Cacao polyphenol extract suppresses transformation of an aryl hydrocarbon receptor in C57BL/6 mice

Journal of Agricultural and Food Chemistry

Volumn 56, Issue 21, 2008, Pages 10399-10405

  Mukai, Rie ^a   Fukuda, Itsuko ^a   Nishiumi, Shin ^a   Natsume, Midori ^b   Osakabe, Naomi ^b   Yoshida, Ken Ichi ^a   Ashida, Hitoshi ^a  

^a KOBE UNIVERSITY   (Japan)

^b MEIJI SEIKA KAISHA LTD   (Japan)

Author keywords

Aryl hydrocarbon receptor; Cacao polyphenol extract; Cytochrome P4501A1; Glutathione S transferase; Nad(p)h: quinone oxidoreductase

Indexed keywords

MUS; THEOBROMA CACAO;

AROMATIC HYDROCARBON RECEPTOR; DIOXIN; FLAVONOID; PHENOL DERIVATIVE; PLANT EXTRACT; POLYPHENOLS; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; C57BL MOUSE; CACAO; CELL TRANSFORMATION; CHEMICALLY INDUCED DISORDER; DIMERIZATION; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION; GENETICS; HUMAN; LIVER; MALE; METABOLISM; MOUSE; PROTEIN BINDING; PROTEIN TRANSPORT; RANDOMIZATION; TUMOR CELL LINE;

ANIMALS; CACAO; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DIMERIZATION; DIOXINS; DOWN-REGULATION; FLAVONOIDS; GENE EXPRESSION; HUMANS; LIVER; MALE; MICE; MICE, INBRED C57BL; PHENOLS; PLANT EXTRACTS; PROTEIN BINDING; PROTEIN TRANSPORT; RANDOM ALLOCATION; RECEPTORS, ARYL HYDROCARBON;

EID: 58149345878     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf802453t     Document Type: Article

References (53)

