Human and rat primary hepatocyte CYP1A1 and 1A2 induction with 2,3,7,8-tetrachlorodibenzo-p-dioxin, 2,3,7,8-tetrachlorodibenzofuran, and 2,3,4,7,8-pentachlorodibenzofuran

Toxicological Sciences

Volumn 118, Issue 1, 2010, Pages 224-235

  Budinsky, Robert A ^a   LeCluyse, Edward L ^b   Ferguson, Stephen S ^b   Rowlands, J Craig ^a   Simon, Ted ^c  

^a DOW CHEMICAL COMPANY   (United States)

^b Invitrogen Corporation/CellzDirect   (United States)

^c Ted Simon LLC   (United States)

Author keywords

Aryl hydrocarbon receptor; CYP1A; Dioxin; Enzyme induction; Gene expression; Risk assessment

Indexed keywords

2,3,4,7,8 PENTACHLORODIBENZOFURAN; 2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 2,3,7,8 TETRACHLORODIBENZOFURAN; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; MESSENGER RNA; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DRUG SURVEILLANCE PROGRAM; DUNNETT TEST; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; FEMALE; GENE EXPRESSION; GENE INDUCTION; HILL REACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; LINEAR REGRESSION ANALYSIS; LIVER CELL; LIVER TOXICITY; RISK ASSESSMENT; STATISTICAL ANALYSIS; WELCH ASPIN TEST;

ANIMALS; BENZOFURANS; CELLS, CULTURED; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1A2; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; ENZYME INDUCTION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEPATOCYTES; HUMANS; NO-OBSERVED-ADVERSE-EFFECT LEVEL; RATS; RECEPTORS, ARYL HYDROCARBON; RISK ASSESSMENT; SPECIES SPECIFICITY; TETRACHLORODIBENZODIOXIN;

RATTUS;

EID: 77958495547     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq238     Document Type: Article

References (68)

