An in vitro and in silico study on the flavonoid-mediated modulation of the transport of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) through Caco-2 monolayers

Toxicology and Applied Pharmacology

Volumn 217, Issue 2, 2006, Pages 204-215

  Schutte, Maaike E ^a   Freidig, Andreas P ^b   van de Sandt, Johannes J M ^b   Alink, Gerrit M ^a   Rietjens, Ivonne M C M ^a,b   Groten, John P ^b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b TNO   (Netherlands)

Author keywords

ABC transporter; Caco 2; Flavonoid; Heterocyclic amine; In silico

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; BREAST CANCER RESISTANCE PROTEIN; CHRYSOERIOL; ELACRIDAR; FLAVONE; FLAVONOID; KAEMPFEROL; LUTEOLIN; MORIN; MULTIDRUG RESISTANCE PROTEIN; MYRICETIN; NARINGENIN; QUERCETIN; ROBINETIN; TAXIFOLIN; UNCLASSIFIED DRUG; VERLUKAST;

ABSORPTION; APICAL MEMBRANE; ARTICLE; CELL STRAIN CACO 2; COMPUTER MODEL; CONTROLLED STUDY; DRUG EFFECT; HUMAN; HUMAN CELL;

ACRIDINES; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT, ACTIVE; CACO-2 CELLS; CARCINOGENS; CELL MEMBRANE PERMEABILITY; DIFFUSION; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVANONES; FLAVONOIDS; HUMANS; IMIDAZOLES; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; KINETICS; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; P-GLYCOPROTEIN; PROPIONATES; QUINOLINES; REPRODUCIBILITY OF RESULTS; TETRAHYDROISOQUINOLINES;

EID: 33750683906     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2006.08.005     Document Type: Article

References (40)

