Comparative temporal toxicogenomic analysis of TCDD- and TCDF-mediated hepatic effects in immature female C57BL/6 mice

Toxicological Sciences

Volumn 103, Issue 2, 2008, Pages 285-297

  N'Jai, Alhaji ^a   Boverhof, Darrell R ^a   Dere, Edward ^a   Burgoon, Lyle D ^a   Tan, Ying S ^a   Rowlands, J Craig ^b   Budinsky, Robert A ^b   Stebbins, Kenneth E ^b   Zacharewski, Timothy R ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b DOW CHEMICAL COMPANY   (United States)

Author keywords

Liver; Microarray; Mouse; TCDD; TCDF; Temporal

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 2,3,7,8 TETRACHLORODIBENZOFURAN; CARBONYL REDUCTASE; CASEIN KINASE II; CATHEPSIN L; CD3 ANTIGEN; CD36 ANTIGEN; CHOLINE DEHYDROGENASE; COMPLEMENTARY DNA; CYTOCHROME P450 1A1; DYSFERLIN; GLUTATHIONE TRANSFERASE ALPHA; GLUTATHIONE TRANSFERASE P1; GLYCINE DEHYDROGENASE (DECARBOXYLATING); GLYOXALASE; HEME OXYGENASE 1; HISTIDINE AMMONIALYASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 7; PROTEIN DNAJ; PROTEIN S24; RIBOSOME PROTEIN; RNA BINDING MOTIF PROTEIN 13; RNA BINDING PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 2; THYMIDINE KINASE 1; THYMOPOIETIN; URIDINE DIPHOSPHATE GLUCOSE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; DNA MICROARRAY; DOSE RESPONSE; ENZYME INDUCTION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; HISTOPATHOLOGY; LIPID STORAGE; LIVER CELL; LIVER TOXICITY; LIVER WEIGHT; MOUSE; NONHUMAN; TOXICOGENETICS; TOXICOKINETICS;

ADMINISTRATION, ORAL; ANIMALS; BENZOFURANS; ENVIRONMENTAL POLLUTANTS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEPATOCYTES; LIVER; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; TETRACHLORODIBENZODIOXIN; TIME FACTORS; TOXICOGENETICS; VACUOLES;

MUS;

EID: 43349092793     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn053     Document Type: Article

References (70)

