Breast cancer resistance protein (Bcrp1/Abcg2) limits net intestinal uptake of quercetin in rats by facilitating apical efflux of glucuronides

Molecular Pharmacology

Volumn 67, Issue 6, 2005, Pages 1999-2006

  Sesink, Aloys L A ^a   Arts, Ilja C W ^b   De Boer, Vincent C J ^b   Breedveld, Pauline ^c   Schellens, Jan H M ^c   Hollman, Peter C H ^b   Russel, Frans G M ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; DRUG METABOLITE; FUMITREMORGIN C; GLUCURONIDE; ISOQUERCITRIN; ISORHAMNETIN; MULTIDRUG RESISTANCE PROTEIN 2; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; ABC TRANSPORTER; ABCG2 PROTEIN, RAT; MITOCHONDRIAL PROTEIN; MRP2 PROTEIN, S CEREVISIAE; QUERCETIN; RIBOSOME PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ABSORPTION; DRUG BLOOD LEVEL; GENETIC TRANSFECTION; INTESTINE; INTESTINE ABSORPTION; INTESTINE PERFUSION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; COMPARATIVE STUDY; DOG; DOSE RESPONSE; DRUG EFFECT; GENETICS; METABOLISM; RAT STRAIN; WISTAR RAT;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; DOGS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUCURONIDES; INTESTINES; MALE; MITOCHONDRIAL PROTEINS; QUERCETIN; RATS; RATS, MUTANT STRAINS; RATS, WISTAR; RIBOSOMAL PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 21744461919     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: 10.1124/mol.104.009753     Document Type: Article

References (40)