1. Abraham, K., Geusau, A., Tosun, Y., Helge, H., Bauer, S., and Brockmoller, J. (2002). Severe 2,3,7,8-tetrachorodibenzo-p-dioxin (TCDD) intoxication: insights into the measurement of hepatic cytochrome P450 IA2 induction. Clin. Pharmacol. Ther. 72, 163-174.
2. Aylward, L. L., Brunet, R. C., Carrier, G., Hays, S. M., Cushing, C. A., Needham, L. L., Patterson, D. G., Jr., Gerthoux, P. M., Brambilla, P., and Mocarelli, P. (2004). Concentration-dependent TCDD elimination kinetics in humans: toxicokinetic modeling for moderately to highly exposed adults from Seveso, Italy, and Vienna, Austria, and impact on dose estimates for the NIOSH cohort. J. Expo. Anal. Environ. Epidemiol. 15, 51-65.
3. Aylward, L. L., Goodman, J. E., Charnley, G., and Rhomberg, L. R. (2008). A margin-of-exposure approach to assessment of noncancer risks of dioxins based on human exposure and response data. Environ. Health Perspect. 116, 1344-1351.
4. Aylward, L. L., Lamb, J. C., and Lewis, S. C. (2005). Issues in risk assessment for developmental effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds. Toxicol. Sci. 87, 3-10.
5. Barker, C. W., Fagan, J. B., and Pasco, D. S. (1992). Interleukin-1 beta suppresses the induction of P4501A1 and P4501A2 mRNAs in isolated hepatocytes. J. Biol. Chem. 267, 8050-8055.
6. Budinsky, R. A., Paustenbach, D., Fontaine, D., Landenberger, B., and Starr, T. B. (2006). Recommended relative potency factors for 2,3,4,7,8-pentachlorodibenzofuran: the impact of different dose metrics. Toxicol. Sci. 91, 275-285.
7. Budinsky, R. A., Rowlands, J. C., Casteel, S., Fent, G., Cushing, C. A., Newsted, J., Giesy, J. P., Ruby, M. V., and Aylward, L. L. (2008). A pilot study of oral bioavailability of dioxins and furans from contaminated soils: impact of differential hepatic enzyme activity and species differences. Chemosphere 70, 1774-1786.
8. Chen, Q., Garabrant, D. H., Hedgeman, E., Little, R. J., Elliott, M. R., Gillespie, B., Hong, B., Lee, S. Y., Lepkowski, J. M., Franzblau, A., et al. (2010). Estimation of background serum 2,3,7,8-TCDD concentrations by using quantile regression in the UMDES and NHANES populations. Epidemiology 21, S51-S57.
9. Collins, J. J., Bodner, K., Aylward, L. L., Wilken, M., and Bodnar, C. M. (2009). Mortality rates among trichlorophenol workers with exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Am. J. Epidemiol. 170, 501-506.
10. Connor, K. T., and Aylward, L. L. (2006). Human response to dioxin: aryl hydrocarbon receptor (AhR) molecular structure, function, and dose-response data for enzyme induction indicate an impaired human AhR. J. Toxicol. Environ. Health B Crit. Rev. 9, 147-171.
11. Connor, K. T., Harris, M. A., Edwards, M. R., Budinsky, R. A., Clark, G. C., Chu, A. C., Finley, B. L., and Rowlands, J. C. (2008). AH receptor agonist activity in human blood measured with a cell-based bioassay: evidence for naturally occurring AH receptor ligands in vivo. J. Expo. Sci. Environ. Epidemiol. 18, 369-380.
12. DeVito, M. J., Ross, D. G., Dupuy, A. E., Jr., Ferrario, J., McDaniel, D., and Birnbaum, L. S. (1998). Dose-response relationships for disposition and hepatic sequestration of polyhalogenated dibenzo-p-dioxins, dibenzofurans, and biphenyls following subchronic treatment in mice. Toxicol. Sci. 46, 223-234.
13. Diliberto, J. J., Burgin, D., and Birnbaum, L. S. (1997). Role of CYP1A2 in hepatic sequestration of dioxin: studies using CYP1A2 knock-out mice. Biochem. Biophys. Res. Commun. 236, 431-433.
