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

Biochemical Pharmacology

Volumn 65, Issue 7, 2003, Pages 1199-1206

  Day, Andrea J ^a   Gee, Jennifer M ^b   DuPont, M Susan ^b   Johnson, Ian T ^b   Williamson, Gary ^b,c  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b NORWICH RESEARCH PARK   (United Kingdom)

^c NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

Deglycosylation; Flavonoid; Intestinal absorption; Lactase phlorizin hydrolase (LPH); Quercetin glucoside; Sodium dependent glucose transporter 1 (SGLT1)

Indexed keywords

CARBOHYDRATE DERIVATIVE; DRUG METABOLITE; GLUCOSE TRANSPORTER; GLYCOSYLCERAMIDASE; ISOQUERCITRIN; LACTASE; N (N BUTYL)DEOXYGALACTONOJIRIMYCIN; PHLORIZIN; QUERCETIN 4' GLUCOSIDE; QUERCETIN DERIVATIVE; SODIUM; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ABSORPTION; DRUG TISSUE LEVEL; HYDROLYSIS; INCUBATION TIME; JEJUNUM; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SEROSA; SMALL INTESTINE ABSORPTION;

EID: 0037377562     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(03)00039-X     Document Type: Article

References (36)

1. Day A.J., DuPont M.S., Ridley S., Rhodes M., Rhodes M.J.C., Morgan M.R.A., Williamson G. Deglycosylation of flavonoid and isoflavonoid glycosides by human small intestine and liver β-glucosidase activity. FEBS Lett. 436:1998;71-75.
2. Day A.J., Cañada F.J., Díaz J.C., Kroon P.A., Mclauchlan R., Faulds C.B., Plumb G.W., Morgan M.R.A., Williamson G. Dietary flavonoid and isoflavone glycosides are hydrolysed by the lactase site of lactase phlorizin hydrolase. FEBS Lett. 468:2000;166-170.
3. Ioku K., Pongpiriyadacha Y., Konishi Y., Takei Y., Nakatani N., Terao J. β-Glucosidase activity in the rat small intestine towards quercetin monogucosides. Biosci. Biotech. Biochem. 62:1998;1428-1431.
4. Day A.J., Mellon F., Barron D., Sarrazin G., Morgan M.R.A., Williamson G. Human metabolism of dietary flavonoids: identification of plasma metabolites of quercetin. Free Radic. Res. 35:2001;941-952.
5. Graefe E.U., Wittig J., Mueller S., Riethling A.K., Uehleke B., Drewelow B., Pforte H., Jacobasch G., Derendorf H., Veit M. Pharmacokinetics and bioavailability of quercetin glycosides in humans. J. Clin. Pharmacol. 41:2001;492-499.
6. Sesink A.L.A., O'Leary K.A., Hollman P.C.H. Quercetin glucuronides but not glucosides are present in human plasma after consumption of quercetin-3-glucoside or quercetin-4′-glucoside. J. Nutr. 131:2001;1938-1941.
7. Walle T., Otake Y., Walle K., Wilson F.A. Quercetin glucosides are completely hydrolyzed in ileostomy patients before absorption. J. Nutr. 130:2001;2658-2661.
8. Hollman P.C.H., Buysman M.N.C.P., van Gameren Y., Cnossen E.P.J., deVries J.H.M., Katan M.B. The sugar moiety is a major determinant of the absorption of dietary flavonoid glycosides in man. Free Radic. Res. 31:1999;569-573.
9. Gee J.M., DuPont M.S., Rhodes M.J.C., Johnson I.T. Quercetin glucosides interact with the intestinal glucose transport pathway. Free Radic. Biol. Med. 25:1998;19-25.
10. Gee J.M., DuPont M.S., Day A.J., Plumb G.W., Williamson G., Johnson I.T. Intestinal transport of quercetin glycosides in the rat involves both deglycosylation and interaction with the hexose transport pathway. J. Nutr. 130:2000;2765-2771.
11. Walgren R.A., Walle U.K., Walle T. Transport of quercetin and its glucosides across human intestinal epithelial Caco-2 cells. Biochem. Pharmacol. 55:1998;1721-1727.
12. Murota K., Shimizu S., Chujo H., Moon J.H., Terao J. Efficiency of absorption and metabolic conversion of quercetin and its glucosides in human intestinal cell line Caco-2. Arch. Biochem. Biophys. 384:2000;391-397.
13. Kuo S.M. Transepithelial transport and accumulation of flavone in human intestinal Caco-2 cells. Life Sci. 63:1998;2323-2331.
14. Walgren R.A., Karnaky K.J., Lindenmayer G.E., Walle T. Efflux of dietary flavonoid quercetin-4′-beta-glucoside across human intestinal Caco-2 cell monolayers by apical multi-drug resistance-associated protein-2. J. Pharmacol. Exp. Ther. 294:2000;830-836.
15. Walgren R.A., Lin J.T., Kinne R.K.H., Walle T. Cellular uptake of dietary flavonoid quercetin-4′-β-glucoside by the sodium-dependent glucose transporter, SGLT1. J. Pharmacol. Exp. Ther. 294:2000;837-843.
