Inflammatory mediators accelerate metabolism of benzo[a]pyrene in rat alveolar type II cells: The role of enhanced cytochrome P450 1B1 expression

Toxicology

Volumn 314, Issue 1, 2013, Pages 30-38

  Šmerdová, Lenka ^a   Neča, Jiří ^b   Svobodová, Jana ^a,c   Topinka, Jan ^d   Schmuczerová, Jana ^d   Kozubík, Alois ^a   Machala, Miroslav ^b   Vondráček, Jan ^a  

^a INSTITUTE OF BIOPHYSICS   (Czech Republic)

^b VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^c MASARYK UNIVERSITY   (Czech Republic)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

Author keywords

CYP1B1; DNA adducts; Inflammation; Metabolism; Polycyclic aromatic hydrocarbons

Indexed keywords

AKR1C14 ENZYME; BENZO[A]PYRENE; CYTOCHROME P450 1B1; DNA; MULTIDRUG RESISTANCE PROTEIN 1; OXIDOREDUCTASE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AKR1C15 PROTEIN, RAT; AUTACOID; CULTURE MEDIUM; CYP1B1 PROTEIN, RAT; CYTOKINE; DNA ADDUCT; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 3; UNSPECIFIC MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LINE; CONTROLLED STUDY; DNA ADDUCT; GENE SILENCING; INFLAMMATION; LUNG ALVEOLUS CELL TYPE 2; LUNG ALVEOLUS MACROPHAGE; MALE; METABOLISM; METABOLITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; UPREGULATION; ANIMAL; BIOSYNTHESIS; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; LUNG ALVEOLUS; REAL TIME POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

RATTUS;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BENZO(A)PYRENE; BLOTTING, WESTERN; CELL LINE; CULTURE MEDIA, CONDITIONED; CYTOCHROME P-450 CYP1B1; CYTOKINES; DNA ADDUCTS; INFLAMMATION MEDIATORS; OXIDOREDUCTASES ACTING ON ALDEHYDE OR OXO GROUP DONORS; P-GLYCOPROTEINS; PULMONARY ALVEOLI; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TANDEM MASS SPECTROMETRY; TRANSFECTION;

EID: 84884940937     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2013.09.001     Document Type: Article

References (43)

