A novel xenobiotic responsive element regulated by aryl hydrocarbon receptor is involved in the induction of BCRP/ABCG2 in LS174T cells

Biochemical Pharmacology

Volumn 80, Issue 11, 2010, Pages 1754-1761

  Tompkins, Leslie M ^a   Li, Haishan ^a   Li, Linhao ^a   Lynch, Caitlin ^a   Xie, Yi ^b   Nakanishi, Takeo ^e   Ross, Douglas D ^b,c,d   Wang, Hongbing ^a,c  

^a UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d BALTIMORE VA MEDICAL CENTER   (United States)

^e KANAZAWA UNIVERSITY   (Japan)

Author keywords

AhR; BCRP; Induction; Regulation; Transporter

Indexed keywords

3 METHYLCHOLANTHRENE; AROMATIC HYDROCARBON RECEPTOR; BREAST CANCER RESISTANCE PROTEIN; CLOFIBRATE; LUCIFERASE; OMEPRAZOLE; RESVERATROL; TROGLITAZONE; ABC TRANSPORTER; ABCG2 PROTEIN, HUMAN; AHR PROTEIN, HUMAN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GINKGO BILOBA EXTRACT 761; PLANT EXTRACT; TUMOR PROTEIN; XENOBIOTIC AGENT;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; COLON ADENOCARCINOMA; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION INITIATION; UPREGULATION; XENOBIOTIC METABOLISM; BIOSYNTHESIS; COMPARATIVE STUDY; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; GENE SILENCING; GENETICS; PHYSIOLOGY; TUMOR CELL LINE;

ATP-BINDING CASSETTE TRANSPORTERS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE, TUMOR; GENE KNOCKDOWN TECHNIQUES; HUMANS; METHYLCHOLANTHRENE; NEOPLASM PROTEINS; PLANT EXTRACTS; RECEPTORS, ARYL HYDROCARBON; RESPONSE ELEMENTS; TRANSCRIPTIONAL ACTIVATION; XENOBIOTICS;

EID: 77957905037     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.08.016     Document Type: Article

References (36)

