Perfluorocarboxylic acids induce cytochrome P450 enzymes in mouse liver through activation of PPAR-α and CAR transcription factors

Toxicological Sciences

Volumn 106, Issue 1, 2008, Pages 29-36

  Cheng, Xingguo ^a   Klaassen, Curtis D ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Constitutive androstane receptor (CAR); Cytochrome p450 enzymes (Cyps); Perfluorocarboxylic acids (PFCAs); Perfluorodecanoic acid (PFDA); Perfluorooctanoic acid (PFOA); Peroxisome proliferator activated receptor alpha (PPAR )

Indexed keywords

CONSTITUTIVE ANDROSTANE RECEPTOR; CYTOCHROME P450; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 2B; CYTOCHROME P450 2B10; CYTOCHROME P450 3A11; CYTOCHROME P450 4A; CYTOCHROME P450 4A14; FARNESOID X RECEPTOR; MESSENGER RNA; OXIDOREDUCTASE; PERFLUORO COMPOUND; PERFLUOROCARBOXYLIC ACID DERIVATIVE; PERFLUORODECANOIC ACID; PERFLUOROOCTANOIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PREGNANE X RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME INDUCTION; ENZYME REGULATION; ENZYME SPECIFICITY; GENE EXPRESSION; LIVER PARENCHYMA; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TOXICOKINETICS; WILD TYPE; XENOBIOTIC METABOLISM;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; CYTOCHROME P-450 ENZYME SYSTEM; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; ENZYME INDUCTION; FLUOROCARBONS; LAURIC ACIDS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OCTANOIC ACIDS; PPAR ALPHA; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, STEROID; RNA, MESSENGER; STEROID HYDROXYLASES; TRANSCRIPTION FACTORS;

MUS;

EID: 54349091338     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn147     Document Type: Article

References (40)

