Effects of diosmin, a flavonoid glycoside in citrus fruits, on P-glycoprotein-mediated drug efflux in human intestinal caco-2 cells

Journal of Agricultural and Food Chemistry

Volumn 55, Issue 18, 2007, Pages 7620-7625

  Hye, Hyun Yoo ^a   Lee, Mijin ^a   Hye, Jin Chung ^a   Sang, Kyu Lee ^a   Kim, Dong Hyun ^a  

^a Korea Institute of Science and Technology   (South Korea)

Author keywords

Caco 2 cells; Citrus fruit; Diosmin; Flavonoid; P glycoprotein

Indexed keywords

DIGOXIN; DIOSMIN; GLYCOPROTEIN P; RHODAMINE 123;

ARTICLE; CELL STRAIN CACO 2; CHEMISTRY; CITRUS FRUIT; DRUG EFFECT; FRUIT; HUMAN; INTESTINE; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CACO-2 CELLS; CITRUS; DIGOXIN; DIOSMIN; FRUIT; HUMANS; INTESTINES; P-GLYCOPROTEIN; RHODAMINE 123;

CITRUS;

EID: 34848835701     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf070893f     Document Type: Article

References (40)

1. Lown, K. S.; Bailey, D. G.; Fontana, R. J.; Janardan, S. K.; Adair, C. H.; Forflage, L. A.; Brown, M. B.; Guo, W.; Watkins, P. B. Grapefruit juice increases felodipine oral availability in humans by decreasing intestinal CYP3A protein expression. J. Clin. Invest. 1997, 99, 2545-2553.
2. Hashimoto, K.; Shirafuji, T.; Sekino, H.; Matsuoka, O.; Sekino, H.; Onnagawa, O.; Okamoto, T.; Kudo, S.; Azuma, J. Interaction of citrus juices with pranidipine, a new 1,4-dihydropyridine calcium antagonist, in healthy subjects. Eur. J. Clin. Pharmacol. 1998, 54, 753-760.
3. Rau, S. E.; Bend, J. R.; Arnold, J. M. O.; Tran, L. T.; Spence, J. D.; Bailey, D. G. Grapefruit juice-terfenadine single-dose interaction: Magnitude, mechanism, and relevance. Clin. Pharmacol. Ther. 1997, 61, 401-409.
4. Kupferschmidt, H. H. T.; Fattinger, K. E.; Ha, H. R.; Follath, F.; Krahenbuhl, S. Grapefruit juice enhances the bioavailability of the HIV protease inhibitor saquinavir in man. Br. J. Clin. Pharmacol. 1998, 45, 355-359.
5. Ku, Y. M.; Min, D. I.; Flanigan, M. Effects of grapefruit juice on the pharmacokinetics of microemulsion cyclosporine and its metabolite in healthy volunteers: Does the formulation difference matter? J. Clin. Pharmacol. 1998, 38, 959-965.
6. Kupferschmidt, H. H. T.; Ha, H. R.; Ziegler, W. H.; Meier, P. J.; Krahenbuhl, S. Interaction between grapefruit juice and midazolam in humans. Clin. Pharmacol. Ther. 1995, 58, 20-28.
7. Schmiedlin-Ren, P.; Edward, D. J.; Fitzsimmons, M. E.; He, K.; Lown, K. S.; Woster, P. M.; Rahman, A.; Thummel, K. E.; Fisher, J. M.; Hollenberg, P. F.; Watkins, P. B. Mechanisms of enhanced oral availability of CYP3A4 substrates by grapefruit constituents. Decreased enterocyte CYP3A4 concentration and mechanism-based inactivation by furanocoumarins. Drug Metab. Dispos. 1991, 25, 1228-1233.
8. Bailey, D. G.; Spence, J. D.; Munoz, C.; Arnold, J. M. Interaction of citrus juices with felodipine and nifedipine. Lancet 1991, 337, 268-269.
9. Takanaga, H.; Ohnishi, A.; Yamada, S.; Matsuo, H.; Morimoto, S.; Shoyama, Y.; Ohtani, H.; Sawada, Y. Polymethoxylated flavones in orange juice are inhibitors of P-glycoprotein but not cytochrome P450 3A4. J. Pharmacol. Exp. Ther. 2000, 293, 230-236.
10. Tian, R.; Koyabu, N.; Takanaga, H.; Matsuo, H.; Ohtani, H.; Sawada, Y. Effects of grapefruit juice and orange juice on the intestinal efflux of P-glycoprotein substrates. Pharm. Res. 2002, 19, 802-809.
