Modulation of CYP1A1 activity by a Ginkgo biloba extract in the human intestinal Caco-2 cells

Toxicology Letters

Volumn 202, Issue 3, 2011, Pages 193-202

  Ribonnet, L ^a   Callebaut, A ^b   Nobels, I ^c   Scippo, M L ^d   Schneider, Y J ^a   De Saeger, S ^e   Pussemier, L ^b   Larondelle, Y ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b VETERINARY AND AGROCHEMICAL RESEARCH CENTRE   (Belgium)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d UNIVERSITY OF LIÈGE   (Belgium)

^e GHENT UNIVERSITY   (Belgium)

Author keywords

Caco 2 cells; CYP1A1; Flavonols; Ginkgo biloba; Intestine; Terpenes

Indexed keywords

BILOBALIDE; CYTOCHROME P450 1A1; FLAVONOL DERIVATIVE; GINKGO BILOBA EXTRACT; GINKGOLIDE DERIVATIVE; ISORHAMNETIN; KAEMPFEROL; QUERCETIN;

ARTICLE; CELL ACTIVITY; CELL STRAIN CACO 2; CYTOTOXICITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

ANTIOXIDANTS; CACO-2 CELLS; CELL SURVIVAL; CYTOCHROME P-450 CYP1A1; DOSE-RESPONSE RELATIONSHIP, DRUG; ENTEROCYTES; ENZYME INDUCTION; GINKGO BILOBA; HUMANS; PLANT EXTRACTS;

GINKGO BILOBA;

EID: 79954618299     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2011.02.006     Document Type: Article

References (81)

