Analysis of flavonoids regulating the expression of UGT1A1 via xenobiotic receptors in intestinal epithelial cells

BioFactors

Volumn 40, Issue 3, 2014, Pages 336-345

  Hiura, Yuto ^a   Satsu, Hideo ^a   Hamada, Mika ^a   Shimizu, Makoto ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

3 hydroxyflavone; Aryl hydrocarbon receptor; Baicalein; Pregnane X receptor; Quartz crystal microbalance; UGT1A1

Indexed keywords

3 HYDROXYFLAVONE; AROMATIC HYDROCARBON RECEPTOR; BAICALEIN; DRUG METABOLIZING ENZYME; FLAVONOID; GLUCURONOSYLTRANSFERASE 1A1; PLANT MEDICINAL PRODUCT; POLYPHENOL; PREGNANE X RECEPTOR; RECOMBINANT PROTEIN; TERPENOID; XENOBIOTIC AGENT; 3-HYDROXYFLAVONE; FLAVANONE DERIVATIVE; GLUCURONOSYLTRANSFERASE; MESSENGER RNA; UGT1A1 ENZYME;

ARTICLE; CHEMICAL STRUCTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE MICROSCOPY; INTESTINE EPITHELIUM; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; QUARTZ CRYSTAL MICROBALANCE; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; RNA ISOLATION; ACTIVE TRANSPORT; CELL NUCLEUS; CYTOLOGY; DRUG EFFECTS; ENZYME INDUCTION; ENZYMOLOGY; EPITHELIUM CELL; GENETIC TRANSCRIPTION; GENETICS; INTESTINE MUCOSA; METABOLISM; TUMOR CELL LINE;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL LINE, TUMOR; CELL NUCLEUS; ENZYME INDUCTION; EPITHELIAL CELLS; FLAVANONES; FLAVONOIDS; GLUCURONOSYLTRANSFERASE; HUMANS; INTESTINAL MUCOSA; QUARTZ CRYSTAL MICROBALANCE TECHNIQUES; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; TRANSCRIPTION, GENETIC; XENOBIOTICS;

EID: 84902553283     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1153     Document Type: Article

References (45)

