Benzo[a]Pyrene, 3-Methylcholanthrene and ß-Naphthoflavone Induce Oxidative Stress in Hepatoma Hepa 1c1c7 Cells by an AHR-dependent Pathway

References

• Ema, E., Sogawa, K., Watanabe, N., Chujoh, Y, Matsushita, N., Gotoh, 0., Funae, Y. and Fujii-Kuriyama, Y. (1992) "cDNA cloning and structure of mouse putative Ah receptor", Biochem. Biophys. Res. Commun. 184, 246–253.
   PubMedGoogle Scholar
• Burbach, K.M., Poland, A. and Bradfield, C.A. (1992) "Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor", Proc. Natl Acad. Sci. USA 89, 8158–8189.
   Web of Science ®Google Scholar
• Carver, L.A. and Bradfield, C.A. (1997) "Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo", J. Biol. Chem. 272, 11452–11456.
   PubMed Web of Science ®Google Scholar
• Ma, Q. and Whitlock, J.P., Jr. (1997) "A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcrip-tional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin", J. Biol. Chem. 272, 8878–8884.
   PubMed Web of Science ®Google Scholar
• Meyer, B.K., Pray-Grant, M.G., Vanden Heuvel, J.P. and Perdew, G.H. (1998) "Hepatitis B virus X-associated protein 2 is a subunit of the unliganded aryl hydrocarbon receptor core complex and exhibits transcriptional enhancer activity", Mol. Cell. Biol. 18, 978–988.
   PubMed Web of Science ®Google Scholar
• Nebert, D.W., Puga, A. and Vasiliou, V. (1993) "Role of the Ah receptor and the dioxin-inducible [Ah] gene battery in toxicity, cancer, and signal transduction", Ann. N.Y. Acad. Sci. 685, 624–640.
   PubMed Web of Science ®Google Scholar
• Whitlock, J.P., Jr. (1999) "Induction of cytochrome P4501A1", Annu. Rev. Pharmacol. Toxicol. 39, 103–125.
   PubMed Web of Science ®Google Scholar
• Bunn, H.F. and Poyton, R.O. (1996) "Oxygen sensing and molecular adaptation to hypoxia", Physiol. Rev. 76, 839–885.
   PubMed Web of Science ®Google Scholar
• Semenza, G.L. (1998) "Hypoxia-inducible factor 1 and the molecular physiology of oxygen homeostasis", J. Lab. Clin. Med. 131, 207–214.
   PubMed Web of Science ®Google Scholar
• Nebert, D.W. and Duffy, J.J. (1997) "How knockout mouse lines will be used to study the role of drug-metabolizing enzymes and their receptors during reproduction and development, and in environmental toxicity, cancer, and oxidative stress", Biochem. Pharmacol. 53, 249–254.
   PubMed Web of Science ®Google Scholar
• Schrenk, D. (1998) "Impact of dioxin-type induction of drug-metabolizing enzymes on the metabolism of endo- and xenobiotics", Biochem. Pharmacol. 55, 1155–1162.
   PubMed Web of Science ®Google Scholar
• Poland, A. and Knutson, J.C. (1982) "2,3,7,8-tetrachlorodi-benzo-p-dioxin and related halogenated aromatic hydrocar-bons: examination of the mechanism of toxicity", Annu. Rev. Pharmcol. Toxicol. 22, 517–554.
   PubMed Web of Science ®Google Scholar
• Stohs, S.J., Alsharif, N.Z., Shara, M.A., al Bayati, Z.A. and Wahba, Z.Z. (1989) "Evidence for the induction of an oxidative stress in rat hepatic mitochondria by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)", Adv. Exp. Med. Biol. 283, 827–831.
   Google Scholar
• Senft, A.P., Dalton, T.P., Nebert, D.W., Genter, M.B., Puga, A., Hutchinson, R.J., Kerzee, J.K., Uno, U. and Shertzer, H.G. (2002) "Mitochondrial reactive oxygen production is depen-dent on the aromatic hydrocarbon receptor", Free Radic. Biol. Med. 33, 1268–1278.
   PubMed Web of Science ®Google Scholar
• Hassoun, E.A., Wilt, S.C., DeVito, M.J., A Van Birgelen, A., Alsharif, N.Z., Birnbaum, L.S. and Stohs, S.J. (1998) "Induction of oxidative stress in brain tissues of mice after subchronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin", Toxicol. Sci. 42, 23–27.
   PubMed Web of Science ®Google Scholar
• Slezak, B.P., Hatch, G.E., DeVito, M.J., Diliberto, J.J., Slade, R., Crissman, K., Hassoun, E. and Birnbaum, L.S. (2000) "Oxidative stress in female B6C3F1 mice following acute and subchronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)", Toxicol. Sci. 54, 390–398.
