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

Volumn 87, Issue 9, 2009, Pages 674-683

  Rajaraman, Ganesh ^a,b   Yang, Guixiang ^a   Chen, Jie ^a   Chang, Thomas K H ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CellzDirect Inc   (United States)

Author keywords

Aryl hydrocarbon receptor; Bilobalide; CYP1A1; CYP1B1; Ginkgo biloba; Ginkgolide; Isorhamnetin; Kaempferol; Quercetin

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; BILOBALIDE; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; ETHOXYRESORUFIN; FLAVONE DERIVATIVE; GINKGO BILOBA EXTRACT; GINKGOLIDE A; GINKGOLIDE B; GINKGOLIDE C; GINKGOLIDE J; ISORHAMNETIN; KAEMPFEROL; LUCIFERASE; MESSENGER RNA; QUERCETIN;

ARTICLE; CELL STRAIN; CELL VIABILITY; CHEMICAL CARCINOGENESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEALKYLATION; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; PLASMID; PRIORITY JOURNAL; REPORTER GENE;

CELL CULTURE TECHNIQUES; CELL LINE; CELL SURVIVAL; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 ENZYME SYSTEM; DNA, COMPLEMENTARY; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; GENES, REPORTER; GINKGO BILOBA; HUMANS; LUCIFERASES, FIREFLY; LUCIFERASES, RENILLA; PLANT EXTRACTS; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; TRANSFECTION;

EID: 70349297460     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/Y09-061     Document Type: Article

References (38)

