Comparison of TCDD-elicited genome-wide hepatic gene expression in Sprague-Dawley rats and C57BL/6 mice

Toxicology and Applied Pharmacology

Volumn 267, Issue 2, 2013, Pages 184-191

  Nault, Rance ^a   Kim, Suntae ^a   Zacharewski, Timothy R ^a  

^a Michigan State University   (United States)

Author keywords

Cross species; Microarray; Mouse; Rat; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ACYLTRANSFERASE; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; FATTY ACID; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; OLIGONUCLEOTIDE; PHOSPHOLIPID; STEROID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOHYDRATE METABOLISM; COMPARATIVE STUDY; CONTROLLED STUDY; FATTY ACID METABOLISM; FATTY LIVER; FEMALE; GENE CLUSTER; GENE EXPRESSION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GENE REPRESSION; GENETIC ASSOCIATION; GENETIC DATABASE; GENETIC VARIABILITY; HEPATIC GENE EXPRESSION; IMMUNOGENETICS; LIPID METABOLISM; MALE; MICROARRAY ANALYSIS; MICROCHIP ANALYSIS; MOLECULAR GENETICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; OVARIECTOMY; PROTEIN FOLDING; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SPECIES DIFFERENCE; TOXICOGENETICS; TOXICOLOGY;

ANIMALS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; LIVER; MALE; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, SPRAGUE-DAWLEY; SPECIES SPECIFICITY; TETRACHLORODIBENZODIOXIN; TRANSCRIPTION FACTORS;

EID: 84873868228     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.11.028     Document Type: Article

References (56)