1. Hankinson, O. The aryl hydrocarbon receptor complex. Arnu. Rev. Phannacol Toxicol. 1995, 35, 307-340.
2. Grassman, J. A.; Masten, S. A.; Walker. N. J.; Lucier, G. W. Animal models of human response to dioxins. Environ. Health Perspect. 1998, 106, 761-775.
3. Tuomisto. J. T.; Pohjanvirta, R.; Unkila. M.; Tuomisto, J. TCDD-induced anorexia and wasting syndrome in rats: effects of diet-induced obesity and nutrition. Pharmacol. Biochem. Behav. 1999, 62, 735-742.
4. Ito, T.; Inouye, K.; Fujimaki, H.; Tohyama, C.; Nohara, K. Mechanism of TCDD-induced suppression of antibody production: effect on T cell-derived cytokine production in the primary immune reaction of mice. Toxicol. Sci. 2002, 70, 46-54.
5. Perdew, G. H. Association of the Ah receptor with the 90-kDa heat shock protein. J. Biol. Chem. 1988, 263, 13802-13805.
6. Petrulis, J. R.; Hord, N. G.; Perdew. G. H. Subcellular localization of the aryl hydrocarbon receptor is modulated by the immunophilin homolog hepatitis B virus X-associated protein 2. J. Biol. Chem. 2000, 275, 37448-37453.
7. Shetty, P. V.; Bhagwat, B. Y.; Chan, W. K. p23 enhances the formation of the aryl hydrocarbon receptor-DNA complex. Biochem. Pharmacol. 2003, 65, 941-948.
8. Denison, M. S.; Vella, L. M.; Okey, A. B. Hepatic Ah receptor for 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. Partial stabilization by molybdate. J. Biol Chem. 1986, 261, 10189-10195.
9. Elferink, C. J.; Gasiewicz, T. A.; Whitlock, J. P., Jr. Protein-DNA interactions at a dioxin-responsive enhancer. Evidence that the transformed Ah receptor is heteromeric. J. Biol Chem. 1990, 265, 20708-20712.
10. Ko, H. P.; Okino, S. T.; Ma, Q.; Whitlock, J. P., Jr. Dioxin-induced CYP1A1 transcription in vivo: the aromatic hydrocarbon receptor mediates transactivation, enhancer-promoter communication, and changes in chromatin structure. Mol. Cell. Biol. 1996, 16, 430-436.
11. Elbekai, R. H.; El-Kadi, A. O. Modulation of aryl hydrocarbon receptor-regulated gene expression by arsenite, cadmium, and chromium. Toxicology 2004, 202, 249-269.
12. Rushmore, T. H.; King, R. G.; Paulson, K. E.; Pickett, C. B. Regulation of glutathione S-transferase Ya subunit gene expression: identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc. Natl. Acad. Sci. U. S. A. 1990, 87, 3826-3830.
13. lyanagi, T.; Haniu, M.; Sogawa, K.; Fujii-Kuriyama, Y.; Watanabe, S.; Shively, J. E.; Anan, K. F. Cloning and characterization of cDNA encoding 3-methylcholanthrene inducible rat mRNA for UDP-glucuronosvltransferase. J. Biol. Chem. 1986, 261, 15607-15614.
14. Thurmond, T. S.: Silverstone, A. E.; Baggs, R. B.; Quimby, F. W.; Staples, J. E.; Gasiewicz, T. A. A chimeric aryl hydrocarbon receptor knockout mouse model indicates that aryl hydrocarbon receptor activation in hematopoietic cells contributes to the hepatic lesions induced by 2.3, 7.8- tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 1999, 158, 33-40.
15. Baba, S.; Osakabe, N.: Natsume, M.; Yasuda, A.; Takizawa, T.; Nakamura, T.; Terao, J. Cocoa powder enhances the level of antioxidative activity in rat plasma, R. J. Nutr. 2000, 84, 673-680.
16. Osakabe. N.; Yamagishi, M.; Natsume. M.; Yasuda, A.; Osawa. T. Ingestion of proanthocyanidins derived from cacao inhibits diabetes-induced cataract formation in rats. Exp. Biol. Med. 2004, 229, 33-39.
17. Kurosawa, T.; Itoh. F; Nozaki, A.; Nakano, Y.; Katsuda. S.; Osakabe, N.; Tsubone, H.; Kondo, K.; Itakura, H. Suppressive effect of cocoa powder on atherosclerosis in Kurosawa and Kusanagi-hypercholes-terolemic rabbits. J. Atheroscler. Thromb. 2005, 12, 20-28.
18. Tomaru, M.; Takano. H.; Osakabe, N.; Yasuda. A.; Inoue, K.; Yanagisawa, R.; Ohwatari, T.; Uematsu, H. Dietary supplementation with cacao liquor proanthocyanidins prevents elevation of blood glucose levels in diabetic obese mice. Nutrition 2007. 23, 351-355.