1. Boulenc X., Bourrie M., Fabre I., Roque C., Joyeux H., Berger Y., Fabre G. Regulation of cytochrome P4501A1 gene expression in a human intestinal cell line, Caco-2. The journal of pharmacology and experimental therapeutics 1992, 263:1471-1478.
2. Burke M.D., Thompson S., Weaver R.J., Wolf C.R., Mayer R.T. Cytochrome P450 specificities of alkoxyresorufin O-dealkylation in human and rat liver. Biochemical Pharmacology 1994, 48:923-936.
3. Carbonaro M., Grant G. Absorption of quercetin and rutin in rat small intestine. Annals of Nutrition & Metabolism 2005, 49:178-182.
4. Chang T.K.H., Chen J., Yeung E.Y.H. Effect of Ginkgo biloba extract on procarcinogen-bioactivating human CYP1 enzymes: identification of isorhamnetin, kaempferol, and quercetin as potent inhibitors of CYP1B1. Toxicology and Applied Pharmacology 2006, 213:18-26.
5. Ciolino H.P., Daschner P.J., Yeh G.C. Dietary flavonols quercetin and kaempferol are ligands of the aryl hydrocarbon receptor that affect CYP1A1 transcription differentially. Biochemical Journal 1999, 340:715-722.
6. Day A.J., Canada F.J., Diaz 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 Letters 2000, 468:166-170.
7. 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 Letters 1998, 436:71-75.
8. Day A.J., Gee J.M., DuPont M.S., Johnson I.T., Williamson G. 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 2003, 65:1199-1206.
9. de Waard P.W.J., de Kok T.M.C.M., Maas L.M., Peijnenburg A.A.C.M., Hoogenboom R.L.A.P., Aarts J.M.M.J.G., van Schooten F.-J. Influence of TCDD and natural Ah receptor agonists on benzo[a]pyrene-DNA adduct formation in the Caco-2 human colon cell line. Mutagenesis 2008, 23:67-73.
10. de Waard W.J., Aarts J.M.M.J.G., Peijnenburg A.A.C.M., Baykus H., Talsma E., Punt A., de Kok T.M.C.M., van Schooten F.J., Hoogenboom L.A.P. Gene expression profiling in Caco-2 human colon cells exposed to TCDD, benzo[a]pyrene, and natural Ah receptor agonists from cruciferous vegetables and citrus fruits. Toxicology in Vitro 2008, 22:396-410.
11. de Waziers I., Cugnenc P., Yang C., Leroux J., Beaune P. Cytochrome P 450 isoenzymes, epoxide hydrolase and glutathione transferases in rat and human hepatic and extrahepatic tissues. The journal of pharmacology and experimental therapeutics 1990, 253:387-394.
12. Deng Y., Bi H.-C., Zhao L.-Z., He F., Liu Y.-Q., Yu J.-J., Ou Z.-M., Ding L., Chen X., Huang Z.-Y., Huang M., Zhou S.-F. Induction of cytochrome P450s by terpene trilactones and flavonoids of the Ginkgo biloba extract EGb 761 in rats. Xenobiotica 2008, 38:465-481.
13. Ding S., Dudley E., Plummer S., Tang J., Newton R.P., Brenton A.G. Fingerprint profile of Ginkgo biloba nutritional supplements by LC/ESI-MS/MS. Phytochemistry 2008, 69:1555-1564.
14. Dubber M.J., Sewram V., Mshicileli N., Shephard G.S., Kanfer I. The simultaneous determination of selected flavonol glycosides and aglycones in Ginkgo biloba oral dosage forms by high-performance liquid chromatography-electrospray ionisation-mass spectrometry. Journal of Pharmaceutical and Biomedical Analysis 2005, 37:723-731.
15. Edenharder R., Rauscher R., Platt K.L. The inhibition by flavonoids of 2-amino-3-methylimidazo[4,5-f]quinoline metabolic activation to a mutagen: a structure-activity relationship study. Mutation Research 1997, 379:21-32.
16. Erlund I., Kosonen T., Alfthan G., Maenpaa J., Perttunen K., Kenraali J., Parantainen J., Aro A. Pharmacokinetics of quercetin from quercetin aglycone and rutin in healthy volunteers. European Journal of Clinical Pharmacology 2000, 56:545-553.
17. Fallone F., Villard P.-H., Decome L., Sérée E., Méo M.d., Chacon C., Durand A., Barra Y., Lacarelle B. PPAR-α activation potentiates AhR-induced CYP1A1 expression. Toxicology 2005, 216:122-128.
