Comparisons of differential gene expression elicited by TCDD, PCB126, βNF, or ICZ in mouse hepatoma Hepa1c1c7 cells and C57BL/6 mouse liver

Toxicology Letters

Volumn 223, Issue 1, 2013, Pages 52-59

  Nault, Rance ^a,b   Forgacs, Agnes L ^a,b   Dere, Edward ^a   Zacharewski, Timothy R ^a,b  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Cross ligand comparison; Microarray; Mouse; Selective AhR modulation

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 3,3',4,4',5 PENTACHLOROBIPHENYL; BETA NAPHTHOFLAVONE; CARBAZOLE DERIVATIVE; INDOLO[3,2 B]CARBAZOLE; LIGAND; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE METABOLISM; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENETIC VARIABILITY; IN VITRO STUDY; IN VIVO STUDY; LIPID METABOLISM; LIVER; LIVER CELL CARCINOMA; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL;

CROSS-LIGAND COMPARISON; MICROARRAY; MOUSE; SELECTIVE AHR MODULATION;

ANIMALS; BETA-NAPHTHOFLAVONE; CARBAZOLES; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYCHLORINATED BIPHENYLS; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN;

EID: 84884217606     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.08.013     Document Type: Article

References (64)

1. Astroff B., Safe S. 6-substituted-1,3,8-trichlorodibenzofurans as 2,3,7,8-tetrachlorodibenzo-p-dioxin antagonists in the rat: structure activity relationships. Toxicology 1989, 59:285-296.
2. Astroff B., Zacharewski T., Safe S., Arlotto M.P., Parkinson A., Thomas P., Levin W. 6-Methyl-1,3,8-trichlorodibenzofuran as a 2,3,7,8-tetrachlorodibenzo-p-dioxin antagonist: inhibition of the induction of rat cytochrome P-450 isozymes and related monooxygenase activities. Mol. Pharmacol. 1988, 33:231-236.
3. Bannister R., Biegel L., Davis D., Astroff B., Safe S. 6-Methyl-1,3,8-trichlorodibenzofuran (MCDF) as a 2,3,7,8-tetrachlorodibenzo-p-dioxin antagonist in C57BL/6 mice. Toxicology 1989, 54:139-150.
4. Beischlag T.V., Luis Morales J., Hollingshead B.D., Perdew G.H. The aryl hydrocarbon receptor complex and the control of gene expression. Crit. Rev. Eukaryot. Gene Expr. 2008, 18:207-250.
5. Berger J.P., Petro A.E., Macnaul K.L., Kelly L.J., Zhang B.B., Richards K., Elbrecht A., Johnson B.A., Zhou G., Doebber T.W., Biswas C., Parikh M., Sharma N., Tanen M.R., Thompson G.M., Ventre J., Adams A.D., Mosley R., Surwit R.S., Moller D.E. Distinct properties and advantages of a novel peroxisome proliferator-activated protein [gamma] selective modulator. Mol. Endocrinol. 2003, 17:662-676.
6. Biegel L., Harris M., Davis D., Rosengren R., Safe L., Safe S. 2,2',4,4',5,5'-Hexachlorobiphenyl as a 2,3,7,8-tetrachlorodibenzo-p-dioxin antagonist in C57BL/6J mice. Toxicol. Appl. Pharmacol. 1989, 97:561-571.
7. Bohonowych J.E., Denison M.S. Persistent binding of ligands to the aryl hydrocarbon receptor. Toxicol. Sci. 2007, 98:99-109.
8. Boitano A.E., Wang J., Romeo R., Bouchez L.C., Parker A.E., Sutton S.E., Walker J.R., Flaveny C.A., Perdew G.H., Denison M.S., Schultz P.G., Cooke M.P. Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 2010, 329:1345-1348.
9. Boobis A.R., Nebert D.W., Felton J.S. Comparison of beta-naphthoflavone and 3-methylcholanthrene as inducers of hepatic cytochrome(s) P-448 and aryl hydrocarbon (benzo[a]pyrene) hydroxylase activity. Mol. Pharmacol. 1977, 13:259-268.
10. Boverhof D.R., Burgoon L.D., Tashiro C., Chittim B., Harkema J.R., Jump D.B., Zacharewski T.R. Temporal and dose-dependent hepatic gene expression patterns in mice provide new insights into TCDD-Mediated hepatotoxicity. Toxicol. Sci. 2005, 85:1048-1063.
11. Brzozowski A.M., Pike A.C., Dauter Z., Hubbard R.E., Bonn T., Engstrom O., Ohman L., Greene G.L., Gustafsson J.A., Carlquist M. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 1997, 389:753-758.