1. Aitken A.E., Richardson T.A., Morgan E.T. Regulation of drug-metabolizing enzymes and transporters in inflammation. Annu. Rev. Pharmacol. Toxicol. 2006, 46:123-149.
2. Anttila S., Raunio H., Hakkola J. Cytochrome P450-mediated pulmonary metabolism of carcinogens: regulation and cross-talk in lung carcinogenesis. Am. J. Respir. Cell Mol. Biol. 2011, 44:583-590.
3. 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.
4. Balkwill F., Charles K.A., Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005, 7:211-217.
5. Borm P.J., Knaapen A.M., Schins R.P., Godschalk R.W., Schooten F.J. Neutrophils amplify the formation of DNA adducts by benzo[a]pyrene in lung target cells. Environ. Health Perspect. 1997, 105(Suppl. 5):1089-1093.
6. Burdick A.D., Davis J.W., Liu K.J., Hudson L.G., Shi H., Monske M.L., Burchiel S.W. Benzo[a]pyrene quinones increase cell proliferation, generate reactive oxygen species, and transactivate the epidermal growth factor receptor in breast epithelial cells. Cancer Res. 2003, 63:7825-7833.
7. Burchiel S.W., Thompson T.A., Lauer F.T., Oprea T.I. Activation of dioxin response element (DRE)-associated genes by benzo[a]pyrene 3,6-quinone and benzo[a]pyrene 1,6-quinone in MCF-10A human mammary epithelial cells. Toxicol. Appl. Pharmacol. 2007, 221:203-214.
8. Cavalieri E.L., Rogan E.G. Central role of radical cations in metabolic activation of polycyclic aromatic hydrocarbons. Xenobiotica 1995, 25:677-688.
9. Driscoll K.E., Carter J.M., Iype P.T., Kumari H.L., Crosby L.L., Aardema M.J., Isfort R.J., Cody D., Chestnut M.H., Burns J.L., Le Boeuf R.A. Establishment of immortalized alveolar type II epithelial cell lines from adult rats. In Vitro Cell. Dev. Biol. Anim. 1995, 31:516-527.
10. Fardel O. Cytokines as molecular targets for aryl hydrocarbon receptor ligands: implications for toxicity and xenobiotic detoxification. Expert Opin. Drug Metab. Toxicol. 2013, 9:141-152.
11. Fardel O., Kolasa E., Le Vee M. Environmental chemicals as substrates, inhibitors or inducers of drug transporters: implication for toxicokinetics, toxicity and pharmacokinetics. Expert Opin. Drug Metab. Toxicol. 2012, 8:29-46.
12. Gonçalves R.B., Coletta R.D., Silverio K.G., Benevides L., Casati M.Z., da Silva J.S., Nociti F.H. Impact of smoking on inflammation: overview of molecular mechanisms. Inflamm. Res. 2011, 60:409-424.
13. Hayes C.L., Spink D.C., Spink B.C., Cao J.Q., Walker N.J., Sutter T.R. 17 beta-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:9776-9781.
14. Hecht S.S. Tobacco smoke carcinogens and lung cancer. J. Natl. Cancer Inst. 1999, 91:1194-1210.
15. IARC Air Pollution, Part 1, Some Non-heterocyclic Polycyclic Aromatic Hydrocarbons and Some Related Industrial Exposures 2010, IARC, Lyon.
16. Jiang H., Shen Y.M., Quinn A.M., Penning T.M. Competing roles of cytochrome P450 1A1/1B1 and aldo-keto reductase 1A1 in the metabolic activation of (+/-)-7,8-dihydroxy-7,8-dihydro-benzo[a]pyrene in human bronchoalveolar cell extracts. Chem. Res. Toxicol. 2005, 18:365-374.
17. Kim J.H., Stansbury K.H., Walker N.J., Trush M.A., Strickland P.T., Sutter T.R. Metabolism of benzo[a]pyrene and benzo[a]pyrene-7,8-diol by human cytochrome P450 1B1. Carcinogenesis 1998, 19:1847-1853.
18. Kurzawski M., Dziedziejko V., Post M., Wojcicki M., Urasinska E., Mietkiewski J., Drozdzik M. Expression of genes involved in xenobiotic metabolism and transport in end-stage liver disease: up-regulation of ABCC4 and CYP1B1. Pharmacol. Rep. 2012, 64:927-939.
19. Li N., Xia T., Nel A.E. The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radic. Biol. Med. 2008, 44:1689-1699.
20. Malaplate-Armand C., Ferrari L., Masson C., Siest G., Batt A.M. Astroglial CYP1B1 up-regulation in inflammatory/oxidative toxic conditions: IL-1beta effect and protection by N-acetylcysteine. Toxicol. Lett. 2003, 138:243-251.
21. Mbawuike I.N., Herscowitz H.B. MH-S, a murine alveolar macrophage cell line: morphological, cytochemical, and functional characteristics. J. Leukoc. Biol. 1989, 46:119-127.
22. Miller K.P., Ramos K.S. Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metab. Rev. 2001, 33:1-35.
23. Moorthy B., Miller K.P., Jiang W., Williams E.S., Kondraganti S.R., Ramos K.S. Role of cytochrome P4501B1 in benzo[a]pyrene bioactivation to DNA-binding metabolites in mouse vascular smooth muscle cells: evidence from 32P-postlabeling for formation of 3-hydroxybenzo[a]pyrene and benzo[a]pyrene-3,6-quinone as major proximate genotoxic intermediates. J. Pharmacol. Exp. Ther. 2003, 305:394-401.