1. Beischlag, T.V., Luis Morales, J., Hollingshead, B.D., and Perdew, G.H. 2008. The aryl hydrocarbon receptor complex and the control of gene expression. Crit. Rev. Eukaryot. Gene Expr. 18(3): 207-250. PMID:18540824.
2. Belous, A.R., Hachey, D.L., Dawling, S., Roodi, N., and Parl, F.F. 2007. Cytochrome P450 1B1-mediated estrogen metabolism results in estrogen- deoxyribonucleoside adduct formation. Cancer Res. 67(2): 812-817. doi:10.1158/0008-5472.CAN-06-2133. PMID:17234793. (Pubitemid 46192222)
3. Bièche, I., Narjoz, C., Asselah, T., Vacher, S., Marcellin, P., Lidereau, R., et al. 2007. Reverse transcriptase-PCR quantification of mRNA levels from cytochrome (CYP)1, CYP2 and CYP3 families in 22 different human tissues. Pharmacogenet. Genomics, 17(9): 731-742. doi:10.1097/FPC. 0b013e32810f2e58. PMID: 17700362.
4. Cermak, R., and Wolffram, S. 2006. The potential of flavonoids to influence drug metabolism and pharmacokinetics by local gastrointestinal mechanisms. Curr. Drug Metab. 7(7): 729-744. doi:10.2174/138920006778520570. PMID:17073577.
5. Chang, T.K.H., Lee, W.B.K., and Ko, H.H. 2000. Trans-resveratrol modulates the catalytic activity and mRNA expression of the procarcinogen- activating human cytochrome P450 1B1. Can. J. Physiol. Pharmacol. 78(11): 874-881. doi:10.1139/cjpp-78-11-874. PMID:11100935.
6. Chang, T.K.H., Chen, J., and Lee, W.B.K. 2001. Differential inhibition and inactivation of human CYP1 enzymes by trans-resveratrol: evidence for mechanism-based inactivation of CYP1A2. J. Pharmacol. Exp. Ther. 299(3): 874-882. PMID: 11714871.
7. Chang, T.K.H., Chen, J., Pillay, V., Ho, J.Y., and Bandiera, S.M. 2003. Real-time polymerase chain reaction analysis of CYP1B1 gene expression in human liver. Toxicol. Sci. 71(1): 11-19. doi:10.1093/toxsci/71.1.11. PMID:12520071.
8. Chang, T.K.H., Chen, J., and Teng, X.W. 2006a. Distinct role of bilobalide and ginkgolide A in the modulation of rat CYP2B1 and CYP3A23 gene expression by Ginkgo biloba extract in cultured hepatocytes. Drug Metab. Dispos. 34(2): 234-242. doi:10.1124/dmd.105.005751. PMID:16258077.
9. Chang, T.K.H., Chen, J., and Yeung, E.Y.H. 2006b. Effect of Ginkgo biloba extract on procarcinogen-bioactivating human CYP1 enzymes: identification of isorhamnetin, kaempferol, and quercetin as potent inhibitors of CYP1B1. Toxicol. Appl. Pharmacol. 213(1): 18-26. doi:10.1016/j.taap.2005.09.007. PMID: 16226778.
10. Chen, Y.H., Beischlag, T.V., Kim, J.H., Perdew, G.H., and Stallcup, M.R. 2006. Role of GAC63 in transcriptional activation mediated by the aryl hydrocarbon receptor. J. Biol. Chem. 281(18): 12242-12247. doi:10.1074/jbc. M512537200. PMID: 16513642.
11. Ciolino, H.P., Daschner, P.J., and Yeh, G.C. 1998. Resveratrol inhibits transcription of CYP1A1 in vitro by preventing activation of the aryl hydrocarbon receptor. Cancer Res. 58(24): 5707-5712. PMID:9865727.
12. Denison, M.S., and Nagy, S.R. 2003. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol. 43(1): 309-334. doi:10.1146/annurev.pharmtox.43.100901. 135828. PMID: 12540743.
13. Donato, M.T., Gómez-Lechón, M.J., and Castell, J.V. 1993. A microassay for measuring cytochrome P450IA1 and P450IIB1 activities in intact human and rat hepatocytes cultured on 96-well plates. Anal. Biochem. 213(1): 29-33. doi:10.1006/abio.1993.1381. PMID:8238878.
14. Guengerich, F.P., Chun, Y.J., Kim, D., Gillam, E.M.J., and Shimada, T. 2003. Cytochrome P450 1B1: a target for inhibition in anticarcinogenesis strategies. Mutat. Res. 523-524: 173-182. doi:10.1016/S0027-5107(02)00333-0. PMID:12628515.
15. Hahn, M.E., Allan, L.L., and Sherr, D.H. 2009. Regulation of constitutive and inducible AHR signaling: complex interactions involving the AHR repressor. Biochem. Pharmacol. 77(4): 485-497. doi:10.1016/j.bcp.2008.09.016. PMID:18848529.
16. Huang, Z., Fasco, M.J., Figge, H.L., Keyomarsi, K., and Kaminsky, L.S. 1996. Expression of cytochromes P450 in human breast tissue and tumors. Drug Metab. Dispos. 24(8): 899-905. PMID: 8869826.
17. Jeuken, A., Keser, B.J.G., Khan, E., Brouwer, A., Koeman, J., and Denison, M.S. 2003. Activation of the Ah receptor by extracts of dietary herbal supplements, vegetables, and fruits. J. Agric. Food Chem. 51(18): 5478-5487. doi:10.1021/jf030252u. PMID: 12926901.
18. +-ATPase inhibitors and other xenobiotics. Xenobiotica, 33(2): 107-118. doi:10.1080/0049825021000023978. PMID:12623754.
19. Lee, J.E., and Safe, S. 2000. 3′,4′-Dimethoxyflavone as an aryl hydrocarbon receptor antagonist in human breast cancer cells. Toxicol. Sci. 58(2): 235-242. doi:10.1093/toxsci/58.2.235. PMID: 11099636.