12. Bunger M.K., Glover E., Moran S.M., Walisser J.A., Lahvis G.P., Hsu E.L., Bradfield C.A. Abnormal liver development and resistance to 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity in mice carrying a mutation in the DNA-binding domain of the aryl hydrocarbon receptor. Toxicol. Sci. 2008, 106:83-92.
13. Burgoon L.D., Zacharewski T.R. dbZach toxicogenomic information management system. Pharmacogenomics 2007, 8:287-291.
14. Chen E.P., Chen L., Ji Y., Tai G., Wen Y.H., Ellens H. A mechanism-based mathematical model of aryl hydrocarbon receptor-mediated CYP1A induction in rats using beta-naphthoflavone as a tool compound. Drug Metab. Dispos. 2010, 38:2278-2285.
15. Chen Y.H., Riby J., Srivastava P., Bartholomew J., Denison M., Bjeldanes L. Regulation of CYP1A1 by indolo[3,2-b]carbazole in murine hepatoma cells. J. Biol. Chem. 1995, 270:22548-22555.
16. Davis D., Safe S. Immunosuppressive activities of polychlorinated dibenzofuran congeners: quantitative structure-activity relationships and interactive effects. Toxicol. Appl. Pharmacol. 1988, 94:141-149.
17. Denison M.S., Heath-Pagliuso S. The Ah receptor: a regulator of the biochemical and toxicological actions of structurally diverse chemicals. Bull. Environ. Contam. Toxicol. 1998, 61:557-568.
18. Denison M.S., Nagy S.R. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol. 2003, 43:309-334.
19. Denison M.S., Soshilov A.A., He G., DeGroot D.E., Zhao B. Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol. Sci. 2011, 124:1-22.
20. Dere E., Boverhof D.R., Burgoon L.D., Zacharewski T.R. In vivo-in vitro toxicogenomic comparison of TCDD-elicited gene expression in Hepa1c1c7 mouse hepatoma cells and C57BL/6 hepatic tissue. BMC Genomics 2006, 7:80.
21. Dere E., Forgacs A.L., Zacharewski T.R., Burgoon L.D. Genome-wide computational analysis of dioxin response element location and distribution in the human, mouse, and rat genomes. Chem. Res. Toxicol. 2011, 24:494-504.
22. Dere E., Lo R., Celius T., Matthews J., Zacharewski T.R. Integration of genome-wide computation DRE search, AhR ChIP-chip and gene expression analyses of TCDD-elicited responses in the mouse liver. BMC Genomics 2011, 12:365.
23. Dickerson R., Howie L., Davis D., Safe S. The structure-dependent effects of heptachlorodibenzofuran isomers in male C57BL/6 mice: immunotoxicity and monooxygenase enzyme induction. Fundam. Appl. Toxicol. 1990, 15:298-307.
24. Eckel J.E., Gennings C., Chinchilli V.M., Burgoon L.D., Zacharewski T.R. Empirical bayes gene screening tool for time-course or dose-response microarray data. J. Biopharm. Stat. 2004, 14:647-670.
25. Eckel J.E., Gennings C., Therneau T.M., Burgoon L.D., Boverhof D.R., Zacharewski T.R. Normalization of two-channel microarray experiments: a semiparametric approach. Bioinformatics 2005, 21:1078-1083.
26. Fong C.J., Burgoon L.D., Williams K.J., Forgacs A.L., Zacharewski T.R. Comparative temporal and dose-dependent morphological and transcriptional uterine effects elicited by tamoxifen and ethynylestradiol in immature, ovariectomized mice. BMC Genomics 2007, 8:151.
27. Fox J., Weisberg S. An {R} companion to applied regressions 2011, Sage, Thousand Oaks.
28. Frasor J., Stossi F., Danes J.M., Komm B., Lyttle C.R., Katzenellenbogen B.S. Selective estrogen receptor modulators: discrimination of agonistic versus antagonistic activities by gene expression profiling in breast cancer cells. Cancer Res. 2004, 64:1522-1533.
29. Gasiewicz T.A., Geiger L.E., Rucci G., Neal R.A. Distribution, excretion, and metabolism of 2,3,7,8-tetrachlorodibenzo-p-dioxin in C57BL/6J, DBA/2J, and B6D2F1/J mice. Drug Metab. Dispos. 1983, 11:397-403.
