Critical role of PPAR-α in perfluorooctanoic acid- and perfluorodecanoic acid-induced downregulation of oatp uptake transporters in mouse livers

Toxicological Sciences

Volumn 106, Issue 1, 2008, Pages 37-45

  Cheng, Xingguo ^a   Klaassen, Curtis D ^a  

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

Author keywords

Na+ taurocholate cotransporting polypeptide (Ntcp); Organic anion transporting polypeptide (Oatp); Perfluorodecanoic acid (PFDA); Perfluorooctanoic acid (PFOA); Peroxisome proliferator activated receptor alpha (PPAR )

Indexed keywords

BILE ACID; CARRIER PROTEIN; CELL PROTEIN; CONSTITUTIVE ANDROSTANE RECEPTOR; FARNESOID X RECEPTOR; MESSENGER RNA; ORGANIC ANION TRANSPORTER POLYPEPTIDE; ORGANIC ANION TRANSPORTER POLYPEPTIDE 1A1; ORGANIC ANION TRANSPORTER POLYPEPTIDE 1A4; ORGANIC ANION TRANSPORTER POLYPEPTIDE 1B2; PERFLUORODECANOIC ACID; PERFLUOROOCTANOIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PREGNANE X RECEPTOR; SODIUM TAUROCHOLATE COTRANSPORTING POLYPEPTIDE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILE ACID BLOOD LEVEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; LIVER PARENCHYMA; MALE; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RECEPTOR UPREGULATION; TOXICOKINETICS;

ANIMALS; BILE ACIDS AND SALTS; DECANOIC ACIDS; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ENVIRONMENTAL POLLUTANTS; FLUOROCARBONS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; OCTANOIC ACIDS; ORGANIC ANION TRANSPORTERS; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; ORGANIC ANION TRANSPORTERS, SODIUM-INDEPENDENT; PPAR ALPHA; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, STEROID; RNA, MESSENGER; SYMPORTERS; TRANSCRIPTION FACTORS;

MUS;

EID: 54349084084     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn161     Document Type: Article

References (77)

