Induction of cytochromes P450 1A1 and 1A2 by tanshinones in human HepG2 hepatoma cell line

Toxicology and Applied Pharmacology

Volumn 252, Issue 1, 2011, Pages 18-27

  Zhang, Rong ^a   Sun, Jianguo ^a   Ma, Liping ^a   Wu, Xiaolan ^a   Pan, Guoyu ^b   Hao, Haiping ^a   Zhou, Fang ^a   A, Jiye ^a   Liu, Changhui ^a   Ai, Hua ^a   Shang, Lili ^a   Gao, Haiyan ^a   Peng, Ying ^a   Wan, Ping ^a   Wu, Hui ^a   Wang, Guangji ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

AhR; CYP1A1; CYP1A2; Induction; Tanshinone

Indexed keywords

BENZO[A]PYRENE; CRYPTOTANSHINONE; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; DACTINOMYCIN; DIHYDROTANSHINONE I; LUCIFERASE; MESSENGER RNA; NUCLEAR RNA; RESVERATROL; TANSHINONE; TANSHINONE I; TANSHINONE IIA; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN HEPG2; CONCENTRATION RESPONSE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1A2; DITERPENES, ABIETANE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUGS, CHINESE HERBAL; ENZYME INDUCTION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEP G2 CELLS; HUMANS;

EID: 79952608593     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.01.008     Document Type: Article

References (67)