30. Gasiewicz T.A., Rucci G. Alpha-naphthoflavone acts as an antagonist of 2,3,7, 8-tetrachlorodibenzo-p-dioxin by forming an inactive complex with the Ah receptor. Mol. Pharmacol. 1991, 40:607-612.
31. Gonzalez F.J., Fernandez-Salguero P. The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab. Dispos. 1998, 26:1194-1198.
32. Hankinson O. The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 1995, 35:307-340.
33. Harris M., Zacharewski T., Astroff B., Safe S. Partial antagonism of 2,3,7,8-tetrachlorodibenzo-p-dioxin-mediated induction of aryl hydrocarbon hydroxylase by 6-methyl-1,3,8-trichlorodibenzofuran: mechanistic studies. Mol. Pharmacol. 1989, 35:729-735.
34. Henry E.C., Welle S.L., Gasiewicz T.A. TCDD and a putative endogenous AhR ligand, ITE, elicit the same immediate changes in gene expression in mouse lung fibroblasts. Toxicol. Sci. 2010, 114:90-100.
35. Huang G., Elferink C.J. A novel nonconsensus xenobiotic response element capable of mediating aryl hydrocarbon receptor-dependent gene expression. Mol. Pharmacol. 2012, 81:338-347.
36. Jin U.H., Lee S.O., Safe S.H. Aryl hydrocarbon receptor (AhR)-active pharmaceuticals are selective AhR modulators in MDA-MB-468 and BT474 breast cancer cells. J. Pharmacol. Exp. Ther. 2012.
37. Kim S.H., Henry E.C., Kim D.K., Kim Y.H., Shin K.J., Han M.S., Lee T.G., Kang J.K., Gasiewicz T.A., Ryu S.H., Suh P.G. Novel compound 2-methyl-2H-pyrazole-3-carboxylic acid (2-methyl-4-o-tolylazo-phenyl)-amide (CH-223191) prevents 2,3,7,8-TCDD-induced toxicity by antagonizing the aryl hydrocarbon receptor. Mol. Pharmacol. 2006, 69:1871-1878.
38. Kopec A.K., Boverhof D.R., Burgoon L.D., Ibrahim-Aibo D., Harkema J.R., Tashiro C., Chittim B., Zacharewski T.R. Comparative toxicogenomic examination of the hepatic effects of PCB126 and TCDD in immature, ovariectomized C57BL/6 mice. Toxicol. Sci. 2008, 102:61-75.
39. Kopec A.K., Boverhof D.R., Nault R., Harkema J.R., Tashiro C., Sharratt B., Chittim B., Burgoon L.D., Zacharewski T.R. Toxicogenomic evaluation of long-term hepatic effects of TCDD in immature, ovariectomized C57bl/6 mice. Toxicol. Sci. 2013.
40. Kremoser C., Albers M., Burris T.P., Deuschle U., Koegl M. Panning for SNuRMs: using cofactor profiling for the rational discovery of selective nuclear receptor modulators. Drug Discovery Today 2007, 12:860-869.
41. Kwekel J.C., Forgacs A.L., Burgoon L.D., Williams K.J., Zacharewski T.R. Tamoxifen-elicited uterotrophy: cross-species and cross-ligand analysis of the gene expression program. BMC Medical Genomics 2009, 2:19.
42. Levenson A.S., Jordan V.C. Selective oestrogen receptor modulation: molecular pharmacology for the millennium. Eur. J. Cancer 1999, 35:1974-1985.
43. Levenson A.S., Kliakhandler I.L., Svoboda K.M., Pease K.M., Kaiser S.A., Ward J.E., Jordan V.C. Molecular classification of selective oestrogen receptor modulators on the basis of gene expression profiles of breast cancer cells expressing oestrogen receptor alpha. Br. J. Cancer 2002, 87:449-456.
44. McKillop D., Case D.E. Mutagenicity, carcinogenicity and toxicity of beta-naphthoflavone, a potent inducer of P448. Biochem. Pharmacol. 1991, 41:1-7.
45. Murray I.A., Flaveny C.A., Chiaro C.R., Sharma A.K., Tanos R.S., Schroeder J.C., Amin S.G., Bisson W.H., Kolluri S.K., Perdew G.H. Suppression of cytokine-mediated complement factor gene expression through selective activation of the Ah receptor with 3',4'-dimethoxy-alpha-naphthoflavone. Mol. Pharmacol. 2011, 79:508-519.
46. Murray I.A., Krishnegowda G., DiNatale B.C., Flaveny C., Chiaro C., Lin J.M., Sharma A.K., Amin S., Perdew G.H. Development of a selective modulator of aryl hydrocarbon (Ah) receptor activity that exhibits anti-inflammatory properties. Chem. Res. Toxicol. 2010, 23:955-966.