1. Adinehzadeh, M., and Reo, N. V. (1998). Effects of peroxisome proliferators on rat liver phospholipids: Sphingomyelin degradation may be involved in hepatotoxic mechanism of perfluorodecanoic acid. Chem. Res. Toxicol. 11, 428-440.
2. Akiyama, T. E., Nicol, C. J., Fievet, C., Staels, B., Ward, J. M., Auwerx, J., Lee, S. S., Gonzalez, F. J., and Peters, J. M. (2001). Peroxisome proliferator-activated receptor-alpha regulates lipid homeostasis, but is not associated with obesity: Studies with congenic mouse lines. J. Biol. Chem. 276, 39088-39093.
3. Brewster, D. W., and Birnbaum, L. S. (1989). The biochemical toxicity of perfluorodecanoic acid in the mouse is different from that of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 99, 544-554.
4. Cai, Y., Appelkvist, E. L., and DePierre, J. W. (1995). Hepatic oxidative stress and related defenses during treatment of mice with acetylsalicylic acid and other peroxisome proliferators. J. Biochem. Toxicol. 10, 87-94.
5. Calafat, A. M., Kuklenyik, Z., Caudill, S. P., Reidy, J. A., and Needham, L. L. (2006). Perfluorochemicals in pooled serum samples from United States residents in 2001 and 2002. Environ. Sci. Technol. 40, 2128-2134.
6. Chen, C., Staudinger, J. L., and Klaassen, C. D. (2003). Nuclear receptor, pregnane X receptor, is required for induction of UDP-glucuronosyl tranferases in mouse liver by pregnenolone-16 alpha-carbonitrile. Drug Metab. Dispos. 31, 908-915.
7. Cheng, X., and Klaassen, C. D. (2006). Regulation of mRNA expression of xenobiotic transporters by the pregnane-X receptor (PXR) in mouse liver, kidney, and intestine. Drug Metab. Dispos. 34, 1863-1867.
8. Cheng, X., Maher, J., Chen, C., and Klaassen, C. D. (2005). Tissue distribution and ontogeny of mouse organic anion transporting polypeptides (Oatps). Drug Metab. Dispos. 33, 1062-1073.
9. Chinje, E., Kentish, P., Jarnot, B., George, M., and Gibson, G. (1994). Induction of the CYP4A subfamily by perfluorodecanoic acid: The rat and the guinea pig as susceptible and non-susceptible species. Toxicol. Lett. 71, 69-75.
10. Cimini, A., Cristiano, L., Bernardo, A., Farioli-Vecchioli, S., Stefanini, S., and Ceru, M. P. (2000). Presence and inducibility of peroxisomes in a human glioblastoma cell line. Biochim. Biophys. Acta 1474, 397-409.
11. De Silva, A. O., and Mabury, S. A. (2006). Isomer distribution of perfluorocarboxylates in human blood: Potential correlation to source. Environ. Sci. Technol. 40, 2903-2909.
12. Denison, M. S., and Deal, R. M. (1990). The binding of transformed aromatic hydrocarbon (Ah) receptor to its DNA recognition site is not affected by metal depletion. Mol. Cell. Endocrinol. 69, 51-57.
13. Falandysz, J., Taniyasu, S., Gulkowska, A., Yamashita, N., and Schulte-Oehlmann, U. (2006). Is fish a major source of fluorinated surfactants and repellents in humans living on the Baltic Coast? Environ. Sci. Technol. 40, 748-751.
14. Gouni-Berthold, I., and Krone, W. (2005). Peroxisome proliferator-activated receptor alpha (PPARalpha) and athero-sclerosis. Curr. Drug Targets Cardiovasc. Haematol. Disord. 5, 513-523.
15. Guo, G. L., Lambert, G., Negishi, M., Ward, J. M., Brewer, H. B., Jr., Kliewer, S. A., Gonzalez, F. J., and Sinal, C. J. (2003). Complementary roles of farnesoid X receptor, pregnane X receptor, and constitutive androstane receptor in protection against bile acid toxicity. J. Biol. Chem. 278, 45062-45071.
16. Guo, D., Sarkar, J., Suino-Powell, K., Xu, Y., Matsumoto, K., Jia, Y., Yu, S., Khare, S., Haldar, K., Rao, M. S., et al. (2007). Induction of nuclear translocation of constitutive androstane receptor by peroxisome proliferator-activated receptor alpha synthetic ligands in mouse liver. J. Biol. Chem. 282, 36766-36776.
17. Hartley, D. P., and Klaassen, C. D. (2000). Detection of chemical-induced differential expression of rat hepatic cytochrome P450 mRNA transcripts using branched DNA signal amplification technology. Drug Metab. Dispos. 28, 608-616.
18. Honkakoski, P., Zelko, I., Sueyoshi, T., and Negishi, M. (1998). The nuclear orphan receptor CAR-retinoid X receptor heterodimer activates the phenobarbital-responsive enhancer module of the CYP2B gene. Mol. Cell. Biol. 18, 5652-5658.
19. Johnson, D. R., and Klaassen, C. D. (2002). Regulation of rat multidrug resistance protein 2 by classes of prototypical microsomal enzyme inducers that activate distinct transcription pathways. Toxicol. Sci. 67, 182-189.
20. Kudo, N., Bandai, N., Suzuki, E., Katakura, M., and Kawashima, Y. (2000). Induction by perfluorinated fatty acids with different carbon chain length of peroxisomal beta-oxidation in the liver of rats. Chem. Biol. Interact. 124, 119-132.
21. Langley, A. E. (1990). Effects of perfluoro-n-decanoic acid on the respiratory activity of isolated rat liver mitochondria. J. Toxicol. Environ. Health. 29, 329-336.