18. Fontana R.J., Lown K.S., Paine M.F., Fortlage L., Santella R.M., Felton J.S., Knize M.G., Greenberg A., Watkins P.B. Effects of a chargrilled meat diet on expression of CYP3A, CYP1A, and P-glycoprotein levels in healthy volunteers. Gastroenterology 1999, 117:89-98.
19. Gaudineau C., Beckerman R., Welbourn S., Auclair K. Inhibition of human P450 enzymes by multiple constituents of the Ginkgo biloba extract. Biochemical and Biophysical Research Communications 2004, 318:1072-1078.
20. Goh L.M.L., Barlow P.J. Flavonoid recovery and stability from Ginkgo biloba subjected to a simulated digestion process. Food Chemistry 2004, 86:195-202.
21. Haghi G., Hatami A. Simultaneous quantification of flavonoids and phenolic acids in plant materials by a newly developed isocratic high-performance liquid chromatography approach. Journal of Agricultural and Food Chemistry 2010, 58:10812-10816.
22. Hollman P., de Vries J., van Leeuwen S., Mengelers M., Katan M. Absorption of dietary quercetin glycosides and quercetin in healthy ileostomy volunteers. The American Journal of Clinical Nutrition 1995, 62:1276-1282.
23. Hollman P.C., van Trijp J.M., Buysman M.N., van der Gaag M.S., Mengelers M.J., de Vries J.H., Katan M.B. Relative bioavailability of the antioxidant flavonoid quercetin from various foods in man. FEBS Letters 1997, 418:152-156.
24. Jaganath I.B., Mullen W., Edwards C.A., Crozier A. The relative contribution of the small and large intestine to the absorption and metabolism of rutin in man. Free Radical Research 2006, 40:1035-1046.
25. Jeuken A., Keser B.J.G., Khan E., Brouwer A., Koeman J., Denison M.S. Activation of the Ah receptor by extracts of dietary herbal supplements, vegetables, and fruits. Journal of Agricultural and Food Chemistry 2003, 51:5478-5487.
26. Kang Z.C, Tsai S.-J., Lee H. Quercetin inhibits benzo[a]pyrene-induced DNA adducts in human Hep G2 cells by altering cytochrome P-450 1A1 gene expression. Nutrition and Cancer 1999, 35:175-179.
27. Kim H.-J., Chun H.-S., Yang R. Inhibition of benzo[a]pyrene-induced cytotoxicity and cytochrome P450 1A activity by dietary flavonoids in human liver cell model: structure-activity relationship. Biotechnology Letters 2000, 22:1941-1946.
28. Kuo I.f., Chen J., Chang T.K.H. Effect of Ginkgo biloba extract on rat hepatic microsomal CYP1A activity: role of ginkgolides, bilobalide, and flavonols. Canadian Journal of Physiology and Pharmacology 2004, 82:57-64.
29. Lampen A., Bader A., Bestmann T., Winkler M., Witte L., Borlak J.T. Catalytic activities, protein- and mRNA-expression of cytochrome P450 isoenzymes in intestinal cell lines. Xenobiotica 1998, 28:429-441.
30. Lampen A., Ebert B., Stumkat L., Jacob J., Seidel A. Induction of gene expression of xenobiotic metabolism enzymes and ABC-transport proteins by PAH and a reconstituted PAH mixture in human Caco-2 cells. Biochimica et Biophysica Acta 2004, 1681:38-46.
31. Lampen A., Meyer S., Arnhold T., Nau H. Metabolism of vitamin A and its active metabolite all-trans-retinoic acid in small intestinal enterocytes. Journal of Pharmacology and Experimental Therapeutics 2000, 295:979-985.
32. Lan K., He J.-l., Tian Y., Tan F., Jiang X.-h., Wang L., Ye L.-m. Intra-herb pharmacokinetics interaction between quercetin and isorhamentin. Acta Pharmacologica Sinica 2008, 29:1376-1382.
33. Le Ferrec E., Chesne C., Artusson P., Brayden D., Fabre G., Gires P., Guillou F., Rousset M., Rubas W., Scarino M.-L. In vitro models of the intestinal barrier. The report and recommandations of ECVAM Workshop 46. ATLA 2001, 29:649-668.