14. Diliberto, J. J., DeVito, M. J., Ross, D. G., and Birnbaum, L. S. (2001). Subchronic exposure of [3H]-2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in female B6C3F1 mice: relationship of steady-state levels to disposition and metabolism. Toxicol. Sci. 61, 241-255.
15. Drahushuk, A. T., McGarrigle, B. P., Tai, H. L., Kitareewan, S., Goldstein, J. A., and Olson, J. R. (1996). Validation of precision-cut liver slices in dynamic organ culture as an in vitro model for studying CYP1A1 and CYP1A2 induction. Toxicol. Appl. Pharmacol. 140, 393-403.
16. Drahushuk, A. T., McGarrigle, B. P., Larsen, K. E., Stegeman, J. J., and Olson, J. R. (1998). Detection of CYP1A1 protein in human liver and induction by TCDD in precision-cut liver slices incubated in dynamic organ culture. Carcinogenesis 19, 1361-1368.
17. Drahushuk, A. T., McGarrigle, B. P., Slezak, B., Stegeman, J. J., and Olson, J. R. (1999). Time-and concentration-dependent induction of CYP1A1 and CYP1A2 in precision-cut rat liver slices incubated in dynamic organ culture in the presence of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 155, 127-138.
18. Ema, M., Ohe, N., Suzuki, M., Mimura, J., Sogawa, K., Ikawa, S., and Fujii-Kuriyama, Y. (1994). Dioxin binding activities of polymorphic forms of mouse and human arylhydrocarbon receptors. J. Biol. Chem. 269, 27337-27343.
19. Ferriby, L. L., Knutsen, J. S., Harris, M., Unice, K. M., Scott, P., Nony, P., Haws, L. C., and Paustenbach, D. (2006). Evaluation of PCDD/F and dioxin-like PCB serum concentration data from the 2001-2002 National Health and Nutrition Examination Survey of the United States population. J. Expo. Sci. Environ. Epidemiol. 17, 358-371.
20. Gaylor, D. W., and Aylward, L. L. (2004). An evaluation of benchmark dose methodology for non-cancer continuous-data health effects in animals due to exposures to dioxin (TCDD). Regul. Toxicol. Pharmacol. 40, 9-17.
21. Goutelle, S., Maurin, M., Rougier, F., Barbaut, X., Bourguignon, L., Ducher, M., and Maire, P. (2008). The Hill equation: a review of its capabilities in pharmacological modelling. Fundam. Clin. Pharmacol. 22, 633-648.
22. Guzelian, P., Quattrochi, L., Karch, N., Aylward, L., and Kaley, R. (2006). Does dioxin exert toxic effects in humans at or near current background body levels?: an evidence-based conclusion. Hum. Exp. Toxicol. 25, 99-105.
23. Halperin, W., Kalow, W., Sweeney, M. H., Tang, B. K., Fingerhut, M., Timpkins, B., and Wille, K. (1995). Induction of P-450 in workers exposed to dioxin. Occup. Environ. Med. 52, 86-91.
24. Haws, L. C., Su, S. H., Harris, M., DeVito, M. J., Walker, N. J., Farland, W. H., Finley, B., and Birnbaum, L. S. (2006). Development of a refined database of mammalian relative potency estimates for dioxin-like compounds. Toxicol. Sci. 89, 4-30.
25. Hedgeman, E., Chen, Q., Hong, B., Chang, C. W., Olson, K., Ladronka, K., Ward, B., Adriaens, P., Demond, A., Gillespie, B. W., et al. (2009). The University of Michigan Dioxin Exposure Study: population survey results and serum concentrations for polychlorinated dioxins, furans, and biphenyls. Environ. Health. Perspect. 117, 811-817.
26. Huwe, J. K., and Larsen, G. L. (2005). Polychlorinated dioxins, furans, and biphenyls, and polybrominated diphenyl ethers in a U.S. meat market basket and estimates of dietary intake. Environ. Sci. Technol. 39, 5606-5611.