1. Adachi Y, Suzuki H, Schinkel AH, and Sugiyama Y (2004) 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. Allen JD, van Loevezijn A, Lakhai JM, van der Valk M, van Tellingen O, Reid G, Schellens JH, Koomen GJ, and Schinkel AH (2002) Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol Cancer Ther 1:417-425.
3. Arts ICW and Hollman PCH (2005) Polyphenols and disease risk in epidemiological studies. Am J Clin Nutr 81:317S-325S.
4. Arts ICW, Sesink ALA, Faassen-Peters M, and Hollman PCH (2004) The type of sugar moiety is a major determinant of the small intestinal uptake and subsequent biliary excretion of dietary quercetin glycosides. Br J Nutr 91:841-847.
5. Arts ICW, Venema DP, and Hollman PCH (2003) Quantitative determination of flavonols in plant foods and biological fluids, in Methods in Polyphenol Analysis (Santos-Buelga C and Williamson G eds) pp 214-228, The Royal Society of Chemistry, Cambridge, UK.
6. Artursson P and Karlsson J (1991) Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells. Biochem Biophys Res Commun 175:880-885.
7. Chen ZS, Robey RW, Belinsky MG, Shchaveleva I, Ren XQ, Sugimoto Y, Ross DD, Bates SE, and Kruh GD (2003) Transport of methotrexate, methotrexate polyglutamates and 17beta-estradiol 17-(beta-D-glucuronide) by ABCG2: effects of acquired mutations at R482 on methotrexate transport. Cancer Res 63:4048-4054.
8. Crespy V, Morand C, Besson C, Cotelle N, Vezin H, Demigne C, and Remesy C (2003) The splanchnic metabolism of flavonoids highly differed according to the nature of the compound. Am J Physiol 284:G980-G988.
9. Crespy V, Morand C, Manach C, Besson C, Demigne C, and Remesy C (1999) Part of quercetin absorbed in the small intestine is conjugated and further secreted in the intestinal lumen. Am J Physiol 277:G120-G126.
10. Day AJ, Gee JM, DuPont MS, Johnson IT, and Williamson G (2003) Absorption of quercetin-3-glucoside and quercetin-4′-glucoside in the rat small intestine: the role of lactase phlorizin hydrolase and the sodium-dependent glucose transporter. Biochem Pharmacol 65:1199-1206.
11. de Vries MH, Redegeld FA, Koster AS, Noordhoek J, de Haan JG, Oude Elferink RP, and Jansen PL (1989) Hepatic, intestinal and renal transport of 1-naphthol-beta-D-glucuronide in mutant rats with hereditary-conjugated hyperbilirubinemia. Naunyn-Schmiedeberg's Arch Pharmacol 340:588-592.
12. Dietrich CG, Geier A, and Oude Elferink RP (2003) ABC of oral bioavailability: transporters as gatekeepers in the gut. Gut 52:1788-1795.
13. Evers R, Kool M, van Deemter L, Janssen H, Calafat J, Oomen LC, Paulusma CC, Oude Elferink RP, Baas F, Schinkel AH, et al. (1998) Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J Clin Investig 101:1310-1319.
14. Hsiu SL, Hou YC, Wang YH, Tsao CW, Su SF, and Chao PD (2002) Quercetin significantly decreased cyclosporin oral bioavailability in pigs and rats. Life Sci 72:227-235.
15. Imai Y, Tsukahara S, Asada S, and Sugimoto Y (2004) Phytoestrogens/ flavonoids reverse breast cancer resistance protein/ABCG2-mediated multidrug resistance. Cancer Res 64:4346-4352.
16. Jager W, Gehring E, Hagenauer B, Aust S, Senderowicz A, and Thalhammer T (2003) Biliary excretion of flavopiridol and its glucuronides in the isolated perfused rat liver: role of multidrug resistance protein 2 (Mrp2). Life Sci 73:2841-2854.
17. Jia X, Chen J, Lin H, and Hu M (2004) Disposition of flavonoids via enteric recycling: enzyme-transporter coupling affects metabolism of biochanin A and formononetin and excretion of their phase II conjugates. J Pharmacol Exp Ther 310:1103-1113.
18. Jonker JW, Smit JW, Brinkhuis RF, Maliepaard M, Beijnen JH, Schellens JH, and Schinkel AH (2000) Role of breast cancer resistance protein in the bioavailability and fetal penetration of topotecan. J Natl Cancer Inst 92:1651-1656.
19. Law MR and Morris JK (1998) By how much does fruit and vegetable consumption reduce the risk of ischaemic heart disease? Eur J Clin Nutr 52:549-556.
20. Maliepaard M, Scheffer GL, Faneyte IF, van Gastelen MA, Pijnenborg AC, Schinkel AH, van De Vijver MJ, Scheper RJ, and Schellens JH (2001) Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res 61:3458-3464.
21. Manach C, Texier O, Regerat F, Agullo G, Demigne C, and Remesy C (1996) Dietary quercetin is recovered in rat plasma as conjugated derivatives of isorhamnetin and quercetin. J Nutr Biochem 7:375-380.
22. Middleton E Jr, Kandaswami C, and Theoharides TC (2000) The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease and cancer. Pharmacol Rev 52:673-751.
23. Nakatomi K, Yoshikawa M, Oka M, Ikegami Y, Hayasaka S, Sano K, Shiozawa K, Kawabata S, Soda H, Ishikawa T, et al. (2001) Transport of 7-ethyl-10-hydroxycamptothecin (SN-38) by breast cancer resistance protein ABCG2 in human lung cancer cells. Biochem Biophys Res Commun 288:827-832.
24. O'Leary KA, Day AJ, Needs PW, Mellon FA, O'Brien NM, and Williamson G (2003) Metabolism of quercetin-7- and quercetin-3-glucuronides by an in vitro hepatic model: the role of human beta-glucuronidase, sulfotransferase, catechol-O-methyltransferase and multi-resistant protein 2 (MRP2) in flavonoid metabolism. Biochem Pharmacol 65:479-491.
25. Rabindran SK, He H, Singh M, Brown E, Collins KI, Annable T, and Greenberger LM (1998) Reversal of a novel multidrug resistance mechanism in human colon carcinoma cells by fumitremorgin C. Cancer Res 58:5850-5858.
26. Scalbert A and Williamson G (2000) Dietary intake and bioavailability of polyphenols. J Nutr 130:2073S-2085S.
27. Sesink ALA, Arts ICW, Faassen-Peters M, and Hollman PCH (2003) Intestinal uptake of quercetin-3-glucoside in rats involves hydrolysis by lactase phlorizin hydrolase. J Nutr 133:773-776.
28. Sparreboom A, Danesi R, Ando Y, Chan J, and Figg WD (2003) Pharmacogenomics of ABC transporters and its role in cancer chemotherapy. Drug Resist Updat 6:71-84.
29. Vaidyanathan JB and Walle T (2001) Transport and metabolism of the tea flavonoid (-)-epicatechin by the human intestinal cell line Caco-2. Pharm Res 18:1420-1425.
30. Vaidyanathan JB and Walle T (2003) Cellular uptake and efflux of the tea flavonoid (-)-epicatechin-3-gallate in the human intestinal cell line Caco-2. J Pharmacol Exp Ther 307:745-752.
31. van der Kolk DM, Vellenga E, Scheffer GL, Muller M, Bates SE, Scheper RJ, and de Vries EG (2002) Expression and activity of breast cancer resistance protein (BCRP) in de novo and relapsed acute myeloid leukemia. Blood 99:3763-3770.
32. 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.
33. van't Veer P, Jansen MC, Klerk M and Kok FJ (2000) Fruits and vegetables in the prevention of cancer and cardiovascular disease. Public Health Nutr 3:103-107.
34. Walgren RA, Karnaky KJ Jr, Lindenmayer GE, and Walle T (2000) Efflux of dietary flavonoid quercetin 4′-β-glucoside across human intestinal Caco-2 cell monolayers by apical multidrug resistance-associated protein-2. J Pharmacol Exp Ther 294:830-836.
35. Walle T, Otake Y, Walle UK, and Wilson FA (2000) Quercetin glucosides are completely hydrolyzed in ileostomy patients before absorption. J Nutr 130:2658-2661.
36. Walle T and Walle UK (2003) The β-D-Glucoside and sodium-dependent glucose transporter 1 (SGLT1)-inhibitor phloridzin is transported by both SGLT1 and multidrug resistance-associated proteins 1/2. Drug Metab Dispos 31:1288-1291.
37. Yoshikawa M, Ikegami Y, Sano K, Yoshida H, Mitomo H, Sawada S, and Ishikawa T (2004) Transport of SN-38 by the wild type of human ABC transporter ABCG2 and its inhibition by quercetin, a natural flavonoid. J Exp Ther Oncol 4:25-35.
38. Youdim KA, Qaiser MZ, Begley DJ, Rice-Evans CA, and Abbott NJ (2004) Flavonoid permeability across an in situ model of the blood-brain barrier. Free Radic Biol Med 36:592-604.
39. Zelcer N, Huisman MT, Reid G, Wielinga P, Breedveld P, Kuil A, Knipscheer P, Schellens JH, Schinkel AH, and Borst P (2003) Evidence for two interacting ligand binding sites in human multidrug resistance protein 2 (ATP binding cassette C2). J Biol Chem 278:23538-23544.
40. Zhang S, Yang X, and Morris ME (2004) Flavonoids are inhibitors of breast cancer resistance protein (ABCG2)-mediated transport. Mol Pharmacol 65:1208-1216.