34. Lee A.J., Cai M.X., Thomas P.E., Conney A.H., Zhu B.T. Characterization of the oxidative metabolites of 17β-estradiol and estrone formed by 15 selectively expressed human cytochrome P450 isoforms. Endocrinology 2003, 144:3382-3398.
35. Li L., Stanton J.D., Tolson A.H., Luo Y., Wang H. Bioactive terpenoids and flavonoids from Ginkgo biloba extract induce the expression of hepatic drug-metabolizing enzymes through pregnane X receptor, constitutive androstane receptor, and aryl hydrocarbon receptor-mediated pathways. Pharmaceutical Research 2008, 26:872-882.
36. Lindell M., Karlsson M.O., Lennernäs H., Påhlman L., Lang M.A. Variable expression of CYP and Pgp genes in the human small intestine. European Journal of Clinical Investigation 2003, 33:493-499.
37. Lown K.S., Bailey D.G., Fontana R.J., Janardan S.K., Adair C.H., Fortlage L.A., Brown M.B., Guo W., Watkins P.B. Grapefruit juice increases felodipine oral availability in humans by decreasing intestinal CYP3A protein expression. The Journal of Clinical Investigation 1997, 99:2545-2553.
38. Lv H., Wang G., Wu X., Xie L., Huang C., Li H., Liang Y., Hao H., Sun J. Transport characteristics of ginkgolide B by Caco-2 cells and examination of ginkgolide B oral absorption potential using rat in situ intestinal loop method. International Journal of Pharmaceutics 2008, 351:31-35.
39. Madgula V.L.M., Avula B., Yu Y.-B., Wang Y.-H., Tchantchou F., Fisher S., Luo Y., Khan I.A., Khan S.I. Intestinal and blood-brain barrier permeability of ginkgolides and bilobalide: in vitro and in vivo approaches. Planta Medica 2010, 76:599-606.
40. Mense S.M., Chhabra J., Bhat H.K. Preferential induction of cytochrome P450 1A1 over cytochrome P450 1B1 in human breast epithelial cells following exposure to quercetin. The Journal of Steroid Biochemistry and Molecular Biology 2008, 110:157-162.
41. Murray M. Altered CYP expression and function in response to dietary factors: potential roles in disease pathogenesis. Current Drug Metabolism 2006, 7:67-81.
42. Nebert D., Dalton T., Okey A., Gonzalez F. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. The Journal of Biological Chemistry 2004, 279:23847-23850.
43. Németh K., Plumb G.W., Berrin J.-G., Juge N., Jacob R., Naim H.Y., Williamson G., Swallow D.M., Kroon P.A. Deglycosylation by small intestinal epithelial cell β-glucosidase is a critical step in the absorption and metabolism of dietary flavonoid glycosides in humans. European Journal of Nutrition 2003, 42:29-42.
44. Oh S.M., Chung K.H. Antiestrogenic activities of Ginkgo biloba extracts. The Journal of Steroid Biochemistry and Molecular Biology 2006, 100:167-176.
45. Paine M.F., Hart H.L., Ludington S.S., Haining R.L., Rettie A.E., Zeldin D.C. The human intestinal cytochrome P450 " pie" Drug Metabolism and Disposition 2006, 34:880-886.
46. Paine M.F., Khalighi M., Fisher J.M., Shen D.D., Kunze K.L., Marsh C.L., Perkins J.D., Thummel K.E. Characterization of interintestinal and intraintestinal variations in human CYP3A-dependent metabolism. Journal of Pharmacology and Experimental Therapeutics 1997, 283:1552-1562.
47. Paine M.F., Schmiedlin-Ren P., Watkins P.B. Cytochrome P-450 1A1 expression in human small bowel: interindividual variation and inhibition by ketoconazole. Drug Metabolism and Disposition 1999, 27:360-364.
48. Parl F.F., Dawling S., Roodi N., Crooke P.S. Estrogen metabolism and breast cancer. Annals of the New York Academy of Sciences 2009, 1155:68-75.
49. Pohl C., Will F., Dietrich H., Schrenk D. Cytochrome P450 1A1 expression and activity in Caco-2 cells: modulation by apple juice extract and certain apple polyphenols. Journal of Agricultural and Food Chemistry 2006, 10262-10268.