27. Jackson, J. P., Kabirov, K. K., Kapetanovic, I. M., and Lyubimov, A. (2009). In vitro assessment of P450 induction potential of novel chemopreventive agents SR13668, 9-cis-UAB30, and pentamethychromanol in primary cultures of human hepatocytes. Chem. Biol. Interact. 179, 263-272.
28. Kishida, T., Muto, S., Hayashi, M., Tsutsui, M., Tanaka, S., Murakami, M., and Kuroda, J. (2008). Strain differences in hepatic cytochrome P450 1A and 3A expression between Sprague Dawley and Wistar rats. J. Toxicol. Sci. 33, 447-457.
29. Kociba, R. J., Keyes, D. G., Beyer, J. E., Carreon, R. M., Wade, C. E., Dittenber, D. A., Kalnins, R. P., Frauson, L. E., Park, C. N., Barnard, S. D., et al. (1978). Results of a two-year chronic toxicity and oncogenicity study of 2,3,7,8-tetrachlorodibenzo-p-dioxin in rats. Toxicol. Appl. Pharmacol. 46, 279-303.
30. LeCluyse, E. L. (2001). Human hepatocyte culture systems for the in vitro evaluation of cytochrome P450 enzyme expression and regulation. Eur. J. Pharm. Sci. 13, 343-341.
31. LeCluyse, E. L., Madan, A., Hamilton, G., Corrol, K., Dehaan, R., and Parkinson, A. (2000). Expression and regulation of cytochrome P450 enzymes in primary cultures of human hepatocytes. J. Biochem. Mol. Toxicol. 14, 177-188.
32. Liu, N., Zhang, Q. Y., Vakharia, D., Dunbar, D., and Kaminsky, L. S. (2001). Induction of CYP1A by benzo[k]fluoranthene in human hepatocytes: CYP1A1 or CYP1A2? Arch. Biochem. Biophys. 389, 130-134.
33. Lutz, W. K., and Lutz, R. W. (2009). Statistical model to estimate a threshold dose and its confidence limits for the analysis of sublinear dose-response relationships, exemplified for mutagenicity data. Mutat. Res. 678, 118-122.
34. Maruyama, W., and Aoki, Y. (2006). Estimated cancer risk of dioxins to humans using a bioassay and physiologically based pharmacokinetic model. Toxicol. Appl. Pharmacol. 214, 188-198.
35. McKinley, M. K., Kedderis, L. B., and Birnbaum, L. S. (1993). The effect of pretreatment on the biliary excretion of 2,3,7,8-tetrachlorodibenzo-p-dioxin, 2,3,7,8-tetrachlorodibenzofuran, and 3,3′,4,4′ tetrachlorodiphenyl in the rat. Fundam. Appl. Toxicol. 21, 425-432.
36. Meredith, C., Scott, M. P., Renwick, A. B., Price, R. J., and Lake, B. G. (2003). Studies on the induction of rat hepatic CYP1A, CYP2B, CYP3A and CYP4A subfamily form mRNAs in vivo and in vitro using precision-cut rat liver slices. Xenobiotica 33, 511-527.
37. Meunier, V., Bourrie, M., Julian, B., Marti, E., Guillou, F., Berger, Y., and Fabre, G. (2000). Expression and induction of CYP1A1/1A2, CYP2A6 and CYP3A4 in primary cultures of human hepatocytes: a 10-year follow-up. Xenobiotica 30, 589-607.
38. Mitchell, K. A., and Elferink, C. J. (2009). Timing is everything: consequences of transient and sustained AhR activity. Biochem. Pharmacol. 77, 947-956.
39. Moriguchi, T., Motohashi, H., Hosoya, T., Nakajima, O., Takahashi, S., Ohsako, S., Aoki, Y., Nishimura, N., Tohyama, C., Fujii-Kuriyama, Y., et al. (2003). Distinct response to dioxin in an arylhydrocarbon receptor (AHR)-humanized mouse. Proc. Natl. Acad. Sci. U.S.A. 100, 5652-5657.
40. National Toxicology Program (NTP). (2006a). NTP technical report on the toxicology and carcinogenesis studies of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) (CAS No. 1746-01-6) in female Harlan Sprague-Dawley rats (Gavage Studies). Natl. Toxicol. Program Tech. Rep. Ser. 1.
41. National Toxicology Program (NTP). (2006b). NTP toxicology and carcino-genesis studies of 2,3,4,7,8-pentachlorodibenzofuran (PeCDF) (CAS No. 57117-31-4) in female Harlan Sprague-Dawley rats (Gavage Studies). Natl. Toxicol. Program Tech. Rep. Ser. 1-198.