1. Beedanagari S.R., Bebenek I., Bui P., Hankinson O. Resveratrol inhibits dioxin-induced expression of human CYP1A1 and CYP1B1 by inhibiting recruitment of the Aryl Hydrocarbon Receptor complex and RNA Polymerase II to the regulatory regions of the corresponding genes. Toxicol. Sci. 2009, 110:61-67.
2. Cao E.H., Liu X.Q., Wang J.J., Xu N.F. Effect of natural antioxidant tanshinone II-A on DNA damage by lipid peroxidation in liver cells. Free Radic. Biol. Med. 1996, 20:801-806.
3. Chang T.K., Chen J., Pillay V., Ho J.Y., Bandiera S.M. Real-time polymerase chain reaction analysis of CYP1B1 gene expression in human liver. Toxicol. Sci. 2003, 71:11-19.
4. Chen Y., Tu J.H., He Y.J., Zhang W., Wang G., Tan Z.R., Zhou G., Fan L., Zhou H.H. Effect of sodium tanshinone II A sulfonate on the activity of CYP1A2 in healthy volunteers. Xenobiotica 2009, 39:508-513.
5. Chen, W., Luo, Y., Liu, L., Zhou, H., Xu, B., Han, X., Shen, T., Liu, Z., Lu, Y., Huang, S., 2010. Cryptotanshinone inhibits cancer cell proliferation by suppressing mammalian target of rapamycin-mediated cyclin d1 expression and rb phosphorylation. Cancer Prev Res (Phila) 3, 1015-1025.
6. Cheng T.O. Cardiovascular effects of danshen. Int. J. Cardiol. 2007, 121:9-22.
7. Ciolino H.P., Yeh G.C. Inhibition of aryl hydrocarbon-induced cytochrome P-450 1A1 enzyme activity and CYP1A1 expression by resveratrol. Mol. Pharmacol. 1999, 56:760-767.
8. 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.
9. Ciolino H.P., Daschner P.J., Yeh G.C. Resveratrol inhibits transcription of CYP1A1 in vitro by preventing activation of the aryl hydrocarbon receptor. Cancer Res. 1998, 58:5707-5712.
10. 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. Biochem. J. 1999, 340(Pt 3):715-722.
11. Delescluse C., Lemaire G., de Sousa G., Rahmani R. Is CYP1A1 induction always related to AHR signaling pathway?. Toxicology 2000, 153:73-82.
12. Dvorak Z., Vrzal R., Henklova P., Jancova P., Anzenbacherova E., Maurel P., Svecova L., Pavek P., Ehrmann J., Havlik R., Bednar P., Lemr K., Ulrichova J. JNK inhibitor SP600125 is a partial agonist of human aryl hydrocarbon receptor and induces CYP1A1 and CYP1A2 genes in primary human hepatocytes. Biochem. Pharmacol. 2008, 75:580-588.
13. El Gendy M.A., El-Kadi A.O. Harman induces CYP1A1 enzyme through an aryl hydrocarbon receptor mechanism. Toxicol. Appl. Pharmacol. 2010, 249:55-64.
14. Elferink C.J., Reiners J.J. Quantitative RT-PCR on CYP1A1 heterogeneous nuclear RNA: a surrogate for the in vitro transcription run-on assay. Biotechniques 1996, 20:470-477.
15. Fan G.W., Gao X.M., Wang H., Zhu Y., Zhang J., Hu L.M., Su Y.F., Kang L.Y., Zhang B.L. The anti-inflammatory activities of Tanshinone IIA, an active component of TCM, are mediated by estrogen receptor activation and inhibition of iNOS. J. Steroid Biochem. Mol. Biol. 2009, 113:275-280.
16. Fontaine F., Delescluse C., de Sousa G., Lesca P., Rahmani R. Cytochrome 1A1 induction by primaquine in human hepatocytes and HepG2 cells: absence of binding to the aryl hydrocarbon receptor. Biochem. Pharmacol. 1999, 57:255-262.
17. Gong Y., Li Y., Lu Y., Li L., Abdolmaleky H., Blackburn G.L, Zhou J.R. Bioactive tanshinones in Salvia miltiorrhiza inhibit the growth of prostate cancer cells in vitro and in mice. Int. J. Cancer. 2010.
18. Guengerich F.P., Shimada T. Activation of procarcinogens by human cytochrome P450 enzymes. Mutat. Res. 1998, 400:201-213.
19. Hao H., Wang G., Cui N., Li J., Xie L., Ding Z. Pharmacokinetics, absorption and tissue distribution of tanshinone IIA solid dispersion. Planta Med. 2006, 72:1311-1317.
20. Hu W., Sorrentino C., Denison M.S., Kolaja K., Fielden M.R. Induction of cyp1a1 is a nonspecific biomarker of aryl hydrocarbon receptor activation: results of large scale screening of pharmaceuticals and toxicants in vivo and in vitro. Mol. Pharmacol. 2007, 71:1475-1486.
21. Hur J.M., Shim J.S., Jung H.J., Kwon H.J. Cryptotanshinone but not tanshinone IIA inhibits angiogenesis in vitro. Exp. Mol. Med. 2005, 37:133-137.
22. Kang B.Y., Chung S.W., Kim S.H., Ryu S.Y., Kim T.S. Inhibition of interleukin-12 and interferon-gamma production in immune cells by tanshinones from Salvia miltiorrhiza. Immunopharmacology 2000, 49:355-361.
23. Kikuchi H., Hossain A., Yoshida H., Kobayashi S. Induction of cytochrome P-450 1A1 by omeprazole in human HepG2 cells is protein tyrosine kinase-dependent and is not inhibited by alpha-naphthoflavone. Arch. Biochem. Biophys. 1998, 358:351-358.