1. Angrish M.M., Mets B.D., Jones A.D., Zacharewski T.R. Dietary fat is a lipid source in 2,3,7,8-tetrachlorodibenzo-rho-dioxin (TCDD)-elicited hepatic steatosis in C57BL/6 mice. Toxicol. Sci. 2012, 128:377-386.
2. Atshaves B.P., Martin G.G., Hostetler H.A., McIntosh A.L., Kier A.B., Schroeder F. Liver fatty acid-binding protein and obesity. J. Nutr. Biochem. 2010, 21:1015-1032.
3. Bank P.A., Yao E.F., Phelps C.L., Harper P.A., Denison M.S. Species-specific binding of transformed Ah receptor to a dioxin responsive transcriptional enhancer. Eur. J. Pharmacol. 1992, 228:85-94.
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. Black M.B., Budinsky R.A., Dombkowski A., Cukovic D., LeCluyse E.L., Ferguson S.S., Thomas R.S., Rowlands J.C. Cross-species comparisons of transcriptomic alterations in human and rat primary hepatocytes exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Sci. 2012, 127:199-215.
6. Boutros P.C., Bielefeld K.A., Pohjanvirta R., Harper P.A. Transcriptomic responses to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in liver: comparison of rat and mouse. BMC Genomics 2008, 9:419.
7. Boutros P.C., Yan R., Moffat I.D., Pohjanvirta R., Okey A.B. Dioxin-dependent and dioxin-independent gene batteries: comparison of liver and kidney in AHR-null mice. Toxicol. Sci. 2009, 112:245-256.
8. 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.
9. Boverhof D.R., Burgoon L.D., Tashiro C., Sharratt B., Chittim B., Harkema J.R., Mendrick D.L., Zacharewski T.R. Comparative toxicogenomic analysis of the hepatotoxic effects of TCDD in Sprague Dawley rats and C57BL/6 mice. Toxicol. Sci. 2006, 94:398-416.
10. Budinsky R.A., LeCluyse E.L., Ferguson S.S., Rowlands J.C., Simon T. 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. Toxicol. Sci. 2010, 118:224-235.
11. Burgoon L.D., Boutros P.C., Dere E., Zacharewski T.R. dbZach: a MIAME-compliant toxicogenomic supportive relational database. Toxicol. Sci. 2006, 90:558-568.
12. Carlson E.A., McCulloch C., Koganti A., Goodwin S.B., Sutter T.R., Silkworth J.B. Divergent transcriptomic responses to aryl hydrocarbon receptor agonists between rat and human primary hepatocytes. Toxicol. Sci. 2009, 112:257-272.
13. Craft E.S., DeVito M.J., Crofton K.M. Comparative responsiveness of hypothyroxinemia and hepatic enzyme induction in Long-Evans rats versus C57BL/6J mice exposed to TCDD-like and phenobarbital-like polychlorinated biphenyl congeners. Toxicol. Sci. 2002, 68:372-380.
14. DeAngelis A.M., Heinrich G., Dai T., Bowman T.A., Patel P.R., Lee S.J., Hong E.G., Jung D.Y., Assmann A., Kulkarni R.N., Kim J.K., Najjar S.M. Carcinoembryonic antigen-related cell adhesion molecule 1 - a link between insulin and lipid metabolism. Diabetes 2008, 57:2296-2303.
15. 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.
16. Denison M.S., Vella L.M., Okey A.B. Structure and function of the Ah receptor for 2,3,7,8-tetrachlorodibenzo-p-dioxin. Species difference in molecular properties of the receptors from mouse and rat hepatic cytosols. J. Biol. Chem. 1986, 261:3987-3995.
17. 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.
18. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., Lempicki R.A. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 2003, 4:P3.
19. 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.
20. Dere E., Lee A.W., Burgoon L.D., Zacharewski T.R. Differences in TCDD-elicited gene expression profiles in human HepG2, mouse Hepa1c1c7 and rat H4IIE hepatoma cells. BMC Genomics 2011, 12:193.
21. 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.
22. 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.
23. 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.
24. Fletcher N., Wahlstrom D., Lundberg R., Nilsson C.B., Nilsson K.C., Stockling K., Hellmold H., Hakansson H. 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. 2005, 207:1-24.
25. Forgacs A.L., Kent M.N., Makley M.K., Mets B., DelRaso N., Jahns G.L., Burgoon L.D., Zacharewski T.R., Reo N.V. Comparative metabolomic and genomic analyses of TCDD-elicited metabolic disruption in mouse and rat liver. Toxicol. Sci. 2012, 125:41-55.
26. Forgacs, A.L., Dere, E., Angrish, M.M., Zacharewski, T., submitted for publication. Comparative analysis of TCDD-elicited gene expression in human, mouse and rat primary hepatocytes.
27. Fujita P.A., Rhead B., Zweig A.S., Hinrichs A.S., Karolchik D., Cline M.S., Goldman M., Barber G.P., Clawson H., Coelho A., Diekhans M., Dreszer T.R., Giardine B.M., Harte R.A., Hillman-Jackson J., Hsu F., Kirkup V., Kuhn R.M., Learned K., Li C.H., Meyer L.R., Pohl A., Raney B.J., Rosenbloom K.R., Smith K.E., Haussler D., Kent W.J. The UCSC Genome Browser database: update 2011. Nucleic Acids Res. 2011, 39:D876-D882.