24. 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.
25. 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.
26. Penning T.M., Burczynski M.E., Hung C.F., McCoull K.D., Palackal N.T., Tsuruda L.S. Dihydrodiol dehydrogenases and polycyclic aromatic hydrocarbon activation: generation of reactive and redox active o-quinones. Chem. Res. Toxicol. 1999, 12:1-18.
27. Piscaglia F., Knittel T., Kobold D., Barnikol-Watanabe S., Di Rocco P., Ramadori G. Cellular localization of hepatic cytochrome 1B1 expression and its regulation by aromatic hydrocarbons and inflammatory cytokines. Biochem. Pharmacol. 1999, 58:157-165.
28. Quinn A.M., Penning T.M. Comparisons of (+/-)-benzo[a]pyrene-trans-7,8-dihydrodiol activation by human cytochrome P450 and aldo-keto reductase enzymes: effect of redox state and expression levels. Chem. Res. Toxicol. 2008, 21:1086-1094.
29. Rodríguez-Fragoso L., Melendez K., Hudson L.G., Lauer F.T., Burchiel S.W. EGF-receptor phosphorylation and downstream signaling are activated by benzo[a]pyrene 3,6-quinone and benzo[a]pyrene 1,6-quinone in human mammary epithelial cells. Toxicol. Appl. Pharmacol. 2009, 235:321-328.
30. Schuetz E.G., Yasuda K., Arimori K., Schuetz J.D. Human MDR1 and mouse mdr1a P-glycoprotein alter the cellular retention and disposition of erythromycin, but not of retinoic acid or benzo(a)pyrene. Arch. Biochem. Biophys. 1998, 350:340-347.
31. Shiizaki K., Kawanishi M., Yagi T. Dioxin suppresses benzo[a]pyrene-induced mutations and DNA adduct formation through cytochrome P450 1A1 induction and (+/-)-anti-benzo[a]pyrene-7,8-diol-9,10-epoxide inactivation in human hepatoma cells. Mutat. Res. 2013, 750:77-85.
32. Shimada T., Gillam E.M., Oda Y., Tsumura F., Sutter T.R., Guengerich F.P., Inoue K. Metabolism of benzo[a]pyrene to trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene by recombinant human cytochrome P450 1B1 and purified liver epoxide hydrolase. Chem. Res. Toxicol. 1999, 12:623-629.
33. Shimada T., Hayes C.L., Yamazaki H., Amin S., Hecht S.S., Guengerich F.P., Sutter T.R. Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 1996, 56:2979-2984.
34. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
35. Sissung T.M., Price D.K., Sparreboom A., Figg W.D. Pharmacogenetics and regulation of human cytochrome P450 1B1: implications in hormone-mediated tumor metabolism and a novel target for therapeutic intervention. Mol. Cancer Res. 2006, 4:135-150.
36. Tian Y., Rabson A.B., Gallo M.A. Ah receptor and NF-kappaB interactions: mechanisms and physiological implications. Chem. Biol. Interact. 2002, 141:97-115.
37. Umannová L., Machala M., Topinka J., Nováková Z., Milcová A., Kozubík A., Vondráček J. Tumor necrosis factor-alpha potentiates genotoxic effects of benzo[a]pyrene in rat liver epithelial cells through upregulation of cytochrome P450 1B1 expression. Mutat. Res. 2008, 640:162-169.
38. Umannová L., Machala M., Topinka J., Schmuczerová J., Krcmář P., Neča J., Šujanová K., Kozubík A., Vondráček J. Benzo[a]pyrene and tumor necrosis factor-alpha coordinately increase genotoxic damage and the production of proinflammatory mediators in alveolar epithelial type II cells. Toxicol. Lett. 2011, 206:121-129.
39. Uppstad H., Ovrebo S., Haugen A., Mollerup S. Importance of CYP1A1 and CYP1B1 in bioactivation of benzo[a]pyrene in human lung cell lines. Toxicol. Lett. 2010, 192:221-228.
40. Vondráček J., Krčmář P., Procházková J., Trilecová L., Gavelová M., Skálová L., Szotáková B., Bunček M., Radilová H., Kozubík A., Machala M. The role of aryl hydrocarbon receptor in regulation of enzymes involved in metabolic activation of polycyclic aromatic hydrocarbons in a model of rat liver progenitor cells. Chem. Biol. Interact. 2009, 180:226-237.
41. Vondráček J., Umannová L., Machala M. Interactions of the aryl hydrocarbon receptor with inflammatory mediators: beyond CYP1A regulation. Curr. Drug Metab. 2011, 12:89-103.
42. Xu J., Xu F., Lin Y. Cigarette smoke synergizes lipopolysaccharide-induced interleukin-1beta and tumor necrosis factor-alpha secretion from macrophages via substance P-mediated nuclear factor-kappa B activation. Am. J. Respir. Cell Mol. Biol. 2011, 44:302-308.
43. Xue W., Warshawsky D. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol. Appl. Pharmacol. 2005, 206:73-93.