1. Gottesman M.M., Fojo T., Bates S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002, 2:48.
2. Hardwick L.J., Velamakanni S., van Veen H.W. The emerging pharmacotherapeutic significance of the breast cancer resistance protein (ABCG2). Br J Pharmacol 2007, 151:163-174.
3. Maliepaard M., Scheffer G.L., Faneyte I.F., van Gastelen M.A., Pijnenborg A.C.L.M., Schinkel A.H., et al. Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res 2001, 61:3458-3464.
4. Bunting K.D. ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 2002, 20:11-20.
5. Doyle L.A., Yang W., Abruzzo L.V., Krogmann T., Gao Y., Rishi A.K., et al. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 1998, 95:15665-15670.
6. Chen Z.S., Robey R.W., Belinsky M.G., Shchaveleva I., Ren X.Q., Sugimoto Y., et al. Transport of methotrexate, methotrexate polyglutamates, and 17beta-estradiol 17-(beta-d-glucuronide) by ABCG2: effects of acquired mutations at R482 on methotrexate transport. Cancer Res 2003, 63:4048-4054.
7. Ebert B., Seidel A., Lampen A. Identification of BCRP as transporter of benzo[a]pyrene conjugates metabolically formed in Caco-2 cells and its induction by Ah-receptor agonists. Carcinogenesis 2005, 26:1754-1763.
8. Kruijtzer C.M.F., Beijnen J.H., Rosing H., ten Bokkel Huinink W.W., Schot M., Jewell R.C., et al. Increased oral bioavailability of topotecan in combination with the breast cancer resistance protein and P-glycoprotein inhibitor GF120918. J Clin Oncol 2002, 20:2943-2950.
9. Ejendal K.F., Hrycyna C.A. Multidrug resistance and cancer: the role of the human ABC transporter ABCG2. Curr Protein Peptide Sci 2002, 3:503-511.
10. Bailey-Dell K.J., Hassel B., Doyle L.A., Ross D.D. Promoter characterization and genomic organization of the human breast cancer resistance protein (ATP-binding cassette transporter G2) gene. Biochim Biophys Acta 2001, 1520:234-241.
11. Krishnamurthy P., Ross D.D., Nakanishi T., Bailey-Dell K., Zhou S., Mercer K.E., et al. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 2004, 279:24218-24225.
12. Ee P.L.R., Kamalakaran S., Tonetti D., He X., Ross D.D., Beck W.T. Identification of a novel estrogen response element in the breast cancer resistance protein (ABCG2) gene. Cancer Res 2004, 64:1247-1251.
13. Szatmari I., Vamosi G., Brazda P., Balint B.L., Benko S., Szeles L., et al. Peroxisome proliferator-activated receptor {gamma}-regulated ABCG2 expression confers cytoprotection to human dendritic cells. J Biol Chem 2006, 281:23812-23823.
14. Jigorel E., Le Vee M., Boursier-Neyret C., Parmentier Y., Fardel O. Differential regulation of sinusoidal and canalicular hepatic drug transporter expression by xenobiotics activating drug-sensing receptors in primary human hepatocytes. Drug Metab Dispos 2006, 34:1756-1763.
15. Burger H., van Tol H., Brok M., Wiemer E.A., de Bruijn E.A., Guetens G., et al. Chronic imatinib mesylate exposure leads to reduced intracellular drug accumulation by induction of the ABCG2 (BCRP) and ABCB1 (MDR1) drug transport pumps. Cancer Biol Ther 2005, 4:747-752.
16. Ebert B., Seidel A., Lampen A. Phytochemicals induce breast cancer resistance protein in Caco-2 cells and enhance the transport of benzo[a]pyrene-3-sulfate. Toxicol Sci 2007, 96:227-236.
17. Wang H., Zhou L., Gupta A., Vethanayagam R.R., Zhang Y., Unadkat J.D., et al. Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells. Am J Physiol Endocrinol Metab 2006, 290:E798-E807.
18. Phelan D., Winter G.M., Rogers W.J., Lam J.C., Denison M.S. Activation of the Ah receptor signal transduction pathway by bilirubin and biliverdin. Arch Biochem Biophys 1998, 357:155-163.
19. Quattrochi L.C., Tukey R.H. Nuclear uptake of the Ah (dioxin) receptor in response to omeprazole: transcriptional activation of the human CYP1A1 gene. Mol Pharmacol 1993, 43:504-508.
20. Li L., Stanton J.D., Tolson A.H., Luo Y., Wang H. 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 2009, 26:872-882.
21. Knight B., Troutman M., Thakker D.R. Deconvoluting the effects of P-glycoprotein on intestinal CYP3A: a major challenge. Curr Opin Pharmacol 2006, 6:528-532.
22. Benet L.Z. The drug transporter-metabolism alliance: uncovering and defining the interplay. Mol Pharm 2009, 6:1631-1643.
23. Gehm B.D., McAndrews J.M., Chien P.Y., Jameson J.L. Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. Proc Natl Acad Sci USA 1997, 94:14138-14143.
24. Chen C.Y., Jang J.H., Li M.H., Surh Y.J. Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells. Biochem Biophys Res Commun 2005, 331:993-1000.
25. Hankinson O. The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacool. Toxicol. 1995, 35:307-340.
26. Tan K.P., Wang B., Yang M., Boutros P.C., Macaulay J., Xu H., et al. Aryl hydrocarbon receptor is a transcriptional activator of the human breast cancer resistance protein (BCRP/ABCG2). Mol Pharmacol 2010, 78:175-185.
27. Burbach K.M., Poland A., Bradfield C.A. Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor. Proc Natl Acad Sci USA 1992, 89:8185-8189.
28. Yueh M.F., Huang Y.H., Hiller A., Chen S., Nguyen N., Tukey R.H. Involvement of the xenobiotic response element (XRE) in Ah receptor-mediated induction of human UDP-glucuronosyltransferase 1A1. J Biological Chem 2003, 278:15001-15006.
29. Erichsen T.J., Ehmer U., Kalthoff S., Lankisch T.O., Muller T.M., Munzel P.A., et al. Genetic variability of aryl hydrocarbon receptor (AhR)-mediated regulation of the human UDP glucuronosyltransferase (UGT) 1A4 gene. Toxicol Appl Pharmacol 2008, 230:252-260.
30. Sugatani J., Kojima H., Ueda A., Kakizaki S., Yoshinari K., Gong Q.H., et al. The phenobarbital response enhancer module in the human bilirubin UDP-glucuronosyltransferase UGT1A1 gene and regulation by the nuclear receptor CAR. Hepatology (Baltimore, MD) 2001, 33:1232-1238.
31. Xie W., Yeuh M.F., Radominska-Pandya A., Saini S.P., Negishi Y., Bottroff B.S., et al. Control of steroid, heme, and carcinogen metabolism by nuclear pregnane X receptor and constitutive androstane receptor. Proc Natl Acad Sci USA 2003, 100:4150-4155.
32. Imai Y., Ishikawa E., Asada S., Sugimoto Y. Estrogen-mediated post transcriptional down-regulation of breast cancer resistance protein/ABCG2. Cancer Res 2005, 65:596-604.
33. 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.
34. Casper R.F., Quesne M., Rogers I.M., Shirota T., Jolivet A., Milgrom E., et al. Resveratrol has antagonist activity on the aryl hydrocarbon receptor: implications for prevention of dioxin toxicity. Mol Pharmacol 1999, 56:784-790.
35. Klinge C.M., Kaur K., Swanson H.I. The aryl hydrocarbon receptor interacts with estrogen receptor alpha and orphan receptors COUP-TFI and ERRalpha1. Arch Biochem Biophys 2000, 373:163-174.
36. Yeager R.L., Reisman S.A., Aleksunes L.M., Klaassen C.D. Introducing the " TCDD-inducible AhR-Nrf2 gene battery" Toxicol Sci 2009, 111:238-246.