   PubMed Web of Science ®Google Scholar
• Hassoun, E.A., Li, F., Abushaban, A. and Stohs, S.J. (2000) "The relative abilities of TCDD and its congeners to induce oxidative stress in the hepatic and brain tissues of rats after subchronic exposure", Toxicology 145, 103–113.
   PubMed Web of Science ®Google Scholar
• Stohs, S.J. (1990) "Oxidative stress induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)", Free Radic. Biol. Med. 9, 79–90.
   PubMed Web of Science ®Google Scholar
• Shertzer, H.G., Nebert, D.W., Puga, A., Ary, M., Sonntag, D., Dixon, K., Robinson, L.J., Cianciolo, E. and Dalton, T.P. (1998) "Dioxin causes a sustained oxidative stress response in the mouse", Biochem. Biophys. Res. Commun. 253, 44–48.
   PubMed Web of Science ®Google Scholar
• Park, J.-Y., Shigenaga, M.K. and Ames, B.N. (1996) "Induction of cytochrome P4501A1 by 2,3,7,8-tetrachlorodibenzo-p-dioxin or indolo(3,2-b)carbazole is associated with oxidative DNA damage", Proc. Natl Acad. Sci. USA 93, 2322–2327.
   Google Scholar
• Hamm, J.T., Ross, D.C., Richardson, V.M., Diliberto, J.J. and Birnbaum, L.S. (1998) "Methoxyresorufin: an inappropriate substrate for CYP1A2 in the mouse", Biochem. Pharmacol. 56, 1657–1660.
   PubMed Web of Science ®Google Scholar
• Sambrook, J., Fritsch, E.F., Maniatatis, T., eds (1989) Molecular Cloning. A Laboratory Manual (Cold Spring Harbour Laboratory Press, New York).
   Google Scholar
• Vakharia, D.D., Liu, N., Pause, R., Fasco, M., Bessette, E., Zhang, Q.Y. and Kaminsky, L.S. (2001) "Polycydic aromatic hydrocarbon/metal mixtures: effect on PAH induction of CYP1A1 in human HEPG2 cells", Drug Metab. Dispos. 29, 999–1006.
   PubMed Web of Science ®Google Scholar
• Sinal, C.J. and Bend, J.R. (1997) "Aryl hydrocarbon-dependent induction of cyp1a1 by bilirubin in mouse hepatoma Hepa 1c1c7 cells", Mol. Pharmacol. 52, 590–599.
   PubMed Web of Science ®Google Scholar
• Lorenzen, A. and Kennedy, S.W. (1993) "A fluorescence-based protein assay for use with a microplate reader", Anal. Biochem. 214, 346–348.
   PubMed Web of Science ®Google Scholar
• LeBel, C.P., Ischiropoulos, H. and Bondy, S.C. (1992) "Evaluation of the probe 2',7'-dichlorofluorescein as an indicator of reactive oxygen species formation and oxidative stress", Chem. Res. Toxicol. 5, 227–231.
   PubMed Web of Science ®Google Scholar
• Ohkawa, H., Ohishi, N. and Yagi, K. (1979) "Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction", Anal. Biochem. 95, 351–358.
   PubMed Web of Science ®Google Scholar
• Seubert, J.M., Darmon, A.J., El-Kadi, A.O., D'Souza, S.J. and Bend, J.R. (2002) "Apoptosis in murine hepatoma hepa 1c1c7 wild-type, C12, and C4 cells mediated by bilirubin", Mol. Pharmacol. 62, 257–264.
   PubMed Web of Science ®Google Scholar
• Devary, Y., Gottlieb, R.A., Smeal, T. and Karin, M. (1992) "The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases", Cell 71, 1081–1091.
   PubMed Web of Science ®Google Scholar
• Philip, P.A., Kaklamanis, L., Ryley, N., Stratford, I., Wolf, R., Harris, A. and Carmichael, J. (1994) "Expression of xenobiotic-metabolizing enzymes by primary and secondary hepatic tumors in man", Int. J. Radiat. Oncol. Biol. Phys. 29,277–283.
   PubMed Web of Science ®Google Scholar
• Bassi, A.M., Ledda, S., Penco, S., Menini, S., Muzio, G., Canuto, R. and Ferro, M. (2000) "Changes of CYP1A1, GST, and ALDH3 enzymes in hepatoma cell lines undergoing enhanced lipid peroxidation", Free Radic. Biol. Med. 29, 1186–1196.
   PubMed Web of Science ®Google Scholar
• El-Kadi, A.O., Bleau, A.-M., Dumont, I., Maurice, H. and du Souich, P. (2000) "Role of reactive oxygen intermediates in the decrease of hepatic cytochrome P450 activity by serum of humans and rabbits with an acute inflammatory reaction", Drug Metab. Dispos. 28, 1112–1120.