24. Kuo Y.H., Lin Y.L., Don M.J., Chen R.M., Ueng Y.F. Induction of cytochrome P450-dependent monooxygenase by extracts of the medicinal herb Salvia miltiorrhiza. J. Pharm. Pharmacol. 2006, 58:521-527.
25. Le Ferrec E., Lagadic-Gossmann D., Rauch C., Bardiau C., Maheo K., Massiere F., Le Vee M., Guillouzo A., Morel F. Transcriptional induction of CYP1A1 by oltipraz in human Caco-2 cells is aryl hydrocarbon receptor- and calcium-dependent. J. Biol. Chem. 2002, 277:24780-24787.
26. Ledirac N., Delescluse C., de Sousa G., Pralavorio M., Lesca P., Amichot M., Berge J.B., Rahmani R. Carbaryl induces CYP1A1 gene expression in HepG2 and HaCaT cells but is not a ligand of the human hepatic Ah receptor. Toxicol. Appl. Pharmacol. 1997, 144:177-182.
27. Lee I.J., Jeong K.S., Roberts B.J., Kallarakal A.T., Fernandez-Salguero P., Gonzalez F.J., Song B.J. Transcriptional induction of the cytochrome P4501A1 gene by a thiazolium compound, YH439. Mol. Pharmacol. 1996, 49:980-988.
28. Lee C.Y., Sher H.F., Chen H.W., Liu C.C., Chen C.H., Lin C.S., Yang P.C., Tsay H.S., Chen J.J. Anticancer effects of tanshinone I in human non-small cell lung cancer. Mol. Cancer Ther. 2008, 7:3527-3538.
29. Lekas P., Tin K.L., Lee C., Prokipcak R.D. The human cytochrome P450 1A1 mRNA is rapidly degraded in HepG2 cells. Arch. Biochem. Biophys. 2000, 384:311-318.
30. Lewis D.F., Jacobs M.N., Dickins M., Lake B.G. Quantitative structure-activity relationships for inducers of cytochromes P450 and nuclear receptor ligands involved in P450 regulation within the CYP1, CYP2, CYP3 and CYP4 families. Toxicology 2002, 176:51-57.
31. Li X.X., Zhou Z.W., Zhou S.F. Role of P-glycoprotein in the transport of tanshinone I, one active triterpenoid from Salvia miltiorrhiza. Drug Metab. Lett. 2008, 2:223-230.
32. Lin P., Chang H., Tsai W.T., Wu M.H., Liao Y.S., Chen J.T., Su J.M. Overexpression of aryl hydrocarbon receptor in human lung carcinomas. Toxicol. Pathol. 2003, 31:22-30.
33. Lin P., Hu S.W., Chang T.H. 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. 2003, 71:20-26.
34. Liu D., Liu D., Tang H.F., Zhang S.H. Application of macroporous resin in purification for effective part from polygonum cuspidatum. Chin. J. Chin. Meter. Med. 2007, 32:1024-1027.
35. Lu Q., Zhang P., Zhang X., Chen J. Experimental study of the anti-cancer mechanism of tanshinone IIA against human breast cancer. Int. J. Mol. Med. 2009, 24:773-780.
36. Ma Q., Lu A.Y. CYP1A induction and human risk assessment: an evolving tale of in vitro and in vivo studies. Drug Metab. Dispos. 2007, 35:1009-1016.
37. MacDonald C.J., Ciolino H.P., Yeh G.C. Dibenzoylmethane modulates aryl hydrocarbon receptor function and expression of cytochromes P50 1A1, 1A2, and 1B1. Cancer Res. 2001, 61:3919-3924.
38. MacDonald C.J., Cheng R.Y., Roberts D.D., Wink D.A., Yeh G.C. Modulation of carcinogen metabolism by nitric oxide-aspirin 2 is associated with suppression of DNA damage and DNA adduct formation. J. Biol. Chem. 2009, 284:22099-22107.
39. Martignoni M., Groothuis G.M., de Kanter R. Species differences between mouse, rat, dog, monkey and human CYP-mediated drug metabolism, inhibition and induction. Expert Opin. Drug Metab. Toxicol. 2006, 2:875-894.
40. McFadyen M.C., Melvin W.T., Murray G.I. Cytochrome P450 enzymes: novel options for cancer therapeutics. Mol. Cancer Ther. 2004, 3:363-371.
41. Murray G.I., Melvin W.T., Greenlee W.F., Burke M.D. Regulation, function, and tissue-specific expression of cytochrome P450 CYP1B1. Annu. Rev. Pharmacol. Toxicol. 2001, 41:297-316.
42. Pradet-Balade B., Boulme F., Beug H., Mullner E.W., Garcia-Sanz J.A. Translation control: bridging the gap between genomics and proteomics?. Trends Biochem. Sci. 2001, 26:225-229.
43. Qiu F., Wang G., Zhao Y., Sun H., Mao G., A.J., Sun J. Effect of danshen extract on pharmacokinetics of theophylline in healthy volunteers. Br. J. Clin. Pharmacol. 2008, 65:270-274.
44. Qiu F., Zhang R., Sun J., Jiye A., Hao H., Peng Y., Ai H., Wang G. Inhibitory effects of seven components of danshen extract on catalytic activity of cytochrome P450 enzyme in human liver microsomes. Drug Metab. Dispos. 2008, 36:1308-1314.
45. Shih H., Pickwell G.V., Guenette D.K., Bilir B., Quattrochi L.C. Species differences in hepatocyte induction of CYP1A1 and CYP1A2 by omeprazole. Hum. Exp. Toxicol. 1999, 18:95-105.