11. Romiti, N.; Tramonti, G.; Donati, A.; Chieli, E. Effects of grapefruit juice on the multidrug transporter P-glycoprotein in the human proximal tubular cell line HK-2. Life Sci. 2004, 76, 293-302.
12. Mertens-Talcott, S. U.; De Castro, W. V.; Manthey, J. A.; Derendorf, H.; Butterweck, V. Polymethoxylated Flavones and Other Phenolic Derivates from Citrus in Their Inhibitory Effects on P-Glycoprotein-Mediated Transport of Talinolol in Caco-2 Cells. J. Agric. Food Chem. 2007, 55, 2563-2568.
13. Lim, S.-L.; Lim, L.-Y. Effects of citrus fruit juices on cytotoxicity and drug transport pathways of Caco-2 cell monolayers. Int. J. Pharm. 2006, 307, 42-50.
14. Honda, Y.; Ushigome, F.; Koyabu, N.; Morimoto, S.; Shoyama, Y.; Uchiumi, T.; Kuwano, M.; Ohtani, H.; Sawada, Y. Effects of grapefruit juice and orange juice components on P-glycoprotein- and MRP2-mediated drug efflux. Br. J. Pharmacol. 2004, 143, 856-864.
15. Deferme, S.; Van Gelder, J.; Augustijns, P. Inhibitory effect of fruit extracts on P-glycoprotein-related efflux carriers: an invitro screening. J Pharm. Pharmacol. 2002, 54, 1213-1219.
16. Herrmann, K. On the occurrence of flavonol and flavone glycosides in vegetables. Z. Lebensm.-Unters. Forsch. 1988, 186, 1-5.
17. Kanes, K.; Tisserat, B.; Berhow, M.; Vandercook, C. Phenolic composition of various tissues of Rutaceae species. Phytochemistry 1993, 32, 967-974.
18. Buening, M. K.; Chang, R. L.; Huang, M. T.; Fortner, J. G.; Wood, A. W.; Conney, A. H. Activation and inhibition of benzo-(a)pyrene and aflatoxin B1 metabolism in human liver microsomes by naturally occurring flavonoids. Cancer Res. 1981, 41, 67-72.
19. Siess, M. H.; Le Bon, A. M.; Suschetet, M. Dietary modification of drug-metabolizing enzyme activities: dose-response effect of flavonoids. J. Toxicol. Environ. Health. 1992, 35, 141-152.
20. Guengerich, F. P.; Kim, D. H. In vitro inhibition of dihydropyridine oxidation and aflatoxin B1 activation in human liver microsomes by naringenin and other flavonoids. Carcinogenesis 1990, 11, 2275-2279.
21. Middleton, E.; Kandaswami, C. Effects of flavonoids on immune and inflammatory cell functions. Biochem. Pharmacol. 1992, 43, 1167-1179.
22. Mukhtar, H.; Das, M.; Khan, W. A.; Wang, Z. Y.; Bik, D. P.; Bickers, D. R. Exceptional activity of tannic acid among naturally occurring plant phenols in protecting against 7,12-dimethylbenz-(a)anthracene-, benzo(a)pyrene-, 3-methylcholanthrene-, and N-methyl-N-nitrosourea-induced skin tumorigenesis in mice. Cancer Res. 1988, 48, 2361-2365.
23. Verma, A. K.; Johnson, J. A.; Gould, M. N.; Tanner, M. A. Inhibition of 7,12-dimethylbenz(a)anthracene- and N-nitrosom-ethylurea-induced rat mammary cancer by dietary flavonol quercetin. Cancer Res. 1988, 48, 5754-5758.
24. Mitsunaga, Y.; Takanaga, H.; Matsuo, H.; Naito, M.; Tsuruo, T.; Ohtani, H.; Sawada, Y. Effect of bioflavonoids on vincristine transport across blood-brain barrier. Eur. J. Pharmacol. 2000, 395, 193-201.
25. Balimane, P. V.; Patel, K.; Marino, A.; Chong, S. Utility of 96 well Caco-2 cell system for increased throughput of P-gp screening in drug discovery. Eur. J. Pharm. Biopharm. 2004, 58, 99-105.