1. Abbott, B. D., Birnbaum, L. S., and Pratt, R. M. (1987). TCDD-induced hyperplasia of the ureteral epithelium produces hydronephrosis in murine fetuses. Teratology 35, 329-34.
2. Afshari, C. A., Nuwaysir, E. F., and Barrett, J. C. (1999). Application of complementary DNA microarray technology to carcinogen identification, toxicology, and drug safety evaluation. Cancer Res. 59, 4759-60.
3. Ahlborg, U. G. (1994). Human health risk assessment and risk perception related to the Baltic Sea. Arch. Toxicol. Suppl. 16, 53-9.
4. Barnes, D., Alford-Stevens, A., Birnbaum, L., Kutz, F. W., Wood, W., and Patton, D. (1991). Toxicity equivalency factors for PCBs? Qual. Assur. 1, 70-81.
5. Barnes, D. G. (1991). Toxicity equivalents and EPA's risk assessment of 2,3,7,8-TCDD. Sci. Total Environ. 104, 73-86.
6. Birnbaum, L. S. (1986). Distribution and excretion of 2,3,7,8-tetrachlorodibenzo-p-dioxin in congenic strains of mice which differ at the Ah locus. Drug Metab. Dispos. 14, 34-40.
7. Birnbaum, L. S. (1995). Developmental effects of dioxins and related endocrine disrupting chemicals. Toxicol. Lett. 82-83, 743-50.
8. Birnbaum, L. S., and DeVito, M. J. (1995). Use of toxic equivalency factors for risk assessment for dioxins and related compounds. Toxicology 105, 391-401.
9. Birnbaum, L. S., Harris, M. W., Crawford, D. D., and Morrissey, R. E. (1987). Teratogenic effects of polychlorinated dibenzofurans in combination in C57BL/6N mice. Toxicol. Appl. Pharmacol. 91, 246-55.
10. Boverhof, D. R., Burgoon, L. D., Tashiro, C., Chittim, B., Harkema, J. R., Jump, D. B., and Zacharewski, T. R. (2005). Temporal and dose-dependent hepatic gene expression patterns in mice provide new insights into TCDD-Mediated hepatotoxicity. Toxicol. Sci. 85 1048-63.
11. Boverhof, D. R., Burgoon, L. D., Tashiro, C., Sharratt, B., Chittim, B., Harkema, J. R., Mendrick, D. L., and Zacharewski, T. R. (2006). Comparative toxicogenomic analysis of the hepatotoxic effects of TCDD in Sprague Dawley rats and C57BL/6 mice. Toxicol. Sci. 94, 398-416.
12. Budinsky, R. A., Rowlands, J. C., Casteel, S., Fent, G., Cushing, C. A., Newsted, J., Giesy, J. P., Ruby, M., 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, 1774-86.
13. 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, 275-85.
14. Burgoon, L. D., Boutros, P. C., Dere, E., and Zacharewski, T. R. (2006). dbZach: A MIAME-compliant toxicogenomic supportive relational database. Toxicol. Sci. 90, 558-68.
15. Burgoon, L. D., Eckel-Passow, J. E., Gennings, C., Boverhof, D. R., Burt, J. W., Fong, C. J., and Zacharewski, T. R. (2005). Protocols for the assurance of microarray data quality and process control. Nucleic Acids Res. 33, e172.
16. Chen, C. Y., Hamm, J. T., Hass, J. R., and Birnbaum, L. S. (2001). Disposition of polychlorinated dibenzo-p-dioxins, dibenzofurans, and non-ortho polychlorinated biphenyls in pregnant long Evans rats and the transfer to offspring. Toxicol. Appl. Pharmacol. 173, 65-88.
17. Davis, D., and Safe, S. (1989). Dose-response immunotoxicities of commercial polychlorinated biphenyls (PCBs) and their interaction with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Lett. 48, 35-43.
18. Decad, G. M., Birnbaum, L. S., and Matthews, H. B. (1981). Distribution and excretion of 2,3,7,8-tetrachlorodibenzofuran in C57BL/6J and DBA/2J mice. Toxicol. Appl. Pharmacol. 59, 564-73.
19. Denison, M. S., and Heath-Pagliuso, S. (1998). The Ah receptor: A regulator of the biochemical and toxicological actions of structurally diverse chemicals. Bull. Environ. Contam. Toxicol. 61, 557-68.
20. Denison, M. S., Pandini, A., Nagy, S. R., Baldwin, E. P., and Bonati, L. (2002). Ligand binding and activation of the Ah receptor. Chem. Biol. Interact. 141, 3-24.
21. DeVito, M. J., and Birnbaum, L. S. (1995). The importance of pharmacokinetics in determining the relative potency of 2,3,7,8-tetrachlorodibenzo-p-dioxin and 2,3,7,8-tetrachlorodibenzofuran. Fundam. Appl. Toxicol. 24, 145-8.
22. DeVito, M. J., Diliberto, J. J., Ross, D. G., Menache, M. G., and Birnbaum, L. S. (1997). Dose-response relationships for polyhalogenated dioxins and dibenzofurans following subchronic treatment in mice. I. CYP1A1 and CYP1A2 enzyme activity in liver, lung, and skin. Toxicol. Appl. Pharmacol. 147, 267-80.
23. DeVito, M. J., Ma, X., Babish, J. G., Menache, M., and Birnbaum, L. S. (1994). Dose-response relationships in mice following subchronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin: CYP1A1, CYP1A2, estrogen receptor, and protein tyrosine phosphorylation. Toxicol. Appl. Pharmacol. 124, 82-90.
