Fipronil induces CYP isoforms and cytotoxicity in human hepatocytes

Chemico-Biological Interactions

Volumn 164, Issue 3, 2006, Pages 200-214

  Das, Parikshit C ^a   Cao, Yan ^a   Cherrington, Nathan ^b   Hodgson, Ernest ^a   Rose, Randy L ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Apoptosis; CYP1A1; CYP2B6; CYP3A4; Cytotoxicity; Fipronil; Human hepatic and HepG2 cells

Indexed keywords

ANTIBODY; CYTOCHROME; CYTOCHROME P450 1A1; CYTOCHROME P450 2B6; CYTOCHROME P450 3A4; CYTOCHROME P450 3A5; DNA; FIPRONIL; FIPRONIL SULFONE; MESSENGER RNA; PESTICIDE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL STRAIN HEPG2; CELL VIABILITY; CYTOTOXICITY; DOSE TIME EFFECT RELATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INDUCTION; HUMAN; HUMAN CELL; LIVER CELL; LOW DRUG DOSE; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; STATISTICAL SIGNIFICANCE; WESTERN BLOTTING;

ANTIGENS, CD95; CASPASE 3; CASPASE 7; CELL SURVIVAL; CELLS, CULTURED; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME INDUCTION; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; ISOENZYMES; PYRAZOLES; RNA, MESSENGER; SULFUR; TRANSCRIPTION, GENETIC;

EID: 33751174299     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2006.09.013     Document Type: Article

References (47)