50. Prueksaritanont T., Gorham L.M., Hochman J.H., Tran L.O., Vyas K.P. Comparative studies of drug-metabolizing enzymes in dog, monkey, and human small intestines, and in Caco-2 cells. Drug Metabolism and Disposition 1996, 24:634-642.
51. Puppala D., Gairola C., Swanson H. Identification of kaempferol as an inhibitor of cigarette smoke-induced activation of the aryl hydrocarbon receptor and cell transformation. Carcinogenesis 2007, 28:639-647.
52. Rajaraman G., Yang G., Chen J., Chang T.K.H. Modulation of CYP1B1 and CYP1A1 gene expression and activation of aryl hydrocarbon receptor by Ginkgo biloba extract in MCF-10A human mammary epithelial cells. Canadian Journal of Physiology and Pharmacology 2009, 87:674-683.
53. Rimmer C.A., Howerton S.B., Sharpless K.E., Sander L.C., Long S.E., Murphy K.E., Porter B.J., Putzbach K., Rearick M.S., Wise S.A., Wood L.J., Zeisler R., Hancock D.K., Yen J.H., Betz J.M., NguyenPho A., Yang L., Scriver C., Willie S., Sturgeon R., Schaneberg B., Nelson C., Skamarack J., Pan M., Levanseler K., Gray D., Waysek E.H., Blatter A., Reich E. Characterization of a suite of ginkgo-containing standard reference materials. Analytical and Bioanalytical Chemistry 2007, 389:179-196.
54. Rosenberg D.W., Leff T. Regulation of cytochrome P450 in cultured human colonic cells. Archives of Biochemistry and Biophysics 1993, 300:186-192.
55. Schwarz D., Kisselev P., Cascorbi I., Schunck W.H., Roots I. Differential metabolism of benzo[a]pyrene and benzo[a]pyrene-7,8-dihydrodiol by human CYP1A1 variants. Carcinogenesis 2001, 22:453-459.
56. Schwarz D., Kisselev P., Roots I. CYP1A1 genotype-selective inhibition of benzo[a]pyrene activation by quercetin. European Journal of Cancer 2005, 41:151-158.
57. Schwarz D., Kisselev P., Schunck W.-H., Roots I. Inhibition of 17(-estradiol activation by CYP1A1: genotype- and regioselective inhibition by St. John's Wort and several natural polyphenols. Biochimica et Biophysica Acta 2010, 1814:168-174.
58. Schwarz D., Roots I. In vitro assessment of inhibition by natural polyphenols of metabolic activation of procarcinogens by human CYP1A1. Biochemical and Biophysical Research Communications 2003, 303:902-907.
59. Sérée E., Villard P.-H., Pascussi J.-M., Pineau T., Maurel P., Nguyen Q.B., Fallone F., Martin P.-M., Champion S., Lacarelle B., Savouret J.-F., Barra Y. Evidence for a new human CYP1A1 regulation pathway involving PPAR-α and 2 PPRE sites. Gastroenterology 2004, 127:1436-1445.
60. Sergent T., Dupont I., Van Der Heiden E., Scippo M.-L., Pussemier L., Larondelle Y., Schneider Y.-J. CYP1A1 and CYP3A4 modulation by dietary flavonoids in human intestinal Caco-2 cells. Toxicology Letters 2009, 184.
61. Shi Z., Dragin N., Galvez-Peralta M., Jorge-Nebert L.F., Miller M.L., Wang B., Nebert D.W. Organ-specific roles of CYP1A1 during detoxication of dietary benzo[a]pyrene. Molecular Pharmacology 2010, 78:46-57.
62. Shimada T., Oda Y., Gillam E.M., Guengerich F.P., Inoue K. Metabolic activation of polycyclic aromatic hydrocarbons and other procarcinogens by cytochromes P450 1A1 and P450 1B1 allelic variants and other human cytochromes P450 in Salmonella typhimurium NM2009. Drug Metabolism and Disposition 2001, 29:1176-1182.
63. Siess M.H., Leclerc J., Canivenc-Lavier M.C., Rat P., Suschetet M. Heterogenous effects of natural flavonoids on monooxygenase activities in human and rat liver microsomes. Toxicology and Applied Pharmacology 1995, 130:73-78.
64. Strømgaard K., Nakanishi K. Chemistry and biology of terpene trilactones from Ginkgo biloba. Angewandte Chemie International Edition 2004, 43:1640-1658.