42. Office of Environmental Health Hazard Assessment (OEHHA). (2005). DRAFT Public Health Goal for TCDD in Drinking Water. Pesticide and Environmental Toxicology Branch, Sacramento and Oakland, CA.
43. Olson, J. R., McGarrigle, B. P., Gigliotti, P. J., Kumar, S., and McReynolds, J. H. (1994). Hepatic uptake and metabolism of 2,3,7,8-tetrachlorodibenzo-p-dioxin and 2,3,7,8-tetrachlorodibenzofuran. Fundam. Appl. Toxicol. 22, 631-640.
44. Ooe, H., Kon, J., Miyamoto, S., Ozone, Y., Ninomiya, S., and Mitaka, T. (2006). Cytochrome p450 expression of cultured rat small hepatocytes after long-term cryopreservation. Drug. Metab. Dispos. 34, 1667-1671.
45. Pohjanvirta, R., Nittynen, M., Linden, J., Boutrous, P. C., Moffat, I. D., and Okey, A. B. (2006). Evaluation of various housekeeping genes for their applicability for normalization of mRNA expression in dioxin-treated rats. Chem. Biol. Interact. 160, 134-149.
46. Procopio, M., Lahm, A., Tramontano, A., Bonati, L., and Pitea, D. (2002). A model for recognition of polychlorinated dibenzo-p-dioxins by the aryl hydrocarbon receptor. Eur. J. Biochem. 269, 13-18; 2619 [pii].
47. Richert, L., Tuschl, G., Abadie, C., Blanchard, N., Pekthong, D., Mantion, G., Weber, J. C., and Mueller, S. O. (2009). Use of mRNA expression to detect the induction of drug metabolising enzymes in rat and human hepatocytes. Toxicol. Appl. Pharmacol. 235, 86-96.
48. Rowlands, J., Budinsky, R., Gollapudi, B., Drinkwater, K., and Storck, M. (2008). The human AHR: identification of single nucleotide polymorphisms from six ethnic populations. Organohalogen. Compd. 70, 2107-2111.
49. Schecter, A. J., Sheu, S. U., Birnbaum, L. S., DeVito, M. J., Denison, M. S., and Papke, O. (1999). A comparison and discussion of two differing methods of measuring dioxin-like compounds: gas chromatography-mass spectrometry and the CALUX bioassay-implications for health studies. Org. Halogen. Cmpds. 40, 247-250.
50. Schrenk, D., Stuven, T., Gohl, G., Viebahn, R., and Bock, K. W. (1995). Induction of CYP1A and glutathione S-transferase activities by 2,3,7,8-tetrachlorodibenzo-p-dioxin in human hepatocyte cultures. Carcinogenesis 16, 943-946.
51. Schweikl, H., Taylor, J. A., Kitareewan, S., Linko, P., Nagorney, D., and Goldstein, J. A. (1993). Expression of CYP1A1 and CYP1A2 genes in human liver. Pharmacogenetics 3, 239-249.
52. Silkworth, J. B., Koganti, A., Illouz, K., Possolo, A., Zhao, M., and Hamilton, S. B. (2005). Comparison of TCDD and PCB CYP1A induction sensitivities in fresh hepatocytes from human donors, sprague-dawley rats, and rhesus monkeys and HepG2 cells. Toxicol. Sci. 87, 508-519.
53. Simon, T., Kirman, C. R., Aylward, L. L., Budinsky, R. A., Rowlands, J. C., and Long, T. F. (2008). Estimates of cancer potency of 2,3,4,7,8-pentachlorodibenzofuran using both nonlinear and linear approaches. Toxicol. Sci. 106, 519-537.
54. Simon, T., Aylward, L. L., Kirman, C. R., Rowlands, J. C., and Budinsky, R. A. (2009). Estimates of cancer potency of 2,3,7,8-tetrachlorodibenzo(p)dioxin using linear and nonlinear dose-response modeling and toxicokinetics. Toxicol. Sci. 112, 490-506.
55. Tai, H. L., McReynolds, Goldstein, J. A., Eugster, H. P., Sengstag, C., Alworth, W. L., and Olson, J. R. (1993). Cytochrome P4501A1 mediates the metabolism of 2,3,7,8-tetrachlorodibenzofuran in the rat and human. Toxicol. Appl. Pharmacol. 123, 34-42.
56. Till, M., Riebniger, D., Schmitz, H. J., and Schrenk, D. (1999). Potency of various polycyclic aromatic hydrocarbons as inducers of CYP1A1 in rat hepatocyte cultures. Chem. Biol. Interact. 117, 135-150.