19. Natsume, M.; Osakabe, N.; Yamagishi, M.; Takizawa, T.; Nakamura, T.; Miyatake, H.: Hatano, T.; Yoshida, T. Analyses of polyphenols in cacao liquor, cocoa, and chocolate by normal-phase and reversed-phase HPLC. Biosci., Biotechnol., Biochem. 2000, 64, 2581-2587.
20. Baba, S.; Osakabe, N.; Natsume, M.; Muto, Y.; Takizawa, T.; Terao, J. Absorption and urinary excretion of (-) -epicatechin after administration of different levels of cocoa powder or (-) - epicatechin in rats. J. Agric. Food Chem. 2001, 49, 6050-6056.
21. Rechner, A. R.; Kuhnle. G.; Bremner, P.; Hubbard, G. P.; Moore, K. P.; Rice-Evans, C. A. The metabolic fate of dietary polyphenols in humans. Free Radical Biol. Med. 2002, 33, 220-235.
22. Gonthier, M. P.; Cheynier, V.: Donovan, J. L.; Manach, C: Morand, C.; Mila, I.; Lapierre, C.; Remesy, C.; Scalbert, A. Microbial aromatic acid metabolites formed in the gut account for a major fraction of the polyphenols excreted in urine of rats fed red wine polyphenols. J. Nutr. 2003, 133, 461-467.
23. Baba, S.; Osakabe, N.; Natsume, M.; Muto, Y.; Takizawa, T.; Terao, J. In vivo comparison of the bioavailability of (+) -catechin, (-) -epicatechin and their mixture in orally administered rats. J. Nutr. 2001, 131, 2885-2891.
24. Fukuda. I.: Sakane. I.: Yabushita. Y.; Kodoi, R.; Nishiumi. S.; Kakuda, T.; Sawamura, S.; Kanazawa, K.; Ashida, H. Pigments in green tea leaves (Camellia sinensis) suppress transformation of the aryl hydrocarbon receptor induced by dioxin. J. Agric. Food Chem. 2004, 52, 2499-2506.
25. Fukuda. I.; Sakane, I.: Yabushita. Y.; Sawamura. S.; Kanazawa. K.; Ashida, H. Black tea theaflavins suppress dioxin-induced transformation of the aryl hydrocarbon receptor. Biosci., Biotechnol., Biochem. 2005, 69, 883-890.
26. Ashida, H.; Fukuda, I.; Yamashita, T.: Kanazawa, K. Flavones and flavonols at dietary levels inhibit a transformation of aryl hydrocarbon receptor induced by dioxin. FEBS Lett. 2000, 476, 213-217.
27. Ciolino. H. P.; Daschner, P. J.; Wang. T. T.; Yeh, G. C. Effect of curcumin on the aryl hydrocarbon receptor and cytochrome P450 1A1 in MCF-7 human breast carcinoma cells. Biochem. Pharmacol. 1998, 56, 197-206.
28. Casper, R. F.; Quesne, M.; Rogers, I. M.; Shirota, T.; Jolivet, A.; Milgrom, E.; Savouret, J. F. Resveratrol has antagonist activity on the aryl hydrocarbon receptor: implications for prevention of dioxin toxicity. Mol. Pharmacol. 1999, 56, 784-790.
29. Hamada, M.: Satsu, H.; Natsume, Y.; Nishiumi, S.; Fukuda, I.; Ashida, H.; Shimizu, M. TCDD-induced CYP1A1 expression, an index of dioxin toxicity, is suppressed by flavonoids permeating the human intestinal Caco-2 cell monolayers. J. Agric. Food Chem. 2006, 54, 8891-8898.
30. Nishiumi, S.: Yabushita, Y.: Fukuda, I.; Mukai, R.: Yoshida, K.; Ashida, H. Molokhia (Corchorus olitorius L.) extract suppresses transformation of the aryl hydrocarbon receptor induced by dioxins. Food Chem. Toxicol. 2006, 44, 250-260.
31. Fukuda, I.; Nishiumi, S.; Yabushita, Y.; Mukai, R.; Kodoi, R.; Hashizume, K.; Mizuno. M.; Hatanaka, Y.; Ashida, H. A new southwestern chemistry-based ELISA for detection of aryl hydrocarbon receptor transformation: application to the screening of its receptor agonists and antagonists. J. Immunol. Methods 2004, 287, 187-201.
32. Mukai. R.; Fukuda, I.: Hosokawa. K.; Nishiumi, S.; Kaneko. A.; Ashida, H. Anthocyans fail to suppress transformation of aryl hydrocarbon receptor induced by dioxin. Biosci., Biotechnol., Biochem. 2005, 69, 896-903.
33. Lind, C.; Cadenas, E.; Hochstein, P.; Ernster, L. DT-diaphorase: purification, properties, and function. Methods Enzymol. 1990, 186, 287-301.
34. Habig. W. H.; Pabst. M. J.; Jakoby, W. B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974, 249, 7130-7139.
35. Poland, A.; Knutson, J. C. 2, 3, 7, 8-Tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: examination of the mechanism of toxicity. Annu. Rev. Pharmacol. Toxicol. 1982, 22, 517-554.