46. Shin D.S., Kim H.N., Shin K.D., Yoon Y.J., Kim S.J., Han D.C., Kwon B.M. Cryptotanshinone inhibits constitutive signal transducer and activator of transcription 3 function through blocking the dimerization in DU145 prostate cancer cells. Cancer Res. 2009, 69:193-202.
47. Sinal C.J., Bend J.R. Aryl hydrocarbon receptor-dependent induction of cyp1a1 by bilirubin in mouse hepatoma hepa 1c1c7 cells. Mol. Pharmacol. 1997, 52:590-599.
48. Takahashi Y., Itoh S., Shimojima T., Kamataki T. Characterization of Ah receptor promoter in human liver cell line, HepG2. Pharmacogenetics 1994, 4:219-222.
49. Tian H., Ip L., Luo H., Chang D.C., Luo K.Q. A high throughput drug screen based on fluorescence resonance energy transfer (FRET) for anticancer activity of compounds from herbal medicine. Br. J. Pharmacol. 2007, 150:321-334.
50. Tsai S.L., Suk F.M., Wang C.I., Liu D.Z., Hou W.C., Lin P.J., Hung L.F., Liang Y.C. Anti-tumor potential of 15, 16-dihydrotanshinone I against breast adenocarcinoma through inducing G1 arrest and apoptosis. Biochem. Pharmacol. 2007, 74:1575-1586.
51. Ueng Y.F., Kuo Y.H., Peng H.C., Chen T.L., Jan W.C., Peter Guengerich F., Lin Y.L. Diterpene quinone tanshinone IIA selectively inhibits mouse and human cytochrome p4501A2. Xenobiotica 2003, 33:603-613.
52. Ueng Y.F., Kuo Y.H., Wang S.Y., Lin Y.L., Chen C.F. Induction of CYP1A by a diterpene quinone tanshinone IIA isolated from a medicinal herb Salvia miltiorrhiza in C57BL/6J but not in DBA/2J mice. Life Sci. 2004, 74:885-896.
53. Vakharia D.D., Liu N., Pause R., Fasco M., Bessette E., Zhang Q.Y., Kaminsky L.S. Polycyclic aromatic hydrocarbon/metal mixtures: effect on PAH induction of CYP1A1 in human HEPG2 cells. Drug Metab. Dispos. 2001, 29:999-1006.
54. Wang H.W., Chen T.L., Yang P.C., Ueng T.H. Induction of cytochromes P450 1A1 and 1B1 by emodin in human lung adenocarcinoma cell line CL5. Drug Metab. Dispos. 2001, 29:1229-1235.
55. Wang X., Wei Y., Yuan S., Liu G., Lu Y., Zhang J., Wang W. Potential anticancer activity of tanshinone IIA against human breast cancer. Int. J. Cancer 2005, 116:799-807.
56. Wang Y., Ye X., Ma Z., Liang Q., Lu B., Tan H., Xiao C., Zhang B., Gao Y. Induction of cytochrome P450 1A1 expression by ginsenoside Rg1 and Rb1 in HepG2 cells. Eur. J. Pharmacol. 2008, 601:73-78.
57. Wang X., Lee W.Y., Or P.M., Yeung J.H. Effects of major tanshinones isolated from danshen (Salvia miltiorrhiza) on rat CYP1A2 expression and metabolism of model CYP1A2 probe substrates. Phytomedicine 2009, 16:712-725.
58. Wen X., Walle U.K., Walle T. 5, 7-Dimethoxyflavone downregulates CYP1A1 expression and benzo[a]pyrene-induced DNA binding in Hep G2 cells. Carcinogenesis 2005, 26:803-809.
59. Westerink W.M., Schoonen W.G. Cytochrome P450 enzyme levels in HepG2 cells and cryopreserved primary human hepatocytes and their induction in HepG2 cells. Toxicol. In Vitro 2007, 21:1581-1591.
60. Whitlock J.P. Induction of cytochrome P4501A1. Annu. Rev. Pharmacol. Toxicol. 1999, 39:103-125.
61. Wilkening S., Stahl F., Bader A. Comparison of primary human hepatocytes and hepatoma cell line Hepg2 with regard to their biotransformation properties. Drug Metab. Dispos. 2003, 31:1035-1042.
62. Xu L., Li A.P., Kaminski D.L., Ruh M.F. 2, 3, 7, 8 Tetrachlorodibenzo-p-dioxin induction of cytochrome P4501A in cultured rat and human hepatocytes. Chem. Biol. Interact. 2000, 124:173-189.
63. Yang X.F., Wang N.P., Lu W.H., Zeng F.D. Effects of Ginkgo biloba extract and tanshinone on cytochrome P-450 isozymes and glutathione transferase in rats. Acta Pharmacol. Sin. 2003, 24:1033-1038.
64. Zhang S., Qin C., Safe S.H. Flavonoids as aryl hydrocarbon receptor agonists/antagonists: effects of structure and cell context. Environ. Health Perspect. 2003, 111:1877-1882.
65. Zhang J., Huang M., Guan S., Bi H.C., Pan Y., Duan W., Chan S.Y., Chen X., Hong Y.H., Bian J.S., Yang H.Y., Zhou S. A mechanistic study of the intestinal absorption of cryptotanshinone, the major active constituent of Salvia miltiorrhiza. J. Pharmacol. Exp. Ther. 2006, 317:1285-1294.
66. Zhou L., Zuo Z., Chow M.S. Danshen: an overview of its chemistry, pharmacology, pharmacokinetics, and clinical use. J. Clin. Pharmacol. 2005, 45:1345-1359.
67. Zhou S.F., Wang B., Yang L.P., Liu J.P. Structure, function, regulation and polymorphism and the clinical significance of human cytochrome P450 1A2. Drug Metab. Rev. 2009, 42:268-354.