Fucoxanthin attenuates rifampin-induced cytochrome P450 3A4 (CYP3A4) and multiple drug resistance 1 (MDR1) gene expression through pregnane X receptor (PXR)-mediated pathways in human hepatoma HepG2 and colon adenocarcinoma LS174T cells

Marine Drugs

Volumn 10, Issue 1, 2012, Pages 242-257

  Liu, Cheng Ling ^a   Lim, Yun Ping ^b,c   Hu, Miao Lin ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

CYP3A4; Drug resistance; Fucoxanthin; MDR1; PXR; Rifampin

Indexed keywords

CONSTITUTIVE ANDROSTANE RECEPTOR; CYTOCHROME P450 3A4; FUCOXANTHIN; MULTIDRUG RESISTANCE PROTEIN 1; PREGNANE X RECEPTOR; RIFAMPICIN; STEROID RECEPTOR COACTIVATOR 1;

ARTICLE; CELL STRAIN HEPG2; COLON ADENOCARCINOMA; CONTROLLED STUDY; CYP3A4 GENE; DRUG ANTAGONISM; DRUG MECHANISM; DRUG RESISTANCE; ENZYME ACTIVITY; GENE; GENE EXPRESSION; HEPATOMA CELL; HUMAN; HUMAN CELL; MDR1 GENE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TUMOR CELL;

ALGAE; MAMMALIA;

EID: 84863032179     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md10010242     Document Type: Article

References (49)