1. Tingle C.C., Rother J.A., Dewhurst C.F., Lauer S., and King W.J. Fipronil: environmental fate, ecotoxicology, and human health concerns. Rev. Environ. Contam. Toxicol. 176 (2003) 1-66
2. U.S. EPA, Expediting the review of alternatives to the organophosphates (OPs). US EPA committee to advice on reassessment and transition CARAT2-2, 2000.
3. Jennings K.A., Keller R.J., Atieh B.H., Doss R.B., and Gupta R.C. Human exposure to fipronil from dogs treated with frontline. Vet. Hum. Toxicol. 44 (2002) 303
4. Hainzl D., Cole L.M., and Casida J.E. Mechanisms for selective toxicity of fipronil insecticide and its sulfone metabolite and desulfinyl photoproduct. Chem. Res. Toxicol. 11 (1998) 1529-1535
5. U.S. EPA, Fipronil Pesticide Fact Sheet. PB96-181516. EPA-737-F-96-005. U.S. Environmental Protection Agency, Office of Prevention, Pesticides and Toxic Substances. Washington, DC, 1996.
6. Hamon N., Shaw R., and Yang H. Worldwide development of fipronil insecticide. Proceedings of the Beltwide Cotton Conference, Cotton Insect Research and Control Conference. Nashville, TN (1996)
7. U.S. EPA. Tolerance Petition for Residues of Fipronil in or on Corn and Animal RAC's: HED Risk Assessment (1997), U.S. Environmental Protection Agency, Washington, DC
8. Tang J., Usmani K.A., Hodgson E., and Rose R.L. In vitro metabolism of fipronil by human and rat cytochrome P450 and its interactions with testosterone and diazepam. Chemico-Biol. Interact. 147 (2004) 319-329
9. Hainzl D., and Casida J.E. Fipronil insecticide: novel photochemical desulfinylation with retention of neurotoxicity. Proceedings of the National Academy of Sciences of the United States of America, vol. 93 (1996) 12764-12767
10. Hurley P.M., Hill R.N., and Whiting R.L. Mode of carcinogenic action of pesticides inducing thyroid follicular cell tumors in rodents. Environ. Health Perspect. 106 (1998) 437-445
11. Haseman A.-M., and Lockhart J.K. Correlations between chemically related site-specific carcinogenic effects in long-term studies in rats and mice. Environ. Health Perspect. 101 (1993) 50-54
12. Gonzalez F.J., Liu S.Y., and Yano M. Regulation of cytochrome P450 genes: molecular mechanisms. Pharmacogenetics 3 (1993) 51-57
13. Denison M.S., and Whitlock Jr. J.P. Xenobiotic-inducible transcription of cytochrome P450 genes. J. Biol. Chem. 270 (1995) 18175-18178
14. Rose R.L., Tang J., Choi J., Cao Y., Usmani A., Cherrington N., and Hodgson E. Pesticide metabolism in humans, including polymorphisms. Scand. J. Work Environ. Health 31 Suppl 1 (2005) 156-163 discussion 119-22
15. Ledirac N., Delescluse C., deSousa G., Pralavorio M., Lesca P., Amichot M., Berge J.B., and 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. 144 (1997) 177-182
16. Hartley D.P., and Klaassen C.D. Detection of chemical-induced differential expression of rat hepatic cytochrome P450 mRNA transcripts using branched DNA signal amplification technology. Drug Metab. Dispos. 28 (2000) 608-616
17. Laemmli U. Cleavage of structural proteins during the assembly of the head bacteriophage T4. Nature 227 (1970) 680-685
18. Usmani K.A., Rose R.L., and Hodgson E. Inhibition and activation of the human liver microsomal and human cytochrome P450 3A4 metabolism of testosterone by deployment-related chemicals. Drug Metab. Dispos. 31 (2003) 384-391
19. Lemaire G., de Sousa G., and Rahmani R. A PXR reporter gene assay in a stable cell culture system: CYP3A4 and CYP2B6 induction by pesticides. Biochem. Pharmacol. 68 (2004) 2347-2358
20. Heder A.F., Hirsch-Ernst K.I., Bauer D., Kahl G.F., and Desel H. Induction of cytochrome P450 2B1 by pyrethroids in primary rat hepatocyte cultures. Biochem. Pharmacol. 62 (2001) 71-79
21. de Sousa G., Nicolas F., Valles B., Coassolo P., and Rahmani R. Relationships between in vitro and in vivo hepatic biotransformation of drugs in humans and animals: pharmaco-toxicological consequences. Cell Biol. Toxicol. 11 (1995) 147-153
22. Yamazaki H., and Shimada T. Progesterone and testosterone hydroxylation by cytochromes P450 2C19, 2C9, and 3A4 in human liver microsomes. Arch. Biochem. Biophys. 346 (1997) 161-169
23. Waxman D.J., Lapenson D.P., Aoyama T., Gelboin H.V., Gonzalez F.J., and Korzekwa K. Steroid hormone hydroxylase specificities of eleven cDNA-expressed human cytochrome P450s. Arch. Biochem. Biophys. 290 (1991) 160-166
24. Waxman D.J., Attisano C., Guengerich F.P., and Lapenson D.P. Human liver microsomal steroid metabolism: identification of the major microsomal steroid hormone 6 beta-hydroxylase cytochrome P-450 enzyme. Arch. Biochem. Biophys. 263 (1988) 424-436
25. Goodwin B., Moore L.B., Stoltz C.M., McKee D.D., and Kliewer S.A. Regulation of the human CYP2B6 gene by the nuclear pregnane X receptor. Mol. Pharmacol. 60 (2001) 427-431