1. Abdellatif, A. G., Preat, V., Taper, H. S., and Roberfroid, M. (1991). The modulation of rat liver carcinogenesis by perfluorooctanoic acid, a peroxisome proliferator. Toxicol. Appl. Pharmacol. 111, 530-537.
2. 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.
3. 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.
4. Aleksunes, L. M., Scheffer, G. L., Jakowski, A. B., Pruimboom-Brees, I. M., and Manautou, J. E. (2006). Coordinated expression of multidrug resistance-associated proteins (Mrps) in mouse liver during toxicant-induced injury. Toxicol. Sci. 89, 370-379.
5. Bookstaff, R. C., Moore, R. W., Ingall, G. B., and Peterson, R. E. (1990). Androgenic deficiency in male rats treated with perfluorodecanoic acid. Toxicol. Appl. Pharmacol. 104, 322-333.
6. Borges, T., Peterson, R. E., Pitot, H. C., Robertson, L. W., and Glauert, H. P. (1993). Effect of the peroxisome proliferator perfluorodecanoic acid on the promotion of two-stage hepatocarcinogenesis in rats. Cancer Lett. 72, 111-120.
7. Boujrad, N., Vidic, B., Gazouli, M., Culty, M., and Papadopoulos, V. (2000). The peroxisome proliferator perfluorodecanoic acid inhibits the peripheral-type benzodiazepine receptor (PBR) expression and hormone-stimulated mitochondrial cholesterol transport and steroid formation in Leydig cells. Endocrinology 141, 3137-3148.
8. 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.
9. 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.
10. Calafat, A. M., Kuklenyik, Z., Reidy, J. A., Caudill, S. P., Tully, J. S., and Needham, L. L. (2007a). Serum concentrations of 11 polyfluoroalkyl compounds in the u.s. population: Data from the national health and nutrition examination survey (NHANES). Environ. Sci. Technol. 41, 2237-2242.
11. Calafat, A. M., Wong, L. Y., Kuklenyik, Z., Reidy, J. A., and Needham, L. L. (2007b). Polyfluoroalkyl chemicals in the U.S. population: Data from the National Health and Nutrition Examination Survey (NHANES) 2003-2004 and comparisons with NHANES 1999-2000. Environ. Health Perspect. 115, 1596-1602.
12. Cheng, X., Buckley, D., and Klaassen, C.D. (2007). Regulation of hepatic bile acid transporters Ntcp and Bsep expression. Biochem. Pharmacol. 74, 1665-1676.
13. 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.
14. Cheng, X., Maher, J., Chen, C., and Klaassen, C. D. (2005a). Tissue distribution and ontogeny of mouse organic anion transporting polypeptides (Oatps). Drug Metab. Dispos. 33, 1062-1073.
15. Cheng, X., Maher, J. M., Dieter, M. Z., and Klaassen, C. D. (2005b). Regulation of mouse organic anion-transporting polypeptides (Oatps) in liver by prototypical microsomal enzyme inducers that activate distinct transcription factor pathways. Drug Metab. Dispos. 33, 1276-1282.
16. Cheng, X., Maher, J. M., Lu, H., and Klaassen, C. D. (2006). Endocrine regulation of gender-divergent mouse organic anion transporting polypeptide (Oatp) expression. Mol. Pharmacol. 70, 1291-1297.
17. 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.
18. De Silva, A. O., and Mabury, S. A. (2004). Isolating isomers of perfluorocarboxylates in polar bears (Ursus maritimus) from two geographical locations. Environ. Sci. Technol. 38, 6538-6545.
19. 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.
20. Fei, C., McLaughlin, J. K., Tarone, R. E., and Olsen, J. (2007). Perfluorinated chemicals and fetal growth: A study within the Danish National Birth Cohort. Environ. Health Perspect. 115, 1677-1682.
21. Gannon, J. T. H. R., Kaiser, M. A., and Mueller, T. (2006). Review II: Perfluorooctanoic acid (PFOA) in the environment. White paper by DuPont Wilmington. DE. Report Number: DuPont-19567. US EPA Administrative Record. AR-226-3679.
22. George, M. E., and Andersen, M. E. (1986). Toxic effects of nonadecafluoro-n-decanoic acid in rats. Toxicol. Appl. Pharmacol. 85, 169-180.
23. 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.
24. Guo, G. L., Johnson, D. R., and Klaassen, C. D. (2002a). Postnatal expression and induction by pregnenolone-16alpha-carbonitrile of the organic anion-transporting polypeptide 2 in rat liver. Drug Metab. Dispos. 30, 283-288.
25. Guo, G. L., Staudinger, J., Ogura, K., and Klaassen, C. D. (2002b). Induction of rat organic anion transporting polypeptide 2 by pregnenolone-16alpha-carbonitrile is via interaction with pregnane X receptor. Mol. Pharmacol. 61, 832-839.