1. Arts I.C.W., and Hollman P.C.H. Polyphenols and disease risk in epidemiologic studies. Am. J. Clin. Nutr. 81 (2005) 317S-325S
2. Artursson P., and Karlsson J. Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells. Biochem. Biophys. Res. Commun. 175 (1991) 880-885
3. Crofts F.G., Sutter T.R., and Strickland P.T. Metabolism of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine by human cytochrome P4501A1, P4501A2 and P4501B1. Carcinogenesis 19 (1998) 1969-1973
4. de Bruin M., Miyake K., Litman T., Robey R., and Bates S.E. Reversal of resistance by GF120918 in cell lines expressing the ABC half-transporter, MXR. Cancer Lett. 146 (1999) 117-126
5. Dietrich C.G., de Waart D.R., Ottenhoff R., Schoots I.G., and Elferink R.P.J. Increased bioavailability of the food-derived carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine in MRP2-deficient rats. Mol. Pharmacol. 59 (2001) 974-980
6. Di Pietro A., Conseil G., Perez-Victoria J.M., Dayan G., Baubichon-Cortay H., Trompier D., Steinfels E., Jault J.M., de Wet H., Maitrejean M., Comte G., Boumendjel A., Mariotte A.M., Dumontet C., McIntosh D.B., Goffeau A., Castanys S., Gamarro F., and Barron D. Modulation by flavonoids of cell multidrug resistance mediated by P-glycoprotein and related ABC transporters. Cell. Mol. Life Sci. 59 (2002) 307-322
7. Duizer E., Penninks A.H., Stenhuis W.H., and Groten J.P. Comparison of permeability characteristics of the human colonic Caco-2 and rat small intestinal IEC-18 cell lines. J. Control. Releases 49 (1997) 39-49
8. Duizer E., van der Wulp C., Versantvoort C.H.M., and Groten J.P. Absorption enhancement, structural changes in tight junctions and cytotoxicity caused by palmitoyl carnitine in Caco-2 and IEC-18 cells. J. Pharmacol. Exp. Ther. 287 (1998) 395-402
9. Duizer E., Gilde A.J., Versantvoort C.H.M., and Groten J.P. Effects of cadmium chloride on the paracellular barrier function of intestinal epithelial cell lines. Toxicol. Appl. Pharmacol. 155 (1999) 117-126
10. Ebert B., Seidel A., and Lampen A. Identification of BCRP as transporter of benzo(a)pyrene conjugates metabolically formed in Caco-2 cells and its induction by Ah-receptor agonists. Carcinogenesis 26 (2005) 1754-1763
11. Felton J.S., Knize M.G., Shen N.H., Lewis P.R., resen B.D., Happe J., and Hatch F.T. The isolation and identification of a new mutagen from fried ground beef: 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis 7 (1986) 1081-1086
12. Gao J., Murase O., Schowen R.L., Aube J., and Borchardt R.T. A functional assay for quantitation of the apparent affinities of ligands of P-glycoprotein in Caco-2 cells. Pharm. Res. 18 (2001) 171-176
13. Gekeler V., Ise W., Sanders K.H., Ulrich W.R., and Beck J. The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem. Biophys. Res. Commun. 208 (1995) 345-352
14. Hooijberg J.H., Broxterman H.J., Heijn M., Fles D.L.A., Lankelma J., and Pinedo H.M. Modulation by (iso)flavonoids of the ATPase activity of the multidrug resistance protein. FEBS Lett. 413 (1997) 344-348
15. Imai Y., Tsukahara S., Asada S., and Sugimoto Y. Phytoestrogens/flavonoids reverse breast cancer resistance protein/ABCG2-mediated multidrug resistance. Cancer Res. 64 (2004) 4346-4352
16. Jagerstad M., Reutersward A.L., Olsson R., Grivas S., Nyhammar T., Olsson K., and Dahlqvist A. Creatin(in)e and Maillard reaction products as precursors of mutagenic compounds: effects of various amino acids. Food Chem. 12 (1983) 255
17. Leslie E.M., Mao Q., Oleschuk C.J., Deeley R.G., and Cole S.P. Modulation of multidrug resistance protein 1 (MRP1/ABCC1) transport and ATPase activities by interaction with dietary flavonoids. Mol. Pharmacol. 59 (2001) 1171-1180
18. Mitchell D.B., Santone K.S., and Acosta D. Evaluation of cytotoxicity in cultured cells by enzyme leakage. J. Tissue Cult. Methods 6 (1980) 113-116
19. Morris M.E., and Zhang S. Flavonoid-drug interactions: effects of flavonoids on ABC transporters. Life Sci. 78 (2006) 2116-2130
20. Nakamura T., Sakaeda T., Ohmoto N., Tamura T., Aoyama N., Shirakawa T., Kamigaki T., Kim K.I., Kim S.R., Kuroda Y., Matsuo M., Kasuga M., and Okumura K. Real-time quantitative polymerase chain reaction for MDR1, MRP1, MRP2, CYP3A-mRNA levels in Caco-2 cell lines, human duodenal enterocytes, normal colorectal tissues, colorectal adenocarcinomas. Drug Metab. Dispos. 30 (2002) 4-6