1. Maeda, H.; Hosokawa, M.; Sashima, T.; Takahashi, N.; Kawada, T.; Miyashita, K. Fucoxanthin and its metabolite, fucoxanthinol, suppress adipocyte differentiation in 3T3-L1 cells. Int. J. Mol. Med. 2006, 18, 147-152.
2. Nishino, H.; Tokuda, H.; Murakoshi, M.; Satomi, Y.; Masuda, M.; Onozuka, M.; Yamaguchi, S.; Takayasu, J.; Tsuruta, J.; Okuda, M.; Khachik, F.; Narisawa, T.; Takasuka, N.; Yano, M. Cancer prevention by natural carotenoids. Biofactors 2000, 13, 89-94. (Pubitemid 32107350)
3. Shiratori, K.; Ohgami, K.; Ilieva, I.; Jin, X.H.; Koyama, Y.; Miyashita, K.; Yoshida, K.; Kase, S.; Ohno, S. Effects of fucoxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo. Exp. Eye Res. 2005, 81, 422-428. (Pubitemid 41356505)
4. Kotake-Nara, E.; Kushiro, M.; Zhang, H.; Sugawara, T.; Miyashita, K.; Nagao, A. Carotenoids affect proliferation of human prostate cancer cells. J. Nutr. 2001, 131, 3303-3306. (Pubitemid 33136153)
5. Kotake-Nara, E.; Terasaki, M.; Nagao, A. Characterization of apoptosis induced by fucoxanthin in human promyelocytic leukemia cells. Biosci. Biotechnol. Biochem. 2005, 69, 224-227. (Pubitemid 40383507)
6. Hosokawa, M.; Kudo, M.; Maeda, H.; Kohno, H.; Tanaka, T.; Miyashita, K. Fucoxanthin induces apoptosis and enhances the antiproliferative effect of the PPARgamma ligand, troglitazone, on colon cancer cells. Biochim. Biophys. Acta 2004, 1675, 113-119.
7. Sugawara, T.; Baskaran, V.; Tsuzuki, W.; Nagao, A. Brown algae fucoxanthin is hydrolyzed to fucoxanthinol during absorption by caco-2 human intestinal cells and mice. J. Nutr. 2002, 132, 946-951. (Pubitemid 34493558)
8. Asai, A.; Sugawara, T.; Ono, H.; Nagao, A. Biotransformation of fucoxanthinol into amarouciaxanthin a in mice and HepG2 cells: Formation and cytotoxicity of fucoxanthin metabolites. Drug Metab. Dispos. 2004, 32, 205-211. (Pubitemid 38176937)
9. Hashimoto, T.; Ozaki, Y.; Mizuno, M.; Yoshida, M.; Nishitani, Y.; Azuma, T.; Komoto, A.; Maoka, T.; Tanino, Y.; Kanazawa, K. Pharmacokinetics of fucoxanthinol in human plasma after the oral administration of kombu extract. Br. J. Nutr. 2011, 16, 1-4.
10. Choi, B.H.; Kim, C.G.; Lim, Y.; Shin, S.Y.; Lee, Y.H. Curcumin down-regulates the multidrug-resistance mdr1b gene by inhibiting the PI3K/Akt/NF kappa B pathway. Cancer Lett. 2008, 259, 111-118. (Pubitemid 350235095)
11. Chan, M.M.; Soprano, K.J.; Weinstein, K.; Fong, D. Epigallocatechin-3- gallate delivers hydrogen peroxide to induce death of ovarian cancer cells and enhances their cisplatin susceptibility. J. Cell. Physiol. 2006, 207, 389-396.
12. Hwang, J.T.; Kwak, D.W.; Lin, S.K.; Kim, H.M.; Kim, Y.M.; Park, O.J. Resveratrol induces apoptosis in chemoresistant cancer cells via modulation of AMPK signaling pathway. Ann. N. Y. Acad. Sci. 2007, 1095, 441-448.
13. Pan, M.H.; Gao, J.H.; Lai, C.S.; Wang, Y.J.; Chen, W.M.; Lo, C.Y.; Wang, M.; Dushenkov, S.; Ho, C.T. Antitumor activity of 3,5,4′- trimethoxystilbene in COLO 205 cells and xenografts in SCID mice. Mol. Carcinog. 2008, 47, 184-196.
14. Molnar, J.; Gyemant, N.; Mucsi, I.; Molnar, A.; Szabo, M.; Kortvelyesi, T.; Varga, A.; Molnár, P.; Tóth, G. Modulation of multidrug resistance and apoptosis of cancer cells by selected carotenoids. In Vivo 2004, 18, 237-244. (Pubitemid 38489008)
15. Guengerich, F.P. Cytochrome P-450 3A4: Regulation and role in drug metabolism. Annu. Rev. Pharmacol. Toxicol. 1999, 39, 1-17. (Pubitemid 29222549)
16. Moore, L.B.; Goodwin, B.; Jones, S.A.; Wisely, G.B.; Serabjit-Singh, C.J.; Willson, T.M.; Collins, J.L.; Kliewer, S.A. St. John's wort induces hepatic drug metabolism through activation of the pregnane X receptor. Proc. Natl. Acad. Sci. USA 2000, 97, 7500-7502.