47. Nebert D.W., Roe A.L., Dieter M.Z., Solis W.A., Yang Y., Dalton T.P. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 2000, 59:65-85.
48. Nguyen L.P., Bradfield C.A. The search for endogenous activators of the aryl hydrocarbon receptor. Chem. Res. Toxicol. 2008, 21:102-116.
49. Opitz C.A., Litzenburger U.M., Sahm F., Ott M., Tritschler I., Trump S., Schumacher T., Jestaedt L., Schrenk D., Weller M., Jugold M., Guillemin G.J., Miller C.L., Lutz C., Radlwimmer B., Lehmann I., von Deimling A., Wick W., Platten M. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 2011, 478:197-203.
50. Pansoy A., Ahmed S., Valen E., Sandelin A., Matthews J. 3-methylcholanthrene induces differential recruitment of aryl hydrocarbon receptor to human promoters. Toxicol. Sci. 2010, 117:90-100.
51. Pohjanvirta R., Korkalainen M., McGuire J., Simanainen U., Juvonen R., Tuomisto J.T., Unkila M., Viluksela M., Bergman J., Poellinger L., Tuomisto J. Comparison of acute toxicities of indolo[3,2-b]carbazole (ICZ) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in TCDD-sensitive rats. Food Chem. Toxicol. 2002, 40:1023-1032.
52. Pohjanvirta R., Vartiainen T., Uusi-Rauva A., Monkkonen J., Tuomisto J. Tissue distribution, metabolism, and excretion of 14C-TCDD in a TCDD-susceptible and a TCDD-resistant rat strain. Pharmacol. Toxicol. 1990, 66:93-100.
53. Poland A., Knutson J.C. 2,3,7,8-Tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: examination of the mechanism of toxicity. Annu. Rev. Pharmacol. Toxicol. 1982, 22:517-554.
54. Quintana F.J., Murugaiyan G., Farez M.F., Mitsdoerffer M., Tukpah A.M., Burns E.J., Weiner H.L. An endogenous aryl hydrocarbon receptor ligand acts on dendritic cells and T cells to suppress experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20768-20773.
55. Romkes M., Piskorska-Pliszczynska J., Safe S. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on hepatic and uterine estrogen receptor levels in rats. Toxicol. Appl. Pharmacol. 1987, 87:306-314.
56. Safe S., Qin C., McDougal A. Development of selective aryl hydrocarbon receptor modulators for treatment of breast cancer. Expert Opin. Investig. Drugs 1999, 8:1385-1396.
57. Sears D.D., Hsiao A., Ofrecio J.M., Chapman J., He W., Olefsky J.M. Selective modulation of promoter recruitment and transcriptional activity of PPARgamma. Biochem. Biophys. Res. Commun. 2007, 364:515-521.
58. Smith C.L., O'Malley B.W. Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr. Rev. 2004, 25:45-71.
59. Tanos R., Patel R.D., Murray I.A., Smith P.B., Patterson A.D., Perdew G.H. Aryl hydrocarbon receptor regulates the cholesterol biosynthetic pathway in a dioxin response element-independent manner. Hepatology 2012, 55:1994-2004.
60. van den Berg M., Peterson R.E., Schrenk D. Human risk assessment and TEFs. Food Addit. Contam. 2000, 17:347-358.
61. Wei Y.D., Rannug U., Rannug A. UV-induced CYP1A1 gene expression in human cells is mediated by tryptophan. Chem. Biol. Interact. 1999, 118:127-140.
62. Yao C., Safe S. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced porphyria in genetically inbred mice: partial antagonism and mechanistic studies. Toxicol. Appl. Pharmacol. 1989, 100:208-216.
63. Yin X.F., Chen J., Mao W., Wang Y.H., Chen M.H. A selective aryl hydrocarbon receptor modulator 3,3'-Diindolylmethane inhibits gastric cancer cell growth. J. Exp. Clin. Cancer Res. 2012, 31:46.
64. Zhang S., Rowlands C., Safe S. Ligand-dependent interactions of the Ah receptor with coactivators in a mammalian two-hybrid assay. Toxicol. Appl. Pharmacol. 2008, 227:196-206.