24. DeVito, M. J., Menache, M. G., Diliberto, J. J., Ross, D. G., and Birnbaum, L. S. (2000). Dose-response relationships for induction of CYP1A1 and CYP1A2 enzyme activity in liver, lung, and skin in female mice following subchronic exposure to polychlorinated biphenyls. Toxicol. Appl. Pharmacol. 167, 157-72.
25. 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, 223-34.
26. Diliberto, J. J., Akubue, P. I., Luebke, R. W., and Birnbaum, L. S. (1995). Dose-response relationships of tissue distribution and induction of CYP1A1 and CYP1A2 enzymatic activities following acute exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice. Toxicol. Appl. Pharmacol. 130, 197-208.
27. 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, 431-3.
28. Diliberto, J. J., Burgin, D. E., and Birnbaum, L. S. (1999). Effects of CYP1A2 on disposition of 2,3,7, 8-tetrachlorodibenzo-p-dioxin, 2,3,4,7,8-pentachlorodibenzofuran, and 2,2′,4,4′,5,5′-hexachlorobiphenyl in CYP1A2 knockout and parental (C57BL/6N and 129/Sv) strains of mice. Toxicol. Appl. Pharmacol. 159, 52-64.
29. 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, 241-55.
30. Eckel, J. E., Gennings, C., Chinchilli, V. M., Burgoon, L. D., and Zacharewski, T. R. (2004). Empirical bayes gene screening tool for timecourse or dose-response microarray data. J. Biopharm. Stat. 14, 647-70.
31. Eckel, J. E., Gennings, C., Therneau, T. M., Burgoon, L. D., Boverhof, D. R., and Zacharewski, T. R. (2005). Normalization of two-channel microarray experiments: A semiparametric approach. Bioinformatics 21, 1078-83.
32. Fletcher, N., Hanberg, A., and Hakansson, H. (2001). Hepatic vitamin a depletion is a sensitive marker of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) exposure in four rodent species. Toxicol. Sci. 62, 166-75.
33. Fletcher, N., Wahlstrom, D., Lundberg, R., Nilsson, C. B., Nilsson, K. C., Stockling, K., Hellmold, H., and Hakansson, H. (2005). 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) alters the mRNA expression of critical genes associated with cholesterol metabolism, bile acid biosynthesis, and bile transport in rat liver: A microarray study. Toxicol. Appl. Pharmacol. 207, 1-24.
34. Gasiewicz, T. A., Geiger, L. E., Rucci, G., and Neal, R. A. (1983). Distribution, excretion, and metabolism of 2,3,7,8-tetrachlorodibenzo-p-dioxin in C57BL/6J, DBA/2J, and B6D2F1/J mice. Drug Metab. Dispos. 11, 397-403.
35. Hamadeh, H. K., Bushel, P. R., Jayadev, S., Martin, K., DiSorbo, O., Sieber, S., Bennett, L., Tennant, R., Stoll, R., Barrett, J. C., et al. (2002). Gene expression analysis reveals chemical-specific profiles. Toxicol. Sci. 67, 219-31.
36. Hamm, J. T., Chen, C. Y., and Birnbaum, L. S. (2003). A mixture of dioxins, furans, and non-ortho PCBs based upon consensus toxic equivalency factors produces dioxin-like reproductive effects. Toxicol. Sci. 74, 182-91.
37. Harris, M., Zacharewski, T., and Safe, S. (1993). Comparative potencies of Aroclors 1232, 1242, 1248, 1254, and 1260 in male Wistar rats-assessment of the toxic equivalency factor (TEF) approach for polychlorinated biphenyls (PCBs). Fundam. Appl. Toxicol. 20, 456-63; S0272059083710560 [pii].
38. 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.
39. Kopec, A. K., Boverhof, D. R., Burgoon, L. D., Ibrahim-Aibo, D., Harkema, J. R., Tashiro, C., Chittim, B., and Zacharewski, T. R. (2007). Comparative toxicogenomic examination of the hepatic effects of PCB126 and TCDD in immature, ovariectomized C57BL/6 mice. Toxicol. Sci. 102, 61-75.
40. Mason, G., and Safe, S. (1986). Synthesis, biologic and toxic effects of the major 2,3,7,8-tetrachlorodibenzo-p-dioxin metabolites in the rat. Toxicology 41, 153-9.
41. 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′-tetrachlorobiphenyl in the rat. Fundam. Appl. Toxicol. 21, 425-32.
42. 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, 624-40.
43. Nebert, D. W., Roe, A. L., Dieter, M. Z., Solis, W. A., Yang, Y., and Dalton, T. P. (2000). Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 59, 65-85.
44. Nuwaysir, E. F., Bittner, M., Trent, J., Barrett, J. C., and Afshari, C. A. (1999). Microarrays and toxicology: The advent of toxicogenomics. Mol. Carcinog. 24, 153-9.
45. 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-totrachlorodibenzofuran. Fundam. Appl. Toxicol. 22, 631-40. S0272059084710694 [pii].
46. Poland, A., and Glover, E. (1973). Chlorinated dibenzo-p-dioxins: Potent inducers of delta-aminolevulinic acid synthetase and aryl hydrocarbon hydroxylase. II. A study of the structure-activity relationship. Mol. Pharmacol. 9, 736-47.
47. Poland, A., and Knutson, J. C. (1982). 2,3,7,8-tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: Examination of the mechanism of toxicity. Annu. Rev. Pharmacol. Toxicol. 22, 517-54.