   PubMed Web of Science ®Google Scholar
• Puga, A., Barnes, S.J., Chang, C., Zhu, H., Nephew, K.P., Khan, S.A. and Shertzer, H.G. (2000) "Activation of transcription factors activator protein-1 and nuclear factor-kappaB by 2,3,7,8-tetrachlorodibenzo-p-dioxin", Biochem. Pharmacol. 59, 997–1005.
   PubMed Web of Science ®Google Scholar
• Fernandez-Salguero, P.M., Ward, J.M., Sundberg, J.P. and Gonzalez, F.J. (1997) "Lesions of aryl-hydrocarbon receptor-deficient mice", Vet. Pathol. 34, 605–614.
   PubMed Web of Science ®Google Scholar
• Smith, A.G., Clothier, B., Robinson, S., Scullion, M.J., Carthew, P., Edwards, R., Luo, J., Lim, C.K. and Toledano, M. (1998) "Interaction between iron metabolism and 2,3,7,8-tetrachlorodibenzo-p-dioxin in mice with variants of the Ahr gene: a hepatic oxidative mechanism", Mol. Pharmacol. 53, 52–61.
   PubMed Web of Science ®Google Scholar
• Hassoun, E.A. and Stohs, S.J. (1996) "TCDD, endrin and lindane induced oxidative stress in fetal and placental tissues of C57BL/6J and DBA /2J mice", Comp. Biochem. Physiol. C. Pharmacol. Toxicol. Endocrinol. 115, 11–18.
   PubMed Web of Science ®Google Scholar
• Guengerich, F.P. and Lieber, D.C. (1985) "Enzymatic activation of chemicals to toxic metabolites", Crit. Rev. Toxicol. 14, 259–307.
   PubMed Web of Science ®Google Scholar
• Poulos, T.L. and Raag, R. (1992) "Cytochrome P450cam: crystallography, oxygen activation, and electron transfer", FASEB J. 6, 674–679.
   PubMed Web of Science ®Google Scholar
• Schlezinger, J.J., White, R.D. and Stegeman, J.J. (1999) "Oxidative inactivation of cytochrome P-450 1A (CYP1A) stimulated by 3,3',4,4'-tetrachlorobiphenyl: production of reactive oxygen by vertebrate CYP1As", Mol. Pharmacol. 56, 588–597.
   PubMed Web of Science ®Google Scholar
• Gooch, J.W., Elskus, A.A., Kloepper-Sams, P.J., Hahn, M.E. and Stegeman, J.J. (1989) "Effects of ortho and non-ortho substituted polychlorinated biphenyl congeners on the hepatic monooxygenase system in scup (Stenotomus chrysops)", Toxicol. Appl. Pharmacol. 98, 422–433.
   PubMed Web of Science ®Google Scholar
• Sinclair, P., Frezza, J., Sinclair, J., Bement, W., Haugen, S., Healey, J. and Bonkovsky, H. (1989) "Immunochemical detection of different isoenzymes of cytochrome P-450 induced in chick hepatocyte cultures", Biochem. J. 258, 237–245.
   PubMed Web of Science ®Google Scholar
• White, R.D., Shea, D., Solow, A.R. and Stegeman, J.J. (1997) "Induction and post-transcriptional suppression of hepatic cytochrome P4501A1 by 3,3',4,4'-tetrachlorobiphenyl", Biochem. Pharmacol. 53, 1029–1040.
   PubMed Web of Science ®Google Scholar
• Morel, Y. and Barouki, R. (1998) "Down-regulation of cytochrome P450 1A1 gene promoter by oxidative stress. Critical contribution of nuclear factor 1", J. Biol. Chem. 273, 26969–26976.
   PubMed Web of Science ®Google Scholar
• Morel, Y. and Barouki, R. (1999) "Repression of gene expression by oxidative stress", Biochem. J. 342, 481–496.
   PubMed Web of Science ®Google Scholar
• Karuzina, I.I. and Archakov, A.L. (1994) "Hydrogen peroxide-mediated inactivation of microsomal cytochrome P450 during monooxygenase reactions", Free Radic. Biol. Med. 17, 557–567.
   PubMed Web of Science ®Google Scholar
• Archakov, A.L., Zgoda, V.G. and Karuzina, LI. (1998) "Oxidative modification of cytochrome P450 and other macromolecules during its turnover", Vopr. Med. Khim. 44, 3–27.
   PubMedGoogle Scholar
• Paton, T.E. and Renton, K.W. (1998) "Cytokine-mediated down-regulation of CYP1A1 in Hepa1 cells", Biochem. Pharmacol. 55, 1791–1796.
   PubMed Web of Science ®Google Scholar
• Bogdan, C. (2001) "Nitric oxide and the regulation of gene expression", Trends Cell. Biol. 11, 66–75.
   PubMed Web of Science ®Google Scholar