36. Nishiumi, S.; Sakane, I.; Yoshida, K.; Ashida, H. Isolation and identification of the active compound from molokhia (Corchorus olitorius L.) to suppress the transformation of an aryl hydrocarbon receptor. J. Clin. Biochem. Nutr. 2008, 43, 277-280.
37. Nishiumi, S.; Yoshida. K.; Ashida, H. Curcumin suppresses the transformation of an aryl hydrocarbon receptor through its phosphorylation. Arch. Biochem. Biophys. 2007, 466, 267-273.
38. Vaidyanathan, J. B.; Walle, T. Glucuronidation and sulfation of the tea flavonoid (-) -epicatechin by the human and rat enzymes. Drug Metab. Dispos. 2002, 30, 897-903.
39. Spencer, J. P.; Chowrimootoo, G.; Choudhury, R.; Debnam, E. S.; Srai, S. K.; Rice-Evans, C. The small intestine can both absorb and glucuronidate luminal flavonoids. FEBS Lett. 1999, 458, 224-230.
40. Okushio, K.; Suzuki, M.; Matsumoto, N.; Nanjo, F.; Hara, Y. Identification of (-) -epicatechin metabolites and their metabolic fate in the rat. Drug Metab. Dispos. 1999, 27, 309-316.
41. Baba, S.; Osakabe, N.; Natsume, M.; Terao, J. Absorption and urinary excretion of procyanidin B2 [epicatechin-(4β-8) -epicat-echin] in rats. Free Radical Biol. Med. 2002, 33, 142-148.
42. Baba. S.; Osakabe, N.: Yasuda. A.; Natsume, M.; Takizawa, T.; Nakamura, T.; Terao, J. Bioavailability of (-) -epicatechin upon intake of chocolate and cocoa in human volunteers. Free Radical Res. 2000, 33, 635-641.
43. Lemaire, G.; Delescluse, C.; Pralavorio, M.; Ledirac, N.; Lesca, P.; Rahmani, R. The role of protein tyrosine kinases in CYP1A1 induction by omeprazole and thiabendazole in rat hepatocytes. Life Sci. 2004, 74, 2265-2278.
44. Tan, Z.; Chang, X.; Puga. A.; Xia, Y. Activation of mitogen-activated protein kinases (MAPKs) by aromatic hydrocarbons: role in the regulation of aryl hydrocarbon receptor (AHR) function. Biochem. Pharmacol. 2002, 64, 771-780.
45. Long, W. P.; Pray-Grant, M.; Tsai, J. C.; Perdew, G. H. Protein kinase C activity is required for aryl hydrocarbon receptor pathway-mediated signal transduction. Mol. Pharmacol. 1998, 53, 691-700.
46. Palermo, C. M.; Westlake, C. A.; Gasiewicz, T. A. Epigallocat-echin gallate inhibits aryl hydrocarbon receptor gene transcription through an indirect mechanism involving binding to a 90 kDa heat shock protein. Biochemistry 2005, 44, 5041-5052.
47. Pongratz, 1.; Mason, G. G.; Poellinger, L. Dual roles of the 90-kDa heat shock protein hsp90 in modulating functional activities of the dioxin receptor. Evidence that the dioxin receptor functionally belongs to a subclass of nuclear receptors which require hsp90 both for ligand binding activity and repression of intrinsic DNA binding activity. J. Biol. Chem. 1992, 267, 13728-13734.
48. Ramadoss, P.; Perdew. G. H. The transactivation domain of the Ah receptor is a key determinant of cellular localization and ligand-independent nucleocytoplasmic shuttling properties. Biochemistry 2005, 44, 11148-11159.
49. Schrenk, D. Impact of dioxin-type induction of drug-metabolizing enzymes on the metabolism of endo- and xenobiotics. Biochem. Pharmacol. 1998, 55, 1155-1162.
50. Kohle. C.; Bock, K. W. Coordinate regulation of Phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2. Biochem. Pharmacol. 2007, 73, 1853-1862.
51. Nijhoff, W. A.; Bosboom, M. A.; Smidt, M. H.; Peters, W. H. Enhancement of rat hepatic and gastrointestinal glutathione and glutathione S-transferases by a-angelicalactone and flavone. Carcinogenesis 1995, 16, 607-612.
52. Maliakal, P. P.; Coville, P. F.; Wanwimolruk. S. Tea consumption modulates hepatic drug metabolizing enzymes in Wistar rats. J. Pharm. Pharmacol. 2001, 53, 569-577.
53. Clapper, M. L.; Szarka, C. E. Glutathione S-transferases-biomarkers of cancer risk and chemopreventive response. Chem.-Biol. Interact. 1998, 111-112, 377-388.