26. Bertilsson G., Heidrich J., Svensson K., Asman M., Jendeberg L., Sydow-Backman M., Ohlsson R., Postlind H., Blomquist P., and Berkenstam A. Identification of a human nuclear receptor defines a new signaling pathway for CYP3A induction. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 12208-12213
27. Geick A., Eichelbaum M., and Burk O. Nuclear receptor response elements mediate induction of intestinal MDR1 by rifampin. J. Biol. Chem. 276 (2001) 14581-14587
28. Coumoul X., Diry M., and Barouki R. PXR-dependent induction of human CYP3A4 gene expression by organochlorine pesticides. Biochem. Pharmacol. 64 (2002) 1513-1519
29. G. Lemaire, W. Mnif, J.M. Pascussi, A. Pillon, F. Rabenoelina, H. Fenet, E. Gomez, C. Casellas, J.C. Nicolas, V. Cavailles, M.J. Duschesne, P. Balguer, Identification of new human PXR ligands among pesticides using a stable reporter cell system. Toxicol Sci. (2006).
30. Di Consiglio E., Meneguz A., and Testai E. Organophosphorothionate pesticides inhibit the bioactivation of imipramine by human hepatic cytochrome P450s. Toxicol. Appl. Pharmacol. 205 (2005) 237-246
31. Usmani K., Rose R.L., and Hodgson E. Inhibition of the human liver microsomal and human cytochrome P450 1A2 and 3A4 metabolism of estradiol by deployment-related chemicals. Drug Metab. Dispos. 34 (2006) 1606-1614
32. Okey A.B., Riddick D.S., and Harper P.A. The Ah receptor: mediator of the toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and related compounds. Toxicol. Lett. 70 (1994) 1-22
33. Nebert D.W., Puga A., and Vasiliou V. Role of the Ah receptor and the dioxin-inducible [Ah] gene battery in toxicity, cancer, and signal transduction. Ann. N.Y. Acad. Sci. 685 (1993) 624-640
34. Nebert D.W. The Ah locus: genetic differences in toxicity, cancer, mutation, and birth defects. Crit. Rev. Toxicol. 20 (1989) 153-174
35. Nebert D.W., McKinnon R.A., and Puga A. Human drug-metabolizing enzyme polymorphisms: effects on risk of toxicity and cancer. DNA Cell Biol. 15 (1996) 273-280
36. Kopponen P., Torronen R., Maki-Paakkanen J., von Wright A., and Karenlampi S. Comparison of CYP1A1 induction and genotoxicity in vitro as indicators of potentially harmful effects of environmental samples. Arch. Toxicol. 68 (1994) 167-173
37. de Sousa G., Fontaine F., Pralavorio M., Botta-Fridlund D., Letreut Y., and Rahmani R. Insecticide cytotoxicity and CYP1A1/2 induction in primary human and rat hepatocyte cultures. Toxicol. In Vitro 11 (1997) 451-457
38. Grant D., Chalmers A.E., Wolff M.A., Hoffman H.B., and Bushey D.F. Fipronil: action at the GABA receptor. Rev. Toxicol. 2 (1998) 147-156
39. Casida J.E. Insecticide action at the GABA-gated chloride channel: recognition, progress, and prospects. Arch. Insect. Biochem. Physiol. 22 (1993) 13-23
40. Bloomquist J. GABA and glutamate receptors as biochemical sites for insecticide action. In: Ishaaya I. (Ed). Biochemical Sites of Insecticide Action and Resistance (2001), Springer-Verlag, Berlin
41. LeCluyse E.L. Human hepatocyte culture systems for the in vitro evaluation of cytochrome P450 expression and regulation. Eur. J. Pharm. Sci. 13 (2001) 343-368
42. Lu C., and Li A.P. Species comparison in P450 induction: effects of dexamethasone, omeprazole, and rifampin on P450 isoforms 1A and 3A in primary cultured hepatocytes from man, Sprague-Dawley rat, minipig, and beagle dog. Chem. Biol. Interact. 134 (2001) 271-281
43. Yager J.D. Endogenous estrogens as carcinogens through metabolic activation. J. Natl. Cancer Inst. Monogr. (2000) 67-73
44. Rogan E.G., Badawi A.F., Devanesan P.D., Meza J.L., Edney J.A., West W.W., Higginbotham S.M., and Cavalieri E.L. Relative imbalances in estrogen metabolism and conjugation in breast tissue of women with carcinoma: potential biomarkers of susceptibility to cancer. Carcinogenesis 24 (2003) 697-702
45. Cavalieri E.L., Stack D.E., Devanesan P.D., Todorovic R., Dwivedy I., Higginbotham S., Johansson S.L., Patil K.D., Gross M.L., Gooden J.K., Ramanathan R., Cerny R.L., and Rogan E.G. Molecular origin of cancer: catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 10937-10942
46. Cavalieri E.L., Devanesan P., Bosland M.C., Badawi A.F., and Rogan E.G. Catechol estrogen metabolites and conjugates in different regions of the prostate of Noble rats treated with 4-hydroxyestradiol: implications for estrogen-induced initiation of prostate cancer. Carcinogenesis 23 (2002) 329-333
47. Gomez-Lechon M.J., Serralta A., Donato M.T., Jimenez N., O'Connor E., Castell J.V., and Mir J. The immunosuppressant drug FK506 prevents Fas-induced apoptosis in human hepatocytes. Biochem. Pharmacol. 68 (2004) 2427-2433