48. Puga, A., Nebert, D. W., and Carrier, F. (1992). Dioxin induces expression of c-fos and c-jun proto-oncogenes and a large increase in transcription factor AP-1. DNA Cell Biol 11, 269-81.
49. Safe, S. (1990). Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: Environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit. Rev. Toxicol. 21, 51-88.
50. Safe, S. (1993). Development of bioassays and approaches for the risk assessment of 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds. Environ. Health Perspect. 101(Suppl. 3), 317-25.
51. Safe, S. (1997). Limitations of the toxic equivalency factor approach for risk assessment of TCDD and related compounds. Teratog. Carcinog. Mutagen. 17, 285-304.
52. Safe, S. (2001). Molecular biology of the Ah receptor and its role in carcinogenesis. Toxicol. Lett. 120, 1-7.
53. Safe, S., Robertson, L. W., Safe, L., Parkinson, A., Bandiera, S., Sawyer, T., and Campbell, M. A. (1982). Halogenated biphenyls: Molecular toxicology. Can. J. Physiol. Pharmacol. 60, 1057-64.
54. Safe, S. H. (1995). Modulation of gene expression and endocrine response pathways by 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds. Pharmacol. Ther. 67, 247-81.
55. Santosfefano, M., Liu, H., Wang, X., Chaloupka, K., and Safe, S. (1994). Effect of ligand structure on formation and DNA binding properties of the transformed rat cytosolic aryl hydrocarbon receptor. Chem. Res. Toxicol. 7, 544-50.
56. Stahl, B. U. (1995). 2,3,7,8-Tetrachlorodibenzo-p-dioxin blocks the physiological regulation of hepatic phosphoenolpyruvate carboxykinase activity in primary rat hepatocytes. Toxicology 103, 45-52.
57. Stahl, B. U., Beer, D. G., Weber, L. W., and Rozman, K. (1993). Reduction of hepatic pbosphoenolpyruvate carboxykinase (PEPCK) activity by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) is due to decreased mRNA levels. Toxicology 79, 81-95.
58. Sun, Y. V., Boverhof, D. R., Burgoon, L. D., Fielden, M. R., and Zacharewski, T. R. (2004). Comparative analysis of dioxin response elements in human, mouse and rat genomic sequences. Nucleic Acids Res. 32, 4512-23.
59. Tai, H. L., McReynolds, J. H., 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.
60. Tian, Y., Ke, S., Denison, M. S., Rabson, A. B., and Gallo, M. A. (1999). Ah receptor and NF-kappaB interactions, a potential mechanism for dioxin. toxicity. J. Biol. Chem. 274, 510-5.
61. Toyoshiba, H., Walker, N. J., Bailer, A. J., and Portier, C. J. (2004). Evaluation of toxic equivalency factors for induction of cytochromes P450 CYP1A1 and CYP1A2 enzyme activity by dioxin-like compounds. Toxicol. Appl. Pharmacol. 194, 156-68.
62. van Birgelen, A. P., DeVito, M. J., Akins, J. M., Ross, D. G., Diliberto, J. J., and Birnbaum, L. S. (1996). Relative potencies of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls derived from hepatic porphyrin accumulation in mice. Toxicol. Appl. Pharmacol. 138, 98-109.
63. Van den Berg, M., Birnbaum, L., Bosveld, A. T., Brunstrom, B., Cook, P., Feeley, M., Gies, 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. 106 775-92.
64. Van den Berg, M., Birnbaum, L. S., Denison, M., De Vito, 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, 223-41.
65. Viluksela, M., Bager, Y., Tuomisto, J. T., Scheu, G., Unkila, M., Pohjanvirta, R., Flodstrom, S., Kosma, V. M., Maki-Paakkanen, J., Vartiainen, T., et al. (2000). Liver tumor-promoting activity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in TCDD-sensitive and TCDD-resistant rat strains. Cancer Res. 60, 6911-20.
66. Viluksela, M., Stahl, B. U., Birnbaum, L. S., Schramm, K. W., Kettrup, A., and Rozman, K. K. (1998). Subchronic/chronic toxicity of a mixture of four chlorinated dibenzo-p-dioxins in rats. I. Design, general observations, hematology, and liver concentrations. Toxicol. Appl. Pharmacol. 151, 57-69.
67. Viluksela, M., Unkila, M., Pohjanvirta, R., Tuomisto, J. T., Stahl, B. U., Rozman, K. K., and Tuomisto, J. (1999). Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on liver phosphoenolpyruvate carboxykinase (PEPCK) activity, glucose homeostasis and plasma amino acid concentrations in the most TCDD-susceptible and the most TCDD-resistant rat strains. Arch. Toxicol. 73, 323-36.
68. Weber, L. W., Lebofsky, M., Stahl, B. U., Gorski, J. R., Muzi, G., and Rozman, K. (1991). Reduced activities of key enzymes of gluconeogenesis as possible cause of acute toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in rats. Toxicology 66, 133-44.
69. Yang, Y. H., and Speed, T. (2002). Design issues for cDNA microarray experiments. Nat. Rev. Genet. 3, 579-88.
70. Yuen, T., Wurmbach, E., Pfeffer, R. L., Ebersole, B. J., and Sealfon, S. C. (2002). Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleic Acids Res. 30, e48.