28. Ganter B., Tugendreich S., Pearson C.I., Ayanoglu E., Baumhueter S., Bostian K.A., Brady L., Browne L.J., Calvin J.T., Day G.J., Breckenridge N., Dunlea S., Eynon B.P., Furness L.M., Ferng J., Fielden M.R., Fujimoto S.Y., Gong L., Hu C., Idury R., Judo M.S., Kolaja K.L., Lee M.D., McSorley C., Minor J.M., Nair R.V., Natsoulis G., Nguyen P., Nicholson S.M., Pham H., Roter A.H., Sun D., Tan S., Thode S., Tolley A.M., Vladimirova A., Yang J., Zhou Z., Jarnagin K. Development of a large-scale chemogenomics database to improve drug candidate selection and to understand mechanisms of chemical toxicity and action. J. Biotechnol. 2005, 119:219-244.
29. Gonzalez F.J., Fernandez-Salguero P. The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab. Dispos. 1998, 26:1194-1198.
30. Gonzalez F.J., Shah Y.M. PPARalpha: mechanism of species differences and hepatocarcinogenesis of peroxisome proliferators. Toxicology 2008, 246:2-8.
31. Goudriaan J.R., Tacken P.J., Dahlmans V.E.H., Gijbels M.J.J., van Dijk K.W., Havekes L.M., Jong M.C. Protection from obesity in mice lacking the VLDL receptor. Arterioscler. Thromb. Vasc. Biol. 2001, 21:1488-1493.
32. Guo L., Lobenhofer E.K., Wang C., Shippy R., Harris S.C., Zhang L., Mei N., Chen T., Herman D., Goodsaid F.M., Hurban P., Phillips K.L., Xu J., Deng X., Sun Y.A., Tong W., Dragan Y.P., Shi L. Rat toxicogenomic study reveals analytical consistency across microarray platforms. Nat. Biotechnol. 2006, 24:1162-1169.
33. Hahn M.E., Karchner S.I., Shapiro M.A., Perera S.A. Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:13743-13748.
34. Hankinson O. The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 1995, 35:307-340.
35. He S., McPhaul C., Li J.Z., Garuti R., Kinch L., Grishin N.V., Cohen J.C., Hobbs H.H. A sequence variation (I148M) in PNPLA3 associated with nonalcoholic fatty liver disease disrupts triglyceride hydrolysis. J. Biol. Chem. 2010, 285:6706-6715.
36. 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.
37. IPA Ingenuity Transcription Factor Analysis in IPA [White Paper] (Last accessed February 20, 2012). https://ingenuity--c.na3.content.force.com/servlet/fileField?id=0BE50000000Gmim.
38. Kim S., Dere E., Burgoon L.D., Chang C.C., Zacharewski T.R. Comparative analysis of AhR-mediated TCDD-elicited gene expression in human liver adult stem cells. Toxicol. Sci. 2009, 112:229-244.
39. 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.
40. Kopec A.K., D'Souza M.L., Mets B.D., Burgoon L.D., Reese S.E., Archer K.J., Potter D., Tashiro C., Sharratt B., Harkema J.R., Zacharewski T.R. Non-additive hepatic gene expression elicited by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and 2,2',4,4',5,5'-hexachlorobiphenyl (PCB153) co-treatment in C57BL/6 mice. Toxicol. Appl. Pharmacol. 2011, 256:154-167.
41. Lee W. The CEACAM1 expression is decreased in the liver of severely obese patients with or without diabetes. Diagn. Pathol. 2011, 6:40.
42. Maglich J.M., Stoltz C.M., Goodwin B., Hawkins-Brown D., Moore J.T., Kliewer S.A. Nuclear pregnane×receptor and constitutive androstane receptor regulate overlapping but distinct sets of genes involved in xenobiotic detoxification. Mol. Pharmacol. 2002, 62:638-646.
43. Najjar S.M. Regulation of insulin action by CEACAM1. Trends Endocrinol. Metab. 2002, 13:240-245.
44. National Toxicology Program 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). National Toxicology Program Technical Report Series, 4-232 2006.
45. NIEHS/NTP DrugMatrix Calculations [White Paper] (Last accessed October 4, 2012). https://ntp.niehs.nih.gov/drugmatrix/projects/DrugMatrix/support/White_Paper/DrugMatrix_Calculations.pdf.
46. Nunez B.S., Geng C.-D., Pedersen K.B., Millro-Macklin C.D., Vedeckis W.V. Interaction between the interferon signaling pathway and the human glucocorticoid receptor gene 1A promoter. Endocrinology 2005, 146:1449-1457.
47. Okey A.B., Riddick D.S., Harper P.A. Molecular biology of the aromatic hydrocarbon (dioxin) receptor. Trends Pharmacol. Sci. 1994, 15:226-232.
48. Olson H., Betton G., Robinson D., Thomas K., Monro A., Kolaja G., Lilly P., Sanders J., Sipes G., Bracken W., Dorato M., Van Deun K., Smith P., Berger B., Heller A. Concordance of the toxicity of pharmaceuticals in humans and in animals. Regul. Toxicol. Pharmacol. 2000, 32:56-67.
49. 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.
50. Postic C., Dentin R., Denechaud P.D., Girard J. ChREBP, a transcriptional regulator of glucose and lipid metabolism. Annu. Rev. Nutr. 2007, 27:179-192.
51. Shi L., et al. The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat. Biotechnol. 2006, 24:1151-1161.
52. Silkworth J.B., Koganti A., Illouz K., Possolo A., Zhao M., Hamilton S.B. 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. 2005, 87:508-519.
53. Smith L.L. Key challenges for toxicologists in the 21st century. Trends Pharmacol. Sci. 2001, 22:281-285.
54. Sun Y.V., Boverhof D.R., Burgoon L.D., Fielden M.R., Zacharewski T.R. Comparative analysis of dioxin response elements in human, mouse and rat genomic sequences. Nucleic Acids Res. 2004, 32:4512-4523.
55. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. (RESEARCH0034).
56. Yeager R.L., Reisman S.A., Aleksunes L.M., Klaassen C.D. Introducing the "TCDD-inducible AhR-Nrf2 gene battery". Toxicol. Sci. 2009, 111:238-246.