17. Ambudkar, S.V.; Kimchi-Sarfaty, C.; Sauna, Z.E.; Gottesman, M.M. P-glycoprotein: From genomics to mechanism. Oncogene 2003, 22, 7468-7485. (Pubitemid 37487170)
18. Cole, S.P.; Bhardwaj, G.; Gerlach, J.H.; Mackie, J.E.; Grant, C.E.; Almquist, K.C.; Stewart, A.J.; Kurz, E.U.; Duncan, A.M.; Deeley, R.G. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992, 258, 1650-1654. (Pubitemid 23012438)
19. Sharma, R.C.; Inoue, S.; Roitelman, J.; Schimke, R.T.; Simoni, R.D. Peptide transport by the multidrug resistance pump. J. Biol. Chem. 1992, 267, 5731-5734.
20. Tsuruo, T.; Naito, M.; Tomida, A.; Fujita, N.; Mashima, T.; Sakamoto, H.; Haga, N. Molecular targeting therapy of cancer: Drug resistance, apoptosis and survival signal. Cancer Sci. 2003, 94, 15-21. (Pubitemid 36575852)
21. Biswas, A.; Mani, S.; Redinbo, M.R.; Krasowski, M.D.; Li, H.; Ekins, S. Elucidating the "Jekyl and Hyde" nature of PXR: The case for discovering antagonists or Allosteric antagonists. Pharm. Res. 2009, 26, 1807-1815.
22. Mukherjee, S.; Mani, S. Orphan nuclear receptors as targets for drug development. Pharm. Res. 2010, 27, 1439-1468.
23. Kliewer, S.A.; Moore, J.T.; Wade, L.; Staudinger, J.L.; Watson, M.A.; Jones, S.A.; McKee, D.D.; Oliver, B.B.; Willson, T.M.; Zetterström, R.H.; Perlmann, T.; Lehmann, J.M. An orphan nuclear receptor activated by pregnanes defines a novel steroid signaling pathway. Cell 1998, 92, 73-82. (Pubitemid 28053299)
24. Kliewer, S.A.; Goodwin, B.; Willson, T.M. The nuclear pregnane X receptor: A key regulator of xenobiotic metabolism. Endocr. Rev. 2002, 23, 687-702. (Pubitemid 35191629)
25. Gollamudi, R.; Gupta, D.; Goel, S.; Mani, S. Novel orphan nuclear receptors-coregulator interactions controlling anti-cancer drug metabolism. Curr. Drug Metab. 2008, 9, 611-613.
26. Wang, H.; Venkatesh, M.; Li, H.; Goetz, R.; Mukherjee, S.; Biswas, A.; Zhu, L.; Kaubisch, A.; Wang, L.; Pullman, J.; Whitney, K.; Kuro, M.; Roig, A.I.; Shay, J.W.; Mohammadi, M.; Mani, S. Pregnane X receptor activation induces FGF19-dependent tumor aggressiveness in humans and mice. J. Clin. Invest. 2011, 121, 3220-3232.
27. Miki, Y.; Suzuki, T.; Kitada, K.; Yabuki, N.; Shibuya, R.; Moriya, T.; Takanori, I.; Noriaki, O.; Bruce, B.; Hironobu, S. Expression of the steroid and xenobiotic receptor and its possible target gene, organic anion transporting polypeptide-A, in human breast carcinoma. Cancer Res. 2006, 66, 535-542.
28. Chen, Y.; Nie, D. Pregnane X receptor and its potential role in drug resistance in cancer treatment. Recent Pat. Anticancer Drug Discov. 2009, 4, 19-27.
29. Blumberg, B.; Sabbagh, W., Jr.; Juguilon, H.; Bolado, J., Jr.; van Meter, C.M.; Ong, E.S.; Evans, R.M. SXR, a novel steroid and xenobiotic-sensing nuclear receptor. Genes Dev. 1998, 12, 3195-3205. (Pubitemid 28496264)
30. Dussault, I.; Forman, B.M. The nuclear receptor PXR: A master regulator of "homeland" defense. Crit. Rev. Eukaryot. Gene Expr. 2002, 12, 53-64. (Pubitemid 35239413)
31. Synold, T.W.; Dussault, I.; Forman, B.M. The orphan nuclear receptor SXR coordinately regulates drug metabolism and efflux. Nat. Med. 2001, 7, 584-590. (Pubitemid 32448326)
32. Glass, C.K.; Rosenfeld, M.G. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 2000, 14, 121-141. (Pubitemid 30070977)
33. Bertilsson, G.; Heidrich, J.; Svensson, K.; Asman, M.; Jendeberg, L.; Sydow-Backman, M.; Ohlsson, R.; Postlind, H.; Blomquist, P.; Berkenstam, A. Identification of a human nuclear receptor defines a new signaling pathway for CYP3A induction. Proc. Natl. Acad. Sci. USA 1998, 95, 12208-12213. (Pubitemid 28483744)
34. Goodwin, B.; Hodgson, E.; Liddle, C. The orphan human pregnane X receptor mediates the transcriptional activation of CYP3A4 by rifampicin through a distal enhancer module. Mol. Pharmacol. 1999, 56, 1329-1339.