26. Yamashita, S.; Konishi, K.; Yamazaki, Y.; Taki, Y.; Sakane, T.; Sezaki, H.; Furuyama, Y. New and better protocols for a short-term Caco-2 cell culture system. J. Pharm. Sci. 2002, 91, 669-679.
27. Greiner, B.; Eichelbaum, M.; Fritz, P.; Kreichgauer, H. P.; von Richter, O.; Zundler, J.; Kroemer, H. K. The role of intestinal P-glycoprotein in the interaction of digoxin and rifampin. J. Clin. Invest. 1999, 104, 147-153.
28. Laska, D. A.; Houchins, J. O.; Pratt, S. E.; Horn, J.; Xia, X.; Hanssen, B. R.; Williams, D. C.; Dantzig, A. H.; Lindstrom, T. Characterization and application of a vinblastine-selected Caco-2 line for evaluation of p-glycoprotein. In Vitro Cell. Dev. Biol. Anim. 2002, 38, 401-410.
29. Hansen, M. B.; Nielsen, S. E.; Berg, K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods 1989, 119, 203-210.
30. Cypriani, B.; Limasset, B.; Carrie, M. L.; Le, Doucen, C.; Roussie, M.; de Paulet, A. C.; Damon, M. Antioxidant activity of micronized diosmin on oxygen species from stimulated human neutrophils. Biochem. Pharmacol. 1993, 45, 1531-1535.
31. Tanaka, T.; Makita, H.; Kawabata, K.; Mori, H.; Kakumoto, M.; Satoh, K.; Hara, A.; Sumida, T.; Tanaka, T.; Ogawa, H. Chemoprevention of azoxymethane-induced rat colon carcinogenesis by the naturally occurring flavonoids, diosmin and hesperidin. Carcinogenesis 1997, 18, 957-965.
32. Jantet, G. Chronic venous insufficiency: worldwide results of the RELIEF study. Reflux assessment and quality of life improvement with micronized flavonoids. Angiology 2002, 53, 245-256.
33. Buckshee, K.; Takkar, D.; Aggarwal, N. Micronized flavonoid therapy in internal hemorrhoids of pregnancy. Int. J. Gynaecol. Obstet. 1997, 57, 145-151.
34. Tsimoyiannis, E. C.; Floras, G.; Antoniou, N.; Papanikolaou, N.; Siakas, P.; Tassis, A. Low-molecular-weight heparins and daflon for prevention of postoperative thromboembolism. World J. Surg. 1996, 20, 968-972.
35. Kanaze, F. I.; Gabrieli, C.; Kokkalou, E.; Georgarakis, M.; Niopas, I. Simultaneous reversed-phase high-performance liquid chromatographic method for the determination of diosmin, hesperidin and naringin in different citrus fruit juices and pharmaceutical formulations. J. Pharm. Biomed. Anal. 2003, 33, 243-249.
36. Rajnarayana, K.; Reddy, M. S.; Krishna, D. R. Diosmin pretreatment affects bioavailability of metronidazole. Eur. J. Clin. Pharmacol. 2003, 58, 803-807.
37. Critchfield, J. W.; Welsh, C. J.; Phang, J. M.; Yeh, G. C. Modulation of adriamycin accumulation and efflux by flavonoids in HCT- 15 colon cells. Activation of P-glycoprotein as a putative mechanism. Biochem. Pharmacol. 1994, 48, 1437-1445.
38. Scambia, G.; Ranelletti, F. O.; Panici, P. B.; De Vincenzo, R.; Bonanno, G.; Ferrandina, G.; Piantelli, M.; Bussa, S.; Rumi, C.; Cianfriglia, M.; Mancuso, S. Quercetin potentiates the effect of adriamycin in a multidrug-resistant MCF-7 human breast-cancer cell line: P-glycoprotein as a possible target. Cancer Chemother. Pharmacol. 1994, 34, 459-464.
39. Zhang, S; 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. 2003, 20, 1184-1191.
40. Conseil, G.; Baubichon-Cortay, H.; Dayan, G.; Jault, J.-M.; Barron, D.; Di Pietro, A. Flavonids: a class of modulators with bifunctional interactions at vicinal ATP- and steroid-binding sites on mouse P-glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 9831-9836.