21. Nguyen H., Zhang S., and Morris M.E. Effect of flavonoids on MRP1-mediated transport in Panc-1 cells. J. Pharm. Sci. 92 (2003) 250-257
22. Petri N., Tannergren C., Rungstad D., and Lennernäs H. Transport characteristics of fexofenadine in the Caco-2 cell model. Pharm. Res. 21 (2004) 1398-1404
23. Romiti N., Tramonti G., Donati A., and Chieli E. Effects of grapefruit juice on the multidrug transporter P-glycoprotein in the human proximal tubular cell line HK-2. Life Sci. 76 (2004) 293-302
24. Schutte M.E., van de Sandt J.J.M., Alink G.M., Groten J.P., and Rietjens I.M.C.M. Myricetin stimulates the absorption of the pro-carcinogen PhIP. Cancer Lett. 231 (2006) 36-42
25. Sesink A.L.A., Arts I.C.W., de Boer V.C.J., Breedveld P., Schellens J.H.M., Hollman P.C.H., and Russel F.G.M. Breast cancer resistance protein (Bcrp1/Abcg2) limits net intestinal uptake of quercetin in rats by facilitating apical efflux of glucuronides. Mol. Pharmacol. 67 (2005) 1999-2006
26. Taipalensuu J., Tornblom H., Lindberg G., Einarsson C., Sjoqvist F., Melhus H., Garberg P., Sjostrom B., Lundgren B., and Artursson P. Correlation of gene expression of ten drug efflux proteins of the ATP-binding cassette transporter family in normal human jejunum and in human intestinal epithelial Caco-2 cell monolayers. J. Pharmacol. Exp. Ther. 299 (2001) 164-170
27. Turesky R.J., Lang N.P., Butler M.A., Teitel C.H., and Kadlubar F.F. Metabolic activation of carcinogenic heterocyclic aromatic amines by human liver and colon. Carcinogenesis 12 (1991) 1839-1845
28. van Herwaarden A.E., Jonker J.W., Wagenaar E., Brinkhuis R.F., Schellens J.H.M., Beijnen J.H., and Schinkel A.H. 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 (2003) 6447-6452
29. van Zanden J.J., Wortelboer H.M., Bijlsma S., Punt A., Usta M., Bladeren P.J., Rietjens I.M.C.M., and Cnubben N.H.P. Quantitative structure activity relationship studies on the flavonoid mediated inhibition of multidrug resistance proteins 1 and 2. Biochem. Pharmacol. 69 (2005) 699-708
30. Vlaming M.L.H., Mohrmann K., Wagenaar E., de Waart D.R., Oude Elferink R.P.J., Lagas J.S., van Tellingen O., Vainchtein L.D., Rosing H., Beijnen J.H., Schellens J.H.M., and Schinkel A.H. Carcinogen and anti-cancer drug transport by Mrp2 in vivo: studies using Mrp2 (Abcc2)knockout mice. J. Pharmacol. Exp. Ther. (2006)
31. Walgren R.A., Walle U.K., and Walle T. Transport of quercetin and its glucosides across human intestinal epithelial Caco-2 cells. Biochem. Pharmacol. 55 (1998) 1721-1727
32. Walgren R.A., Karnaky Jr. K.J., Lindenmayer G.E., and Walle T. Efflux of dietary flavonoid quercetin 4′-beta-glucoside across human intestinal Caco-2 cell monolayers by apical multidrug resistance-associated protein-2. J. Pharmacol. Exp. Ther. 294 (2000) 830-836
33. Walle U.K., Galijatovic A., and Walle T. Transport of the flavonoid chrysin and its conjugated metabolites by the human intestinal cell line Caco-2. Biochem. Pharmacol. 58 (1999) 431-438
34. Wu C.-P., Calcagno A.M., Hladky S.B., Ambudkar S.V., and Barrand M.A. Modulatory effects of plant phenols on human multidrug-resistance proteins 1, 4 and 5 (ABCC1, 4 and 5). FEBS J. 272 (2005) 4725-4740
35. Xia C.Q., Liu N., Yang D., Miwa G., and Gan L.-S. Expression, localization, functional characteristics of breast cancer resistance protein in Caco-2 cells. Drug Metab. Dispos. 33 (2005) 637-643
36. Zhang S., and Morris M.E. Effect of the flavonoids biochanin A and silymarin on the P-glycoprotein-mediated transport of digoxin and vinblastine in human intestinal Caco-2 cells. Pharm. Res. 20 (2003) 1184-1191
37. Zhang S., and Morris M.E. Effects of the flavonoids biochanin A, morin, phloretin, silymarin on P-glycoprotein-mediated transport. J. Pharmacol. Exp. Ther. 304 (2003) 1258-1267
38. Zhang S., Yang X., and Morris M.E. Flavonoids are inhibitors of breast cancer resistance protein (ABCG2)-mediated transport. Mol. Pharmacol. 65 (2004) 1208-1216
39. Zhang S., Yang X., Coburn R.A., and Morris M.E. Structure activity relationships and quantitative structure activity relationships for the flavonoid-mediated inhibition of breast cancer resistance protein. Biochem. Pharmacol. 70 (2005) 627-639
40. Zimmermann C., Gutmann H., Hruz P., Gutzwiller J.P., Beglinger C., and Drewe J. Mapping of multidrug resistance gene 1 and multidrug resistance-associated protein isoform 1 to 5 mRNA expression along the human intestinal tract. Drug Metab. Dispos. 33 (2005) 219-224