2004) Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 24:7612-7621.
28. Leslie EM, Deeley RG, and Cole SP (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204:216-237.
29. Matsushima S, Maeda K, Kondo C, Hirano M, Sasaki M, Suzuki H, and Sugiyama Y (2005) Identification of the Hepatic efflux transporters of organic anions using double-transfected Madin-Darby canine kidney II cells expressing human organic anion-transporting polypeptide 1B1 (OATP1B1)/multidrug resistance-associated protein 2, OATP1B1/multidrug resistance 1, and OATP1B1/breast cancer resistance protein. J Pharmacol Exp Ther 314:1059-1067.
30. Mizuno N, Suzuki M, Kusuhara H, Suzuki H, Takeuchi K, Niwa T, Jonker JW, and Sugiyama Y (2004) Impaired renal excretion of 6-hydroxy-5,7-dimethyl-2- methylamino-4-(3-pyridylmethyl) benzothiazole (E3040) sulfate in breast cancer resistance protein (BCRP1/ABCG2) knockout mice. Drug Metab Dispos 32:898-901.
31. Sasabe H, Kato Y, Suzuki T, Itose M, Miyamoto G, and Sugiyama Y (2004) Differential involvement of multidrug resistance-associated protein 1 and P-glycoprotein in tissue distribution and excretion of grepafloxacin in mice. J Pharmacol Exp Ther 310:648-655.
32. Scherrmann JM (2005) Expression and function of multidrug resistance transporters at the blood-brain barriers. Expert Opin Drug Metab Toxicol 1:233-246.
33. Schinkel AH (1999) P-Glycoprotein, a gatekeeper in the blood-brain barrier. Adv Drug Deliv Rev 36:179-194.
34. Suzuki M, Suzuki H, Sugimoto Y, and Sugiyama Y (2003) ABCG2 transports sulfated conjugates of steroids and xenobiotics. J Biol Chem 278:22644-22649.
35. Uhr M, Steckler T, Yassouridis A, and Holsboer F (2000) Penetration of amitriptyline, but not of fluoxetine, into brain is enhanced in mice with blood-brain barrier deficiency due to mdr1a P-glycoprotein gene disruption. Neuropsychopharmacology 22:380-387.
36. van Herwaarden AE, Jonker JW, Wagenaar E, Brinkhuis RF, Schellens JH, Beijnen JH, and Schinkel AH (2003) The breast cancer resistance protein (Bcrp1/Abcg2) restricts exposure to the dietary carcinogen 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine. Cancer Res 63:6447-6452.
37. van Herwaarden AE, Wagenaar E, Karnekamp B, Merino G, Jonker JW, and Schinkel AH (2006) Breast cancer resistance protein (Bcrp1/Abcg2) reduces systemic exposure of the dietary carcinogens aflatoxin B1, IQ and Trp-P-1 but also mediates their secretion into breast milk. Carcinogenesis 27:123-130.
38. Volk EL, Farley KM, Wu Y, Li F, Robey RW, and Schneider E (2002) Overexpression of wild-type breast cancer resistance protein mediates methotrexate resistance. Cancer Res 62:5035-5040.
39. Wijnholds J, Scheffer GL, van der Valk M, van der Valk P, Beijnen JH, Scheper RJ, and Borst P (1998) Multidrug resistance protein 1 protects the oropharyngeal mucosal layer and the testicular tubules against drug-induced damage. J Exp Med 188:797-808.
40. Yagi Y, Shibutani S, Hodoshima N, Ishiwata K, Okudaira N, Li Q, Sai Y, Kato Y, and Tsuji A (2003) Involvement of multiple transport systems in the disposition of an active metabolite of a prodrug-type new quinolone antibiotic, prulifloxacin. Drug Metab Pharmacokinet 18:381-389.
41. Yamazaki M, Neway WE, Ohe T, Chen I, Rowe JF, Hochman JH, Chiba M, and Lin JH (2001) In vitro substrate identification studies for P-glycoprotein- mediated transport: species difference and predictability of in vivo results. J Pharmacol Exp Ther 296:723-735.
42. Zhang Y, Han H, Elmquist WF, and Miller DW (2000) Expression of various multidrug resistance-associated protein (MRP) homologues in brain microvessel endothelial cells. Brain Res 876:148-153.