16. Chantret I., Rodolosse A., Barbat A., Dussaulx E., Brotlaroche E., Zweibaum A., Rousset M. Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell-line Caco-2 - evidence for glucose-dependent negative regulation. J. Cell Sci. 107:1994;213-225.
17. Herrmann K. Flavonols and flavones in food plant: a review. J. Food Tech. 11:1976;433-438.
18. Price K.R., Colquhoun I.J., Barnes K.A., Rhodes M.J.C. The composition and content of flavonol glycosides in green beans and their fate during processing. J. Food Chem. 46:1998;4898-4903.
19. Day A.J., Bao Y.-P., Morgan M.R.A., Williamson G. Conjugation position of quercetin glucuronides and effect on biological activity. Free Radic. Biol. Med. 29:2000;1234-1243.
20. Andersson U., Butters T.D., Dwek R.A., Platt F.M. N-Butyldeoxygalactonojirimycin: a more selective inhibitor of glycosphingolipid biosynthesis than N-butyldeoxynojirimycin. Biochem. Pharmacol. 59:2000;821-829.
21. Andlauer W., Kolb J., Stehle P., Furst P. Absorption and metabolism of genistein in isolated rat small intestine. J. Nutr. 130:2000;843-846.
22. Daniels L.B., Coyle P.J., Chiao Y.B., Glew R.H. Purification and characterization of a cytosolic broad specificity beta-glucosidase from human liver. J. Biol. Chem. 256:1981;13004-13013.
23. Wacker H., Keller P., Falchetto R., Legler G., Semenza G., Raul F., Freund J.N. Location of the two catayltic sites in intestinal lactase phlorizin hydrolase. J. Biol. Chem. 267:1992;18744-18752.
24. DuPont M.S., Mondin Z., Williamson G., Price K.R. Effect of variety, processing, and storage on the flavonoid glycoside content and composition of lettuce and endive. J. Agric. Food Chem. 48:2000;3957-3964.
25. Berrin J.G., McLauchlan W.R., Needs P., Williamson G., Puigserver A., Kroon P.A., Juge N. Functional expression of human liver cytosolic beta-glucosidase in Pichia pastoris: insights into its role in the metabolism of dietary glucosides. Eur. J. Biochem. 269:2002;249-258.
26. Lambert N., Kroon P.A., Faulds C.B., Plumb G.W., McLauchlan W.R., Day A.J., Williamson G. Purification of cytosolic beta-glucosidase from pig liver and its reactivity towards flavonoid glycosides. Biochim. Biophys. Acta. 1435:1998;110-116.
27. Wolffram S., Block M., Ader P. Quercetin-3-glucoside is transported by the glucose carrier SGLT1 across the brush-border membrane of rat small intestine. J. Nutr. 132:2002;630-635.
28. Hanke D.W., Warden D.A., Evans J.O., Fannin F.F., Diedrich D.F. Kinetic advantage for transport into hamster intestine of glucose generated from phlorizin by brush-border beta-glucosidase. Biochim. Biophys. Acta. 599:1980;652-663.
29. Warden D.A., Fannin F.F., Evans J.O., Hanke D.W., Diedrich D.F. A hydrolase-related transport system is not required to explain the intestinal uptake of glucose liberated from phlorizin. Biochim. Biophys. Acta. 599:1980;664-672.
30. +-glucose cotransporters (SGLT1). Am. J. Physiol. 33:1996;G919-G926.
31. Mizuma T., Awazu S. Inhibitory effect of phloridzin and phloretin on glucuronidation of p-nitrophenol, acetaminophen and 1-naphthol: kinetic demonstration of the influence of glucuronidation metabolism of intestinal absorption in rats. Biochim. Biophys. Acta. 1425:1998;398-404.
32. Morand C., Manach C., Crespy V., Remesy C. Quercetin-3-O-beta-glucoside is better absorbed than other quercetin forms and is not present in rat plasma. Free Radic. Res. 33:2000;667-672.
33. Crespy V., Morand C., Besson C., Manach C., Demigne C., Remesy C. Comparison of the intestinal absorption of quercetin, phloretin and their glucosides in rats. J. Nutr. 131:2001;2109-2114.
34. Rossi M., Maiuri L., Fusco M.I., Salvati V.M., Fuccio A., Auricchio S., Mantei N., Zecca L., Gloor S.M., Semenza G. Lactase persistence vs. decline in human adults: multi-factorial events are involved in down-regulation after weaning. Gastroenterology. 112:1997;1506-1514.
35. Goda T., Yasutake H., Tanaka T., Takase S. Lactase-phlorizin hydrolase and sucrase-isomaltase genes are expressed differently along the villus-crypt axis of rat jejunum. J. Nutr. 129:1999;1107-1113.
36. Johnson I.T., Gee J.M., Mahoney R.R. Effect of dietary-supplements of guar gum and cellulose on intestinal-cell proliferation, enzyme levels and sugar-transport in the rat. Br. J. Nutr. 52:1984;477-487.