Promoter analysis of TCDD-inducible genes in a thymic epithelial cell line indicates the potential for cell-specific transcription factor crosstalk in the AhR response

Toxicology and Applied Pharmacology

Volumn 232, Issue 2, 2008, Pages 268-279

  Frericks, Markus ^a   Burgoon, Lyle D ^b   Zacharewski, Timothy R ^b   Esser, Charlotte ^a  

^a IUF LEIBNIZ RESEARCH INSTITUTE FOR ENVIRONMENTAL MEDICINE   (Germany)

^b National Food Safety and Toxicology Center   (United States)

Author keywords

Aryl hydrocarbon receptor; Dioxin; TCDD; Thymus epithelium; Transcription factor crosstalk

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; ESTRADIOL; ESTROGEN RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX4;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE MAPPING; GENETIC TRANSCRIPTION; HYPOXIA; IMMUNE DEFICIENCY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; THYMOCYTE; THYMUS ATROPHY; UNINDEXED SEQUENCE; XENOBIOTIC METABOLISM;

ANIMALS; CELL LINE; CELL SURVIVAL; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; PROMOTER REGIONS (GENETICS); RECEPTOR CROSS-TALK; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN; THYMUS GLAND; TRANSCRIPTION FACTORS;

EID: 52049114881     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2008.07.009     Document Type: Article

References (59)