26. Guruge, K. S., Yeung, L. W., Yamanaka, N., Miyazaki, S., Lam, P. K., Giesy, J. P., Jones, P. D., and Yamashita, N. (2006). Gene expression profiles in rat liver treated with perfluorooctanoic acid (PFOA). Toxicol. Sci. 89, 93-107.
27. Hagenbuch, B., and Meier, P. J. (2003). The superfamily of organic anion transporting polypeptides. Biochim. Biophys. Acta 1609, 1-18.
28. Harris, M. W., Uraih, L. C., and Birnbaum, L. S. (1989). Acute toxicity of perfluorodecanoic acid in C57BL/6 mice differs from 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam. Appl. Toxicol. 13 723-736.
29. 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.
30. Houde, M., Martin, J. W., Letcher, R. J., Solomon, K. R., and Muir, D. C. (2006). Biological monitoring of polyfluoroalkyl substances: A review. Environ. Sci. Technol. 40, 3463-3473.
31. Isern, J., Hagenbuch, B., Stieger, B., Meier, P. J., and Meseguer, A. (2001). Functional analysis and androgen-regulated expression of mouse organic anion transporting polypeptide 1 (Oatp1) in the kidney. Biochim. Biophys. Acta 19(1518), 73-78.
32. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., et al. (1997). An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236, 313-322.
33. Jensen, A. A., and Leffers, H. (2008). Emerging endocrine disrupters: Perfluoroalkylated substances. Int. J. Androl. 31, 161-169.
34. Johnson, D. R., Guo, G. L., and Klaassen, C. D. (2002). Expression of rat multidrug resistance protein 2 (Mrp2) in male and female rats during normal and pregnenolone-16alpha-carbonitrile (PCN)-induced postnatal ontogeny. Toxicology 178, 209-219.
35. 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.
36. Kim, S. K., and Kannan, K. (2007). Perfluorinated acids in air, rain, snow, surface runoff, and lakes: Relative importance of pathways to contamination of urban lakes. Environ. Sci. Technol. 41, 8328-8334.
37. Kok, T., Bloks, V. W., Wolters, H., Havinga, R., Jansen, P. L., Staels, B., and Kuipers, F. (2003). Peroxisome proliferator-activated receptor alpha (PPARalpha)-mediated regulation of multidrug resistance 2 (Mdr2) expression and function in mice. Biochem. J. 369, 539-547.
38. Kudo, N., and Kawashima, Y. (1997). Fish oil-feeding prevents perfluorooctanoic acid-induced fatty liver in mice. Toxicol. Appl. Pharmacol. 145, 285-293.
39. Kullak-Ublick, G. A., Stieger, B., Hagenbuch, B., and Meier, P. J. (2000). Hepatic transport of bile salts. Semin. Liver Dis. 20 273-292.
40. 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.
41. Lau, C., Butenhoff, J. L., and Rogers, J. M. (2004). The developmental toxicity of perfluoroalkyl acids and their derivatives. Toxicol. Appl. Pharmacol. 198, 231-241.
42. 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.
43. Leung, L., Kwong, M., Hou, S., Lee, C., and Chan, J. Y. (2003). Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J. Biol. Chem. 278, 48021-48029.
44. Li, N., Hartley, D. P., Cherrington, N. J., and Klaassen, C. D. (2002). Tissue expression, ontogeny, and inducibility of rat organic anion transporting polypeptide 4. J. Pharmacol. Exp. Ther. 301, 551-560.
45. Maher, J. M., Dieter, M. Z., Aleksunes, L. M., Slitt, A. L., Guo, G., Tanaka, Y., Scheffer, G. L., Chan, J. Y., Manautou, J. E., Chen, Y., et al. (2007). Oxidative and electrophilic stress induces multidrug resistance-associated protein transporters via the nuclear factor-E2-related factor-2 transcriptional pathway. Hepatology 46, 1597-1610.
46. Meier, P. J., Eckhardt, U., Schroeder, A., Hagenbuch, B., and Stieger, B. (1997). Substrate specificity of sinusoidal bile acid and organic anion uptake systems in rat and human liver. Hepatology 26, 1667-1677.
47. Meier, P. J., and Stieger, B. (2002). Bile salt transporters. Annu. Rev. Physiol. 64, 635-661.
48. Ogura, K., Choudhuri, S., and Klaassen, C. D. (2000). Full-length cDNA cloning and genomic organization of the mouse liver-specific organic anion transporter-1 (1st-1). Biochem. Biophys. Res. Commun. 272 563-570.
49. Ogura, K., Choudhuri, S., and Klaassen, C. D. (2001). Genomic organization and tissue-specific expression of splice variants of mouse organic anion transporting polypeptide 2. Biochem. Biophys. Res. Commun. 281, 431-439.
50. Olsen, G. W., Church, T. R., Larson, E. B., van Belle, G., Lundberg, J. K., Hansen, K. J., Burris, J. M., Mandel, J. H., and Zobel, L. R. (2004). Serum concentrations of perfluorooctanesulfonate and other fluorochemicals in an elderly population from Seattle, Washington. Chemosphere 54, 1599-1611.
