Multidrug resistance protein (MRP) 4 attenuates benzo[a]pyrene-mediated DNA-adduct formation in human bronchoalveolar H358 cells

Toxicology Letters

Volumn 209, Issue 1, 2012, Pages 58-66

  Gelhaus, Stacy L ^a   Gilad, Oren ^b   Hwang, Wei Ting ^a   Penning, Trevor M ^a   Blair, Ian A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Aryl hydrocarbon receptor; Benzopyrene; Environmental carcinogen; LC MS

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 7,8 DIHYDRO 7,8 DIHYDROXYBENZO[A]PYRENE; 7,8 DIHYDROXY 9,10 EPOXY 7,8,9,10 TETRAHYDROBENZO[A]PYRENE 2' DEOXYGUANOSINE; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CARCINOGEN; CYTOCHROME P450; MULTIDRUG RESISTANCE PROTEIN 4; PROBENECID; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ARTICLE; DNA ADDUCT; HUMAN; HUMAN CELL; LUNG ALVEOLUS CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

BENZO(A)PYRENE; BRONCHI; BRONCHOALVEOLAR LAVAGE FLUID; CARCINOGENS; CELL LINE; DINOPROSTONE; DNA; DNA ADDUCTS; HUMANS; IMMUNOHISTOCHEMISTRY; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NF-E2-RELATED FACTOR 2; PROBENECID; PULMONARY ALVEOLI; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR CROSS-TALK; RECEPTORS, ARYL HYDROCARBON; RENAL AGENTS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TETRACHLORODIBENZODIOXIN;

EID: 84155173498     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2011.11.021     Document Type: Article

References (47)