22. Lee, S. S., Pineau, T., Drago, J., Lee, E. J., Owens, J. W., Kroetz, D. L., Fernandez-Salguero, P. M., Westphal, H., and Gonzalez, F. J. (1995). Targeted disruption of the alpha isoform of the peroxisome proliferator-activated receptor gene in mice results in abolishment of the pleiotropic effects of peroxisome proliferators. Mol. Cell. Biol. 15, 3012-3022.
23. Marschall, H. U., Wagner, M., Bodin, K., Zollner, G., Fickert, P., Gumhold, J., Silbert, D., Fuchsbichler, A., Sjovall, J., and Trauner, M. (2006). Fxr(-/-) mice adapt to biliary obstruction by enhanced phase I detoxification and renal elimination of bile acids. J. Lipid Res. 47, 582-592.
24. Pacyniak, E. K., Cheng, X., Cunningham, M. L., Crofton, K., Klaassen, C. D., and Guo, G. L. (2007). The flame retardants, polybrominated diphenyl ethers, are pregnane X receptor activators. Toxicol. Sci. 97 94-102.
25. Rosen, M. B., Lee, J. S., Ren, H., Vallanat, B., Liu, J., Waalkes, M. P., Abbott, B. D., Lau, C., and Corton, J. C. (2008). Toxicogenomic Dissection of the perfluorooctanoic acid transcript profile in mouse liver: Evidence for the involvement of nuclear receptors PPAR{alpha} and CAR. Toxicol. Sci. 103, 46-56.
26. Schuetz, E. G., Strom, S., Yasuda, K., Lecureur, V., Assem, M., Brimer, C., Lamba, J., Kim, R. B., Ramachandran, V., Komoroski, B. J., et al. (2001). Disrupted bile acid homeostasis reveals an unexpected interaction among nuclear hormone receptors, transporters, and cytochrome P450. J. Biol. Chem. 276, 39411-39418.
27. Sinal, C. J., Tohkin, M., Miyata, M., Ward, J. M., Lambert, G., and Gonzalez, F. J. (2000). Targeted disruption of the nuclear receptor FXR/ BAR impairs bile acid and lipid homeostasis. Cell 102, 731-744.
28. Sinclair, E., Mayack, D. T., Roblee, K., Yamashita, N., and Kannan, K. (2006). Occurrence of perfluoroalkyl surfactants in water, fish, and birds from New York State. Arch. Environ. Contam. Toxicol. 50 398-410.
29. Smithwick, M., Muir, D. C., Mabury, S. A., Solomon, K. R., Martin, J. W., Sonne, C., Born, E. W., Letcher, R. J., and Dietz, R. (2005). Perfluoroalkyl contaminants in liver tissue from East Greenland polar bears (Ursus maritimus). Environ. Toxicol. Chem. 24, 981-986.
30. So, M. K., Yamashita, N., Taniyasu, S., Jiang, Q., Giesy, J. P., Chen, K., and Lam, P. K. (2006). Health risks in infants associated with exposure to perfluorinated compounds in human breast milk from Zhoushan, China. Environ. Sci. Technol. 40, 2924-2929.
31. Staudinger, J. L., Goodwin, B., Jones, S. A., Hawkins-Brown, D., MacKenzie, K. I., LaTour, A., Liu, Y., Klaassen, C. D., Brown, K. K., Reinhard, J., et al. (2001). The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc. Natl. Acad. Sci. U. S. A. 98, 3369-3374.
32. Takagi, A., Sai, K., Umemura, T., Hasegawa, R., and Kurokawa, Y. (1991). Short-term exposure to the peroxisome proliferators, perfluorooctanoic acid and perfluorodecanoic acid, causes significant increase of 8-hydroxydeoxyguanosine in liver DNA of rats. Cancer Lett. 57 55-60.
33. Ueda, A., Hamadeh, H. K., Webb, H. K., Yamamoto, Y., Sueyoshi, T., Afshari, C. A., Lehmann, J. M., and Negishi, M. (2002). Diverse roles of the nuclear orphan receptor CAR in regulating hepatic genes in response to phenobarbital. Mol. Pharmacol. 61, 1-6.
34. Vanden Heuvel, J. P., Kuslikis, B. I., Van Rafelghem, M. J., and Peterson, R. E. (1991a). Disposition of perfluorodecanoic acid in male and female rats. Toxicol. Appl. Pharmacol. 107, 450-459.
35. Vanden Heuvel, J. P., Kuslikis, B. I., Van Rafelghem, M. J., and Peterson, R. E. (1991b). Tissue distribution, metabolism, and elimination of perfluorooctanoic acid in male and female rats. J. Biochem. Toxicol. 6, 83-92.
36. Vanden Heuvel, J. P., Thompson, J. T., Frame, S. R., and Gillies, P. J. (2006). Differential activation of nuclear receptors by perfluorinated fatty acid analogs and natural fatty acids: A comparison of human, mouse, and rat peroxisome proliferator-activated receptor-alpha, -beta, and -gamma, liver X receptor-beta, and retinoid X receptor-alpha. Toxicol. Sci. 92, 476-489.
37. Van Rafelghem, M. J., Mattie, D. R., Bruner, R. H., and Andersen, M. E. (1987). Pathological and hepatic ultrastructural effects of a single dose of perfluoro-n-decanoic acid in the rat, hamster, mouse, and guinea pig. Fundam. Appl. Toxicol. 9, 522-540.
38. Whitlock, J. P., Jr. (1999). Induction of cytochrome P4501A1. Annu. Rev. Pharmacol. Toxicol. 39, 103-125.
39. Xie, W., Barwick, J. L., Simon, C. M., Pierce, A. M., Safe, S., Blumberg, B., Guzelian, P. S., and Evans, R. M. (2000). Reciprocal activation of xenobiotic response genes by nuclear receptors SXR/PXR and CAR. Genes Dev. 14, 3014-3023.
40. Zhao, A., Yu, J., Lew, J. L., Huang, L., Wright, S. D., and Cui, J. (2004). Polyunsaturated fatty acids are FXR ligands and differentially regulate expression of FXR targets. DNA Cell. Biol. 23, 519-526.