1. Zheng, K., Trivedi, M., and Siahaan, T. J. (2006) Structure and function of the intercellular junctions: barrier of paracellular drug delivery. Curr. Pharm. Des. 12, 2813-2824.
2. Camilleri, M., Madsen, K., Spiller, R., Greenwood-Van, M. B., and Verne, G. N. (2012) Intestinal barrier function in health and gastrointestinal disease. Neurogastroenterol. Motil. 24, 503-512.
3. Xu, C., Li, C. Y., and Kong, A. N. (2005) Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch. Pharm. Res. 28, 249-268.
4. Sim, S. C., Kacevska, M., and Ingelman-Sundberg, M. (2013) Pharmacogenomics of drug-metabolizing enzymes: a recent update on clinical implications and endogenous effects. Pharmacogenomics J. 13, 1-11.
5. Fisher, M. B., Paine, M. F., Strelevitz, T. J., and Wrighton, S. A. (2001) The role of hepatic and extrahepatic UDP-glucuronosyltransferases in human drug metabolism. Drug Metab. Rev. 33, 273-297.
6. Ostrow, J. D. and Murphy, N. H. (1970) Isolation and properties of conjugated bilirubin from bile. Biochem. J. 120, 311-327.
7. Sugatani, J. (2013) Function, genetic polymorphism, and transcriptional regulation of human UDP-glucuronosyltransferase (UGT) 1A1. Drug Metab. Pharmacokinet. 28, 83-92.
8. Iyanagi, T., Emi, Y., and Ikushiro, S. (1998) Biochemical and molecular aspects of genetic disorders of bilirubin metabolism. Biochim. Biophys. Acta 1407, 173-184.
9. Gagne, J. F., Montminy, V., Belanger, P., Journault, K., Gaucher, G., and Guillemette, C. (2002) Common human UGT1A polymorphisms and the altered metabolism of irinotecan active metabolite 7-ethyl-10-hydroxycamptothecin (SN-38). Mol. Pharmacol. 62, 608-617.
10. Mackenzie, P. I., Owens, I. S., Burchell, B., Bock, K. W., Bairoch, A., Belanger, A., Fournel-Gigleux, S., Green, M., Hum, D. W., Iyanagi, T., Lancet, D., Louisot, P., Magdalou, J., Chowdhury, J. R., Ritter, J. K., Schachter, H., Tephly, T. R., Tipton, K. F., and Nebert, D. W. (1997) The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics 7, 255-269.
11. Galijatovic, A., Otake, Y., Walle, U. K., and Walle, T. (2001) Induction of UDP-glucuronosyltransferase UGT1A1 by the flavonoid chrysin in Caco-2 cells-potential role in carcinogen bioinactivation. Pharm. Res. 18, 374-379.
12. Sugatani, J., Kojima, H., Ueda, A., Kakizaki, S., Yoshinari, K., Gong, Q. H., Owens, I. S., Negishi, M., and Sueyoshi, T. (2001) The phenobarbital response enhancer module in the human bilirubin UDP-glucuronosyltransferase UGT1A1 gene and regulation by the nuclear receptor CAR. Hepatology 33, 1232-1238.
13. Xie, W., Yeuh, M. F., Radominska-Pandya, A., Saini, S. P., Negishi, Y., Bottroff, B. S., Cabrera, G. Y., Tukey, R. H., and Evans, R. M. (2003) Control of steroid, heme, and carcinogen metabolism by nuclear pregnane X receptor and constitutive androstane receptor. Proc. Natl. Acad. Sci. USA 100, 4150-4155.
14. Yueh, M. F., Huang, Y. H., Hiller, A., Chen, S., Nguyen, N., and Tukey, R. H. (2003) Involvement of the xenobiotic response element (XRE) in Ah receptor-mediated induction of human UDP-glucuronosyltransferase 1A1. J. Biol. Chem. 278, 15001-15006.
15. Hamada, M., Satsu, H., Natsume, Y., Nishiumi, S., Fukuda, I., Ashida, H., and Shimizu, M. (2006) 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. 54, 8891-8898.
16. Walle, U. K. and Walle, T. (2002) Induction of human UDP-glucuronosyltransferase UGT1A1 by flavonoids-structural requirements. Drug Metab. Dispos. 30, 564-569.
17. Sugatani, J., Yamakawa, K., Tonda, E., Nishitani, S., Yoshinari, K., Degawa, M., Abe, I., Noguchi, H., and Miwa, M. (2004) The induction of human UDP-glucuronosyltransferase 1A1 mediated through a distal enhancer module by flavonoids and xenobiotics. Biochem. Pharmacol. 67, 989-1000.
18. Satsu, H., Chidachi, E., Hiura, Y., Ogiwara, H., Gondo, Y., and Shimizu, M. (2012) Induction of NAD(P)H:quinone oxidoreductase 1 expression by cysteine via Nrf2 activation in human intestinal epithelial LS180 cells. Amino Acids 43, 1547-1555.
19. Goryo, K., Suzuki, A., Del Carpio, C. A., Siizaki, K., Kuriyama, E., Mikami, Y., Kinoshita, K., Yasumoto, K., Rannug, A., Miyamoto, A., Fujii-Kuriyama, Y., and Sogawa, K. (2007) Biochem. Biophys. Res. Commun. 354, 396-402.
20. Chrencik, J. E., Orans, J., Moore, L. B., Xue, Y., Peng, L., Collins, J. L., Wisely, G. B., Lambert, M. H., Kliewer, S. A., and Redinbo, M. R. (2005) Structural disorder in the complex of human pregnane X receptor and the macrolide antibiotic rifampicin. Mol. Endocrinol. 19, 1125-1134.
21. Kawana, K., Ikuta, T., Kobayashi, Y., Gotoh, O., Takeda, K., and Kawajiri, K. (2003) Molecular mechanism of nuclear translocation of an orphan nuclear receptor, SXR. Mol. Pharmacol. 63, 524-531.
22. Janshoff, A., Galla, H. J., and Steinem, C. (2000) Piezoelectric mass-sensing devices as biosensors-an alternative to optical biosensors? Angew. Chem. Int. Ed. Engl. 39, 4004-4032.
23. Cheng, C. I., Chang Y. P., and Chu, Y. H. (2012) Biomolecular interactions and tools for their recognition: focus on the quartz crystal microbalance and its diverse surface chemistries and applications. Chem. Soc. Rev. 41, 1947-1971.