1. Baird W.M., Hooven L.A., Mahadevan B. Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action. Environ. Mol. Mutagen. 2005, 45:106-114.
2. Bostrom C.E., Gerde P., Hanberg A., Jernstrom B., Johansson C., Kyrklund T., Rannug A., Tornqvist M., Victorin K., Westerholm R. Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environ. Health Perspect. 2002, 110(Suppl. 3):451-488.
3. Castano-Vinyals G., D'Errico A., Malats N., Kogevinas M. Biomarkers of exposure to polycyclic aromatic hydrocarbons from environmental air pollution. Occup. Environ. Med. 2004, 61:e12.
4. Chiba T., Uchi H., Yasukawa F., Furue M. Role of the arylhydrocarbon receptor in lung disease. Int. Arch. Allergy Immunol. 2011, 155(Suppl. 1):129-134.
5. Gelhaus S.L., Harvey R.G., Penning T.M., Blair I.A. Regulation of benzo[a]pyrene-mediated DNA- and glutathione-adduct formation by 2,3,7,8-tetrachlorodibenzo-p-dioxin in human lung cells. Chem. Res. Toxicol. 2011, 24:89-98.
6. Georgiadis P., Kyrtopoulos S.A. Molecular epidemiological approaches to the study of the genotoxic effects of urban air pollution. Mutat. Res. 1999, 428:91-98.
7. Gilad O., Nabet B.Y., Ragland R.L., Schoppy D.W., Smith K.D., Durham A.C., Brown E.J. Combining ATR suppression with oncogenic Ras synergistically increases genomic instability, causing synthetic lethality or tumorigenesis in a dosage-dependent manner. Cancer Res. 2010, 70:9693-9702.
8. Gradhand U., Kim R.B. Pharmacogenomics of MRP transporters (ABCC1-5) and BCRP (ABCG2). Drug Metab. Rev. 2008, 40:317-354.
9. Grimmer G., Bohnke H. Polycyclic aromatic hydrocarbon profile analysis of high-protein foods, oils, and fats by gas chromatography. J. Assoc. Off. Anal. Chem. 1975, 58:725-733.
10. Hara Y., Sassi Y., Guibert C., Gambaryan N., Dorfmuller P., Eddahibi S., Lompre A.M., Humbert M., Hulot J.S. Inhibition of MRP4 prevents and reverses pulmonary hypertension in mice. J. Clin. Invest. 2011, 121:2888-2897.
11. Ho L.L., Kench J.G., Handelsman D.J., Scheffer G.L., Stricker P.D., Grygiel J.G., Sutherland R.L., Henshall S.M., Allen J.D., Horvath L.G. Androgen regulation of multidrug resistance-associated protein 4 (MRP4/ABCC4) in prostate cancer. Prostate 2008, 68:1421-1429.
12. Hukkanen J., Pelkonen O., Hakkola J., Raunio H. Expression and regulation of xenobiotic-metabolizing cytochrome P450 (CYP) enzymes in human lung. Crit. Rev. Toxicol. 2002, 32:391-411.
13. Jiang H., Gelhaus S.L., Mangal D., Harvey R.G., Blair I.A., Penning T.M. Metabolism of benzo[a]pyrene in human bronchoalveolar H358 cells using liquid chromatography-mass spectrometry. Chem. Res. Toxicol. 2007, 20:1331-1341.
14. Kruh G.D., Belinsky M.G., Gallo J.M., Lee K. Physiological and pharmacological functions of Mrp2, Mrp3 and Mrp4 as determined from recent studies on gene-disrupted mice. Cancer Metastasis Rev. 2007, 26:5-14.
15. Lee C.H. Reversing agents for ATP-binding cassette drug transporters. Methods Mol. Biol. 2010, 596:325-340.
16. Lee K., Belinsky M.G., Bell D.W., Testa J.R., Kruh G.D. Isolation of MOAT-B, a widely expressed multidrug resistance-associated protein/canalicular multispecific organic anion transporter-related transporter. Cancer Res. 1998, 58:2741-2747.
17. Lee K., Klein-Szanto A.J., Kruh G.D. Analysis of the MRP4 drug resistance profile in transfected NIH3T3 cells. J. Natl. Cancer Inst. 2000, 92:1934-1940.
18. Lee S.H., Blair I.A. Targeted chiral lipidomics analysis by liquid chromatography electron capture atmospheric pressure chemical ionization mass spectrometry (LC-ECAPCI/MS). Methods Enzymol. 2007, 433:159-174.
19. Lemos C., Kathmann I., Giovannetti E., Belien J.A., Scheffer G.L., Calhau C., Jansen G., Peters G.J. Cellular folate status modulates the expression of BCRP and MRP multidrug transporters in cancer cell lines from different origins. Mol. Cancer Ther. 2009, 8:655-664.
20. Lin Z.P., Zhu Y.L., Johnson D.R., Rice K.P., Nottoli T., Hains B.C., McGrath J., Waxman S.G., Sartorelli A.C. Disruption of cAMP and prostaglandin E2 transport by multidrug resistance protein 4 deficiency alters cAMP-mediated signaling and nociceptive response. Mol. Pharmacol. 2008, 73:243-251.
21. Mangal D., Vudathala D.K., Park J.H., Lee S.H., Penning T.M., Blair I.A. Analysis of 7,8-dihydro-8-oxo-2'-deoxyguanosine in cellular DNA during oxidative stress. Chem. Res. Toxicol. 2009, 22:788-797.
22. Mastrangelo G., Fadda E., Marzia V. Polycyclic aromatic hydrocarbons and cancer in man. Environ. Health Perspect. 1996, 104:1166-1170.
23. Miao W., Hu L., Scrivens P.J., Batist G. Transcriptional regulation of NF-E2 P45-related factor (NRF2) expression by the aryl hydrocarbon receptor-xenobiotic response element signaling pathway: direct cross-talk between phase I and II drug-metabolizing enzymes. J. Biol. Chem. 2005, 280:20340-20348.