57. Tritscher, A. M., Goldstein, J. A., Portier, C. J., McCoy, Z., Clark, G. C., and Lucier, G. W. (1992). Dose-response relationships for chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin in a rat tumor promotion model: quantification and immunolocalization of CYP1A1 and CYP1A2 in the liver. Cancer. Res. 52, 3436-3442.
58. U.S. Environmental Protection Agency. (2002). A review of the reference dose and reference concentration processes. EPA/630/P-02/002F. December 2002. Final Report.
59. van den Berg, M., Birnbaum, L., Bosveld, A. T., Brunstrom, B., Cook, P., Feeley, M., Giesy, J. P., Hanberg, A., Hasegawa, R., Kennedy, S. W., et al. (1998). Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ. Health Perspect. 106, 775-792.
60. van den Berg, M., Birnbaum, L. S., Denison, M., De, V. M., Farland, W., Feeley, M., Fiedler, H., Hakansson, H., Hanberg, A., Haws, L., et al. (2006). The 2005 World Health Organization reevaluation of human and Mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol. Sci. 93, 223-241.
61. Vanden Heuvel, J. P., Clark, G. C., Kohn, M. C., Tritscher, A. M., Greenlee, W. F., Lucier, G.w, and Bell, D. A. (1994). Dioxin-responsive genes: examination of dose-response relationships using quantitative reverse transciptase-polymerase chain reaction. Cancer Res. 54, 62-68.
62. Vrzal, R., Daujat-Chavanieu, M., Pascussi, J. M., Ulrichova, J., Maurel, P., and Dvorak, Z. (2008). Microtubules-interfering agents restrict aryl hydrocarbon receptor-mediated CYP1A2 induction in primary cultures of human hepatocytes via c-jun-N-terminal kinase and glucocorticoid receptor. Eur. J. Pharmacol. 581, 244-254.
63. Vrzal, R., Stejskalova, L., Monostory, K., Maurel, P., Bachleda, P., Pavek, P., and Dvorak, Z. (2009). Dexamethasone controls aryl hydrocarbon receptor (AhR)-mediated CYP1A1 and CYP1A2 expression and activity in primary cultures of human hepatocytes. Chem. Biol. Interact. 179, 288-296.
64. Walker, N. J., Crockett, P. W., Nyska, A., Brix, A. E., Jokinen, M. P., Sells, D. M., Hailey, J. R., Easterling, M., Haseman, J. K., Yin, M., et al. (2005). Dose-additive carcinogenicity of a defined mixture of "dioxin-like compounds". Environ. Health Perspect. 113, 43-48.
65. World Health Organization-International Programme on Chemical Safety (WHO-IPCS). (2005). Chemical-Specific Adjustment Factors for Interspecies Differences and Human Variability: Guidance Document for Use of Data in Dose/Concentration Response Assessment Harmonization Project Document No. 2. Available at: http://www.who.int/ipcs/methods/harmonization/areas/uncertainty/en/index.html. Accessed February 15, 2009.
66. Xu, L., Li, A. P., Kaminski, D. L., and Ruh, M. F. (2000). 2,3,7,8 Tetrachlorodibenzo-p-dioxin induction of cytochrome P4501A in cultured rat and human hepatocytes. Chem. Biol. Interact. 124, 173-189.
67. Zhang, Z. Y., Pelletier, R. D., Wong, Y. N., SugawaraZhao, N., and Littlefield, B. A. (2006). Preferrential inducibility of CYP1A1 and CYP1A2 by TCDD: differential regulation in primary human hepatocytes versus transformed cells. Biochem. Biophys. Res. Com. 341, 399-407.
68. Zwiernik, M. J., Bursian, S., Aylward, L. L., Kay, D. P., Moore, J., Rowlands, C., Woodburn, K., Shotwell, M., Khim, J. S., Giesy, J. P., et al. (2008). Toxicokinetics of 2,3,7,8-TCDF and 2,3,4,7,8-PeCDF in mink (Mustela vison) at ecologically relevant exposures. Toxicol. Sci. 105, 33-43.