51. Olsen, G. W., Mair, D. C., Reagen, W. K., Ellefson, M. E., Ehresman, D. J., Butenthoff, J. L., and Zobel, L. R. (2007). Preliminary evidence of a decline in perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) concentrations in American Red Cross blood donors. Chemosphere 68, 105-111.
52. Olson, C. T., and Andersen, M. E. (1983). The acute toxicity of perfluorooctanoic and perfluorodecanoic acids in male rats and effects on tissue fatty acids. Toxicol. Appl. Pharmacol. 70, 362-372.
53. Oono, S., Matsubara, E., Harada, K. H., Takagi, S., Hamada, S., Asakawa, A., Inoue, K., Watanabe, I., and Koizumi, A. (2008). Survey of airborne polyfluorinated telomers in Keihan area, Japan. Bull. Environ. Contam. Toxicol. 80, 102-106.
54. Rosen, M. B., Lee, J. S., Ren, H., Vallanat, B., Liu, J., Waalkes, M. P., Abbott, B. D., Lau, C., and Cotton, 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.
55. Semple, R. K., Chatterjee, V. K., and O'Rahilly, S. (2006). PPAR gamma and human metabolic disease. J. Clin. Invest. 116, 581-589.
56. 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.
57. 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.
58. Skutlarek, D., Exner, M., and Farber, H. (2006). Perfluorinated surfactants in surface and drinking waters. Environ. Sci. Pollut. Res. Int. 13, 299-307.
59. Slatter, J. G., Cheng, O., Cornwell, P. D., de Souza, A., Rockett, J., Rushmore, T., Hartley, D., Evers, R., He, Y., Dai, X., et al. (2006). Microarray-based compendium of hepatic gene expression profiles for prototypical ADME gene-inducing compounds in rats and mice in vivo. Xenobiotica 36, 902-937.
60. Son, H. Y., Kim, S. H., Shin, H. I., Bae, H. I., and Yang, J. H. (2008). Perfluorooctanoic acid-induced hepatic toxicity following 21-day oral exposure in mice. Arch. Toxicol. 82, 239-246.
61. Starkov, A. A., and Wallace, K. B. (2002). Structural determinants of fluorochemical-induced mitochondrial dysfunction. Toxicol. Sci. 66, 244-252.
62. Staudinger, J., Liu, Y., Madan, A., Habeebu, S., and Klaassen, C. D. (2001a). Coordinate regulation of xenobiotic and bile acid homeostasis by pregnane X receptor. Drug Metab. Dispos. 29, 1467-1472.
63. 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. (2001b). The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc. Natl. Acad. Sci. U. S. A. 98, 3369-3374.
64. Takacs, M. L., and Abbott, B. D. (2007). Activation of mouse and human peroxisome proliferator-activated receptors (alpha, beta/delta, gamma) by perfluorooctanoic acid and perfluorooctane sulfonate. Toxicol. Sci. 95, 108-117.
65. 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.
66. Tao, L., Kannan, K., Aldous, K. M., Mauer, M. P., and Eadon, G. A. (2008). Biomonitoring of perfluorochemicals in plasma of New York State personnel responding to the World Trade Center disaster. Environ. Sci. Technol. 42, 3472-3478.
67. Trudel, D., Horowitz, L., Wormuth, M., Scheringer, M., Cousins, I. T., and Hungerbuhler, K. (2008). Estimating consumer exposure to PFOS and PFOA. Risk Anal. 28, 251-269.
68. 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.
69. 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.
70. 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.
71. 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.
72. 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.
73. Wei, Y., Liu, Y., Wang, J., Tao, Y., and Dai, J. (2008). Toxicogenomic analysis of the hepatic effects of perfluorooctanoic acid on rare minnows (Gobiocypris rarus). Toxicol. Appl. Pharmacol. 226, 285-297.
74. Wolf, D. C., Moore, T., Abbott, B. D., Rosen, M. B., Das, K. P., Zehr, R. D., Lindstrom, A. B., Strynar, M. J., and Lau, C. (2008). Comparative hepatic effects of perfluorooctanoic acid and WY 14,643 in PPAR-(alpha) knockout and wild-type mice. Toxicol. Pathol. 36, 632-639.
75. Wolters, H., Elzinga, B. M., Baller, J. F., Boverhof, R., Schwarz, M., Stieger, B., Verkade, H. J., and Kuipers, F. (2002). Effects of bile salt flux variations on the expression of hepatic bile salt transporters in vivo in mice. J. Hepatol. 37, 556-563.
76. Yamamoto, A., and Kawashima, Y. (1997). Perfluorodecanoic acid enhances the formation of oleic acid in rat liver. Biochem. J. 325(Pt 2), 429-434.
77. 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.