24. Monien B.H., Muller C., Bakhiya N., Donath C., Frank H., Seidel A., Glatt H. Probenecid, an inhibitor of transmembrane organic anion transporters, alters tissue distribution of DNA adducts in 1-hydroxymethylpyrene-treated rats. Toxicology 2009, 262:80-85.
25. Myllynen P., Kurttila T., Vaskivuo L., Vahakangas K. DNA damage caused by benzo(a)pyrene in MCF-7 cells is increased by verapamil, probenecid and PSC833. Toxicol. Lett. 2007, 169:3-12.
26. Nebert D.W., Karp C.L. Endogenous functions of the aryl hydrocarbon receptor: intersection of cytochrome P450 (CYP1)-metabolized eicosanoids and AHR biology. J. Biol. Chem. 2008, 283:36061-36065.
27. Niestroy J., Barbara A., Herbst K., Rode S., van L.M., Roos P.H. Single and concerted effects of benzo[a]pyrene and flavanoids on the AhR and Nrf2-pathway in the human colon carcinoma cell line Caco-2. Toxicol. In Vitro 2011, 25:671-683.
28. Norris M.D., Smith J., Tanabe K., Tobin P., Flemming C., Scheffer G.L., Wielinga P., Cohn S.L., London W.B., Marshall G.M., Allen J.D., Haber M. Expression of multidrug transporter MRP4/ABCC4 is a marker of poor prognosis in neuroblastoma and confers resistance to irinotecan in vitro. Mol. Cancer Ther. 2005, 4:547-553.
29. Park J.H., Mangal D., Tacka K.A., Quinn A.M., Harvey R.G., Blair I.A., Penning T.M. Evidence for the aldo-keto reductase pathway of polycyclic aromatic trans-dihydrodiol activation in human lung A549 cells. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6846-6851.
30. 32P-postlabeling detection of aromatic adducts in the white blood cell DNA of nonsmoking police officers. Cancer Epidemiol. Biomarkers Prev. 1998, 7:3-11.
31. Perez-Tomas R. Multidrug resistance: retrospect and prospects in anti-cancer drug treatment. Curr. Med. Chem. 2006, 13:1859-1876.
32. Pozzoli L., Gilardoni S., Perrone M.G., De G.G., De R.M., Vione D. Polycyclic aromatic hydrocarbons in the atmosphere: monitoring, sources, sinks and fate. I: monitoring and sources. Ann. Chim. 2004, 94:17-32.
33. Reid G., Wielinga P., Zelcer N., van der Heijden I., Kuil A., de H.M., Wijnholds J., Borst P. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9244-9249.
34. Ritter C.A., Jedlitschky G., Meyer Zu S.H., Grube M., Kock K., Kroemer H.K. Cellular export of drugs and signaling molecules by the ATP-binding cassette transporters MRP4 (ABCC4) and MRP5 (ABCC5). Drug Metab. Rev. 2005, 37:253-278.
35. Ruan Q., Gelhaus S.L., Penning T.M., Harvey R.G., Blair I.A. Aldo-keto reductase- and cytochrome P450-dependent formation of benzo[a]pyrene-derived DNA adducts in human bronchoalveolar cells. Chem. Res. Toxicol. 2007, 20:424-431.
36. Russel F.G., Koenderink J.B., Masereeuw R. Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol. Sci. 2008, 29:200-207.
37. Srivastava S.K., Watkins S.C., Schuetz E., Singh S.V. Role of glutathione conjugate efflux in cellular protection against benzo[a]pyrene-7,8-diol-9,10-epoxide-induced DNA damage. Mol. Carcinog. 2002, 33:156-162.
38. Sweet D.H. Organic anion transporter (Slc22a) family members as mediators of toxicity. Toxicol. Appl. Pharmacol. 2005, 204:198-215.
39. Torky A.R., Stehfest E., Viehweger K., Taege C., Foth H. Immuno-histochemical detection of MRPs in human lung cells in culture. Toxicology 2005, 207:437-450.
40. Uno S., Dalton T.P., Derkenne S., Curran C.P., Miller M.L., Shertzer H.G., Nebert D.W. Oral exposure to benzo[a]pyrene in the mouse: detoxication by inducible cytochrome P450 is more important than metabolic activation. Mol. Pharmacol. 2004, 65:1225-1237.
41. van Aubel R.A., Smeets P.H., Peters J.G., Bindels R.J., Russel F.G. The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J. Am. Soc. Nephrol. 2002, 13:595-603.
42. Wu C.P., Calcagno A.M., Hladky S.B., Ambudkar S.V., Barrand M.A. Modulatory effects of plant phenols on human multidrug-resistance proteins 1, 4 and 5 (ABCC1, 4 and 5). FEBS J. 2005, 272:4725-4740.
43. Xu S., Weerachayaphorn J., Cai S.Y., Soroka C.J., Boyer J.L. Aryl hydrocarbon receptor and NF-E2-related factor 2 are key regulators of human MRP4 expression. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G126-G135.
44. 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.
45. Zelcer N., Reid G., Wielinga P., Kuil A., van der Heijden I., Schuetz J.D., Borst P. Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem. J. 2003, 371:361-367.
46. Zhang Z.Y., Pelletier R.D., Wong Y.N., Sugawara M., Zhao N., Littlefield B.A. Preferential inducibility of CYP1A1 and CYP1A2 by TCDD: differential regulation in primary human hepatocytes versus transformed human cells. Biochem. Biophys. Res. Commun. 2006, 341:399-407.
47. Zmirou D., Masclet P., Boudet C., Dor F., Dechenaux J. Personal exposure to atmospheric polycyclic aromatic hydrocarbons in a general adult population and lung cancer risk assessment. J. Occup. Environ. Med. 2000, 42:121-126.