24. Kliewer, S. A., Goodwin, B., and Willson, T. M. (2002) The nuclear pregnane X receptor: a key regulator of xenobiotic metabolism. Endocr. Rev. 23, 687-702.
25. Raucy, J. L. (2003) Regulation of CYP3A4 expression in human hepatocytes by pharmaceuticals and natural products. Drug Metab. Dispos. 31, 533-539.
26. Staudinger, J. L., Goodwin, B., Jones, S. A., Hawkins-Brown, D., MacKenzie, K. I., LaTour, A., Liu, Y., Klaassen, C. D., Brown, K. K., Reinhard, J., Willson, T. M., Koller, B. H., and Kliewer, S. A. (2001) The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc. Natl. Acad. Sci. USA 98, 3369-3374.
27. Dussault, I., Lin, M., Hollister, K., Wang, E. H., Synold, T. W., and Forman, B. M. (2001) Peptide mimetic HIV protease inhibitors are ligands for the orphan receptor SXR. J. Biol. Chem. 276, 33309-33312.
28. Satsu, H., Hiura, Y., Mochizuki, K., Hamada, M., and Shimizu, M. (2008) Activation of the pregnane X receptor and induction of MDR1 by dietary phytochemicals. J. Agric. Food Chem. 56, 5366-5373.
29. Squires, E. J., Sueyoshi, T., and Negishi, M. (2004) Cytoplasmic localization of pregnane X receptor and ligand-dependent nuclear translocation in mouse liver. J. Biol. Chem. 279, 49307-49314.
30. Watkins, R. E., Wisely, G. B., Moore, L. B., Collins, J. L., Lambert, M. H., Williams, S. P., Willson, T. M., Kliewer, S. A., and Redinbo, M. R. (2001) The human nuclear xenobiotic receptor PXR: structural determinants of directed promiscuity. Science 292, 2329-2333.
31. Watkins, R. E., Maglich, J. M., Moore, L. B., Wisely, G. B., Noble, S. M., Davis-Searles, P. R., Lambert, M. H., Kliewer, S. A., and Redinbo, M. R. (2003) 2.1 A crystal structure of human PXR in complex with the St. John's wort compound hyperforin. Biochemistry 42, 1430-1438.
32. Fujii-Kuriyama, Y., Ema, M., Mimura, J., and Sogawa, K. (1994) Ah receptor: a novel ligand-activated transcription factor. Exp. Clin. Immunogenet. 11, 65-74.
33. Hahn, M. E. (1998) The aryl hydrocarbon receptor: a comparative perspective. Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol. 121, 23-53.
34. Meyer, B. K. and Perdew, G. H. (1999) Characterization of the AhR-hsp90-XAP2 core complex and the role of the immunophilin-related protein XAP2 in AhR stabilization. Biochemistry 38, 8907-8917.
35. Kazlauskas, A., Poellinger and L., Pongratz, I. (1999). Evidence that the co-chaperone p23 regulates ligand responsiveness of the dioxin (Aryl hydrocarbon) receptor. J. Biol. Chem. 274, 13519-13524.
36. Ko, H. P., Okino, S. T., Ma, Q., and Whitlock, J. P. Jr. (1996) Dioxin-induced CYP1A1 transcription in vivo: the aromatic hydrocarbon receptor mediates transactivation, enhancer-promoter communication, and changes in chromatin structure. Mol. Cell Biol. 16, 430-436.
37. Fukuda, I., Mukai, R., Kawase, M., Yoshida, K., and Ashida, H. (2007) Interaction between the aryl hydrocarbon receptor and its antagonists, flavonoids. Biochem. Biophys. Res. Commun. 359, 822-827.
38. Dong, H., Lin, W., Wu, J., and Chen, T. (2010) Flavonoids activate pregnane x receptor-mediated CYP3A4 gene expression by inhibiting cyclin-dependent kinases in HepG2 liver carcinoma cells. BMC Biochem. 11, 23.
39. Wakabayashi, I. (1999) Inhibitory effects of baicalein and wogonin on lipopolysaccharide-induced nitric oxide production in macrophages. Pharmacol. Toxicol. 84, 288-291.
40. Li, F. Q., Wang, T., Pei, Z., Liu, B., and Hong, J. S. (2005) Inhibition of microglial activation by the herbal flavonoid baicalein attenuates inflammation-mediated degeneration of dopaminergic neurons. J. Neural. Transm. 112, 331-347.
41. Ng, S. P., Wong, K. Y., Zhang, L., Zuo, Z., and Lin, G. (2004) Evaluation of the first-pass glucuronidation of selected flavones in gut by Caco-2 monolayer model. J. Pharm. Pharm. Sci. 20, 1-9.
42. Xu, B., Yang, G., Ge, S., Yin, T., Hu, M., and Gao, S. (2013) Validated LC-MS/MS method for the determination of 3-hydroxflavone and its glucuronide in blood and bioequivalent buffers: application to pharmacokinetic, absorption, and metabolism studies. J. Pharm. Biomed. Anal. 85, 245-252.
43. Zhou, C., Tabb, M. M., Nelson, E. L., Grun, F., Verma, S., Sadatrafiei, A., Lin, M., Mallick, S., Forman, B. M., Thummel, K. E., and Blumberg, B. (2006) Mutual repression between steroid and xenobiotic receptor and NF-kappaB signaling pathways links xenobiotic metabolism and inflammation. J. Clin. Invest. 116, 2280-2289.
44. Cheng, J., Shah, Y. M., and Gonzalez, F. J. (2012) Pregnane X receptor as a target for treatment of inflammatory bowel disorders. Trends Pharmacol. Sci. 33, 323-330.
45. Thatcher, T. H., Maggirwar, S. B., Baglole, C. J., Lakatos, H. F., Gasiewicz, T. A. Phipps, R. P., and Sime, P. J. (2007) Aryl hydrocarbon receptor-deficient mice develop heightened inflammatory responses to cigarette smoke and endotoxin associated with rapid loss of the nuclear factor-kappaB component RelB. Am. J. Pathol. 170, 855-864.