35. Pavek, P.; Dvorak, Z. Xenobiotic-induced transcriptional regulation of xenobiotic metabolizing enzymes of the cytochrome P450 superfamily in human extrahepatic tissues. Curr. Drug Metab. 2008, 9, 129-143. (Pubitemid 351461002)
36. Moore, L.B.; Parks, D.J.; Jones, S.A.; Bledsoe, R.K.; Consler, T.G.; Stimmel, J.B.; Goodwin, B.; Liddle, C.; Blanchard, S.G.; Willson, T.M.; Collins, J.L.; Kliewer, S.A. Orphan nuclear receptors constitutive androstane receptor and pregnane X receptor share xenobiotic and steroid ligands. J. Biol. Chem. 2000, 275, 15122-15127. (Pubitemid 30337234)
37. Kliewer, S.A.; Willson, T.M. Regulation of xenobiotic and bile acid metabolism by the nuclear pregnane X receptor. J. Lipid Res. 2002, 43, 359-364. (Pubitemid 34252265)
38. Auerbach, S.S.; Stoner, M.A.; Su, S.; Omiecinski, C.J. Retinoid X receptor-alpha-dependent transactivation by a naturally occurring structural variant of human constitutive androstane receptor (NR1I3). Mol. Pharmacol. 2005, 68, 1239-1253. (Pubitemid 41539981)
39. Li, Y.; Wang, Q.; Yao, X. Induction of CYP3A4 and MDR1 gene expression by baicalin, baicalein, chlorogenic acid, and ginsenoside Rf through constitutive androstane receptor- and pregnane X receptor-mediated pathways. Eur. J. Pharmacol. 2010, 640, 46-54.
40. Huang, H.; Wang, H.; Sinz, M.; Zoeckler, M.; Staudinger, J.; Redinbo, M.R.; Teotico, D.G.; Locker, J.; Kalpana, G.V.; Mani, S. Inhibition of drug metabolism by blocking the activation of nuclear receptors by ketoconazole. Oncogene 2007, 26, 258-268. (Pubitemid 46095736)
41. Healan-Greenberg, C.; Waring, J.F.; Kempf, D.J.; Blomme, E.A.; Tirona, R.G.; Kim, R.B. A human immunodeficiency virus protease inhibitor is a novel functional inhibitor of human pregnane X receptor. Drug Metab. Dispos. 2007, 36, 500-507.
42. Wang, H.; Li, H.; Moore, L.B.; Johnson, M.D.; Maglich, J.M.; Goodwin, B.; Parks, D.J.; Collins, J.L.; Willson, T.M.; Kalpana, G.V.; Venkatesh, M.; Xie, W.; Cho, S.Y.; Roboz, J.; Redinbo, M.; Moore, J.T.; Mani, S. The phytoestrogen coumestrol is a naturally occurring antagonist of the human pregnane X receptor. Mol. Endocrinol. 2008, 22, 838-857. (Pubitemid 351482821)
43. Chen, Y.; Tang, Y.; Robbins, G.T.; Nie, D. Camptothecin attenuates cytochrome P450 3A4 induction by blocking the activation of human pregnane X receptor. J. Pharmacol. Exp. Ther. 2010, 334, 999-1008.
44. Krausova, L.; Stejskalova, L.; Wang, H.; Vrzal, R.; Dvorak, Z.; Mani, S.; Pavek, P. Metformin suppresses pregnane X receptor (PXR)-regulated transactivation of CYP3A4 gene. Biochem. Pharmcol. 2011, 82, 1771-1780.
45. Zhou, C.; Poulton, E.J.; Grun, F.; Bammler, T.K.; Blumberg, B.; Thummel, K.E.; Eaton, D.L. The dietary isothiocyanate sulforaphane is an antagonist of the human steroid and xenobiotic nuclear receptor. Mol. Pharmacol. 2007, 71, 220-229. (Pubitemid 46020992)
46. Liu, C.L.; Huang, Y.S.; Hosokawa, M.; Miyashita, K.; Hu, M.L. Inhibition of proliferation of a hepatoma cell line by fucoxanthin in relation to cell cycle arrest and enhanced gap junctional intercellular communication. Chem. Biol. Interact. 2009, 182, 165-172.
47. Lin, C.Y.; Huang, C.S.; Hu, M.L. The use of fetal bovine serum as delivery vehicle to improve the uptake and stability of lycopene in cell culture studies. Br. J. Nutr. 2007, 98, 226-232.
48. Lim, Y.P.; Liu, C.H.; Shyu, L.J.; Huang, J.D. Functional characterization of a novel polymorphism of pregnane X receptor, Q158K, in Chinese subjects. Pharmacogenet. Genomics 2005, 15, 337-441.
49. Lim, Y.P.; Huang, J.D. Pregnane X receptor polymorphism affects CYP3A4 induction via a ligand-dependent interaction with steroid receptor coactivator-1. Pharmacogenet. Genomics 2007, 17, 369-382.