65. Sugiyama T., Kubota Y., Shinozuka K., Yamada S., Yamada K., Umegaki K. Induction and recovery of hepatic drug metabolizing enzymes in rats treated with Ginkgo biloba extract. Food and Chemical Toxicology 2004, 42:953-957.
66. Taki Y., Yamazaki Y., Shimura F., Yamada S., Umegaki K. Time-dependent induction of hepatic cytochrome P450 enzyme activity and mRNA expression by bilobalide in rats. Journal of Pharmacological Sciences 2009, 109:459-462.
67. Tang D., Yang D., Tang A., Gao Y., Jiang X., Mou J., Yin X. Simultaneous chemical fingerprint and quantitative analysis of Ginkgo biloba extract by HPLC-DAD. Analytical and Bioanalytical Chemistry 2010, 396:3087-3095.
68. Tian X., Yang X., Wang K., Yang X. The efflux of flavonoids morin, isorhamnetin-3-O-rutinoside and diosmetin-7-O-β-D-xylopyranosyl-(1-6)-β-D-glucopyranoside in the human intestinal cell line Caco-2. Pharmaceutical Research 2006, 23:1721-1728.
69. Tsuchiya Y., Nakajima M., Yokoi T. Cytochrome P450-mediated metabolism of estrogens and its regulation in human. Cancer Letters 2005, 227:115-124.
70. Umegaki K., Saito K., Kubota Y., Sanada H., Yamada K., Shinozuka K. Ginkgo biloba extract markedly induces pentoxyresorufin O-dealkylase activity in rats. The Japanese Journal of Pharmacology 2002, 90:345-351.
71. Umegaki K., Taki Y., Endoh K., Taku K., Tanabe H., Shinozuka K., Sugiyama T. Bilobalide in Ginkgo biloba extract is a major substance inducing hepatic CYPs. Journal of Pharmacy and Pharmacology 2007, 59:871-877.
72. Uno S., Dalton T.P., Derkenne S., Curran C.P., Miller M.L., Shertzer H.G., Nebert D.W. Oral exposure to benzo[a]pyrene in the mouse: detoxication by inducible cytochrome P450 is more important than metabolic activation. Molecular Pharmacology 2004, 65:1225-1237.
73. Uno S., Dalton T.P., Dragin N., Curran C.P., Derkenne S., Miller M.L., Shertzer H.G., Gonzalez F.J., Nebert D.W. Oral benzo[a]pyrene in Cyp1 knockout mouse lines: CYP1A1 important in detoxication, CYP1B1 metabolism required for immune damage independent of total-body burden and clearance rate. Molecular Pharmacology 2006, 69:1103-1114.
74. van Beek T.A., Montoro P. Chemical analysis and quality control of Ginkgo biloba leaves, extracts, and phytopharmaceuticals. Journal of Chromatography A 2009, 1216:2002-2032.
75. Van der Heiden E, Bechoux N., Muller M., Sergent T., Schneider Y.-J., Larondelle Y., Maghuin-Rogister G., Scippo M.-L. Food flavonoid aryl hydrocarbon receptor-mediated agonistic/antagonistic/synergic activities in human and rat reporter gene assays. Analytica Chimica Acta 2009, 637:337-345.
76. Walgren R.A., Karnaky K.J., Lindenmayer G.E., Walle T. Efflux of dietary flavonoid quercetin 4'-β-glucoside across human intestinal Caco-2 cell monolayers by apical multidrug resistance-associated protein-2. Journal of Pharmacology and Experimental Therapeutics 2000, 294:830-836.
77. Walgren R.A., Lin J.T., Kinne R.K., Walle T. Cellular uptake of dietary flavonoid quercetin 4'-β-glucoside by sodium-dependent glucose transporter SGLT1. Journal of Pharmacology and Experimental Therapeutics 2000, 294:837-843.
78. Wang Y., Cao J., Zeng S. Involvement of P-glycoprotein in regulating cellular levels of Ginkgo flavonols: quercetin, kaempferol, and isorhamnetin. Journal of Pharmacy and Pharmacology 2005, 57:751-758.
79. 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. Journal of Nutrition 2002, 132:630-635.
80. Yang X., Wang N., Lu W., Zeng F. Effects of Ginkgo biloba extract and tanshinone on cytochrome P-450 isozymes and glutathione transferase in rats. Acta Pharmacologica Sinica 2003, 24:1033-1038.
81. Zhang Q.Y., Dunbar D., Ostrowska A., Zeisloft S., Yang J., Kaminsky L.S. Characterization of human small intestinal cytochromes P-450. Drug Metabolism and Disposition 1999, 27:804-809.