20. Li, L., Stanton, J.D., Tolson, A.H., Luo, Y., and Wang, H. 2009. 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. Pharm. Res. 26(4): 872-882. doi:10.1007/s11095-008-9788-8. PMID: 19034627.
21. Lin, P., Hu, S.W., and Chang, T.H. 2003. Correlation between gene expression of aryl hydrocarbon receptor (AhR), hydrocarbon receptor nuclear translocator (Arnt), cytochromes P4501A1 (CYP1A1) and 1B1 (CYP1B1), and inducibility of CYP1A1 and CYP1B1 in human lymphocytes. Toxicol. Sci. 71(1): 20-26. doi:10.1093/toxsci/71.1.20. PMID:12520072. (Pubitemid 36163702)
22. MacDonald, C.J., Ciolino, H.P., and Yeh, G.C. 2001. Dibenzoylmethane modulates aryl hydrocarbon receptor function and expression of cytochromes P50 1A1, 1A2, and 1B1. Cancer Res. 61(10): 3919-3924. PMID:11358806.
23. McFadyen, M.C.E., Melvin, W.T., and Murray, G.I. 2004. Cytochrome P450 enzymes: novel options for cancer therapeutics. Mol. Cancer Ther. 3(3): 363-371. PMID:15026557.
24. Mense, S.M., Chhabra, J., and Bhat, H.K. 2008. Preferential induction of cytochrome P450 1A1 over cytochrome P450 1B1 in human breast epithelial cells following exposure to quercetin. J. Steroid Biochem. Mol. Biol. 110(1-2): 157-162. doi:10.1016/j.jsbmb.2008.03.029. PMID:18456490.
25. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65(1-2): 55-63. doi:10.1016/0022-1759(83)90303-4. PMID:6606682.
26. Murray, G.I., Taylor, M.C., McFadyen, M.C.E., McKay, J.A., Greenlee, W.F., Burke, M.D., and Melvin, W.T. 1997. Tumor-specific expression of cytochrome P450 CYP1B1. Cancer Res. 57(14): 3026-3031. PMID:9230218. (Pubitemid 27315056)
27. Nakanishi, K. 2005. Terpene trilactones from Gingko biloba: from ancient times to the 21st century. Bioorg. Med. Chem. 13(17): 4987-5000. doi:10.1016/j.bmc.2005.06.014. PMID:15990319.
28. Nebert, D.W., and Dalton, T.P. 2006. The role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nat. Rev. Cancer, 6(12): 947-960. doi:10.1038/nrc2015. PMID:17128211.
29. Oh, S.M., and Chung, K.H. 2006. Antiestrogenic activities of Ginkgo biloba extracts. J. Steroid Biochem. Mol. Biol. 100(4-5): 167-176. doi:10.1016/j.jsbmb.2006.04.007. PMID:16842996.
30. Puppala, D., Gairola, C.G., and Swanson, H.I. 2007. Identification of kaempferol as an inhibitor of cigarette smoke-induced activation of the aryl hydrocarbon receptor and cell transformation. Carcinogenesis, 28(3): 639-647. doi:10.1093/carcin/bgl169. PMID:17012224. (Pubitemid 46523359)
31. Rajaraman, G., Chen, J., and Chang, T.K.H. 2006. Ginkgolide A contributes to the potentiation of acetaminophen toxicity by Ginkgo biloba extract in primary cultures of rat hepatocytes. Toxicol. Appl. Pharmacol. 217(2): 225-233. doi:10.1016/j.taap.2006.09.005. PMID:17045319.
32. Ramassamy, C., Longpré, F., and Christen, Y. 2007. Ginkgo biloba extract (EGb 761) in Alzheimer's disease: is there any evidence? Curr. Alzheimer Res. 4(3): 253-262. doi:10.2174/156720507781077304. PMID:17627482.
33. Shimada, T., Gillam, E.M., Sutter, T.R., Strickland, P.T., Guengerich, F.P., and Yamazaki, H. 1997. Oxidation of xenobiotics by recombinant human cytochrome P450 1B1. Drug Metab. Dispos. 25(5): 617-622.
34. 2+ in the MCF-10A human mammary epithelial cell line by carcinogenic polycyclic aromatic hydrocarbons. Mol. Carcinog. 25(1): 48-54. doi:10.1002/(SICI)1098-2744(199905)25:1〈48:: AID-MC6〉3.0.CO;2-6. PMID:10331744.
35. van Beek, T.A., and Montoro, P. 2009. Chemical analysis and quality control of Ginkgo biloba leaves, extracts, and phytopharmaceuticals. J. Chromatogr. A, 1216(11): 2002-2032. doi:10.1016/j.chroma.2009.01.013. PMID:19195661.
36. Wu, M.L., Li, H., Wu, D.C., Wang, X.W., Chen, X.Y., Kong, Q.Y., et al. 2005. CYP1A1 and CYP1B1 expressions in medulloblastoma cells are AhR-independent and have no direct link with resveratrol-induced differentiation and apoptosis. Neurosci. Lett. 384(1-2): 33-37. doi:10.1016/j.neulet.2005.04.055. PMID: 15893423.
37. Yang, X., Solomon, S., Fraser, L.R., Trombino, A.F., Liu, D., Sonenshein, G.E., et al. 2008. Constitutive regulation of CYP1B1 by the aryl hydrocarbon receptor (AhR) in pre-malignant and malignant mammary tissue. J. Cell. Biochem. 104(2): 402-417. doi:10.1002/jcb.21630. PMID:18059014.
38. Zhang, S., Qin, C., and Safe, S.H. 2003. Flavonoids as aryl hydrocarbon receptor agonists/antagonists: effects of structure and cell context. Environ. Health Perspect. 111(16): 1877-1882. PMID: 14644660.