1. Adachi S., Amasaki Y., Miyatake S., Arai N., and Iwata M. Successive expression and activation of NFAT family members during thymocyte differentiation. J. Biol. Chem. 275 (2000) 14708-14716
2. Amasaki Y., Adachi S., Ishida Y., Iwata M., Arai N., Arai K., and Miyatake S. A constitutively nuclear form of NFATx shows efficient transactivation activity and induces differentiation of CD4(+)CD8(+) T cells. J. Biol. Chem. 277 (2002) 25640-25648
3. Anderson M.K. At the crossroads: diverse roles of early thymocyte transcriptional regulators. Immunol. Rev. 209 (2006) 191-211
4. Beischlag T.V., and Perdew G.H. ER alpha-AHR-ARNT protein-protein interactions mediate estradiol-dependent transrepression of dioxin-inducible gene transcription. J. Biol. Chem. 280 (2005) 21607-21611
5. Biju M.P., Neumann A.K., Bensinger S.J., Johnson R.S., Turka L.A., and Haase V.H. Vhlh gene deletion induces Hif-1-mediated cell death in thymocytes. Mol. Cell Biol. 24 (2004) 9038-9047
6. Birney E., Stamatoyannopoulos J.A., Dutta A., Guigo R., Gingeras T.R., Margulies E.H., Weng Z., Snyder M., Dermitzakis E.T., Thurman R.E., Kuehn M.S., Taylor C.M., Neph S., Koch C.M., Asthana S., Malhotra A., Adzhubei I., Greenbaum J.A., Andrews R.M., Flicek P., Boyle P.J., Cao H., Carter N.P., Clelland G.K., Davis S., Day N., Dhami P., Dillon S.C., Dorschner M.O., Fiegler H., Giresi P.G., Goldy J., Hawrylycz M., Haydock A., Humbert R., James K.D., Johnson B.E., Johnson E.M., Frum T.T., Rosenzweig E.R., Karnani N., Lee K., Lefebvre G.C., Navas P.A., Neri F., Parker S.C., Sabo P.J., Sandstrom R., Shafer A., Vetrie D., Weaver M., Wilcox S., Yu M., Collins F.S., Dekker J., Lieb J.D., Tullius T.D., Crawford G.E., Sunyaev S., Noble W.S., Dunham I., Denoeud F., Reymond A., Kapranov P., Rozowsky J., Zheng D., Castelo R., Frankish A., Harrow J., Ghosh S., Sandelin A., Hofacker I.L., Baertsch R., Keefe D., Dike S., Cheng J., Hirsch H.A., Sekinger E.A., Lagarde J., Abril J.F., Shahab A., Flamm C., Fried C., Hackermuller J., Hertel J., Lindemeyer M., Missal K., Tanzer A., Washietl S., Korbel J., Emanuelsson O., Pedersen J.S., Holroyd N., Taylor R., Swarbreck D., Matthews N., Dickson M.C., Thomas D.J., Weirauch M.T., Gilbert J., Drenkow J., Bell I., Zhao X., Srinivasan K.G., Sung W.K., Ooi H.S., Chiu K.P., Foissac S., Alioto T., Brent M., Pachter L., Tress M.L., Valencia A., Choo S.W., Choo C.Y., Ucla C., Manzano C., Wyss C., Cheung E., Clark T.G., Brown J.B., Ganesh M., Patel S., Tammana H., Chrast J., Henrichsen C.N., Kai C., Kawai J., Nagalakshmi U., Wu J., Lian Z., Lian J., Newburger P., Zhang X., Bickel P., Mattick J.S., Carninci P., Hayashizaki Y., Weissman S., Hubbard T., Myers R.M., Rogers J., Stadler P.F., Lowe T.M., Wei C.L., Ruan Y., Struhl K., Gerstein M., Antonarakis S.E., Fu Y., Green E.D., Karaoz U., Siepel A., Taylor J., Liefer L.A., Wetterstrand K.A., Good P.J., Feingold E.A., Guyer M.S., Cooper G.M., Asimenos G., Dewey C.N., Hou M., Nikolaev S., Montoya-Burgos J.I., Loytynoja A., Whelan S., Pardi F., Massingham T., Huang H., Zhang N.R., Holmes I., Mullikin J.C., Ureta-Vidal A., Paten B., Seringhaus M., Church D., Rosenbloom K., Kent W.J., Stone E.A., Batzoglou S., Goldman N., Hardison R.C., Haussler D., Miller W., Sidow A., Trinklein N.D., Zhang Z.D., Barrera L., Stuart R., King D.C., Ameur A., Enroth S., Bieda M.C., Kim J., Bhinge A.A., Jiang N., Liu J., Yao F., Vega V.B., Lee C.W., Ng P., Shahab A., Yang A., Moqtaderi Z., Zhu Z., Xu X., Squazzo S., Oberley M.J., Inman D., Singer M.A., Richmond T.A., Munn K.J., Rada-Iglesias A., Wallerman O., Komorowski J., Fowler J.C., Couttet P., Bruce A.W., Dovey O.M., Ellis P.D., Langford C.F., Nix D.A., Euskirchen G., Hartman S., Urban A.E., Kraus P., Van C.S., Heintzman N., Kim T.H., Wang K., Qu C., Hon G., Luna R., Glass C.K., Rosenfeld M.G., Aldred S.F., Cooper S.J., Halees A., Lin J.M., Shulha H.P., Zhang X., Xu M., Haidar J.N., Yu Y., Ruan Y., Iyer V.R., Green R.D., Wadelius C., Farnham P.J., Ren B., Harte R.A., Hinrichs A.S., Trumbower H., and Clawson H. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447 (2007) 799-816
7. Burgoon L.D., Boutros P.C., Dere E., and Zacharewski T.R. dbZach: a MIAME-compliant toxicogenomic supportive relational database. Toxicol. Sci. 90 (2006) 558-568
8. Carver, L. A., and Bradfield, C. A. (1997). Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. J. Biol. Chem. 272, 11452-11456.
9. Chan W.K., Yao G., Gu Y.Z., and Bradfield C.A. Cross-talk between the aryl hydrocarbon receptor and hypoxia inducible factor signaling pathways. Demonstration of competition and compensation. J. Biol. Chem. 274 (1999) 12115-12123
10. De Waal E.J., Schuurman H.J., Van L.H., and Vos J.G. Differential effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin, bis(tri-n-butyltin) oxide and cyclosporine on thymus histophysiology. Crit. Rev. Toxicol. 27 (1997) 381-430
11. Domingo J.L., and Bocio A. Levels of PCDD/PCDFs and PCBs in edible marine species and human intake: a literature review. Environ. Int. 33 (2007) 397-405
12. Eckel J.E., Gennings C., Chinchilli V.M., Burgoon L.D., and Zacharewski T.R. Empirical Bayes gene screening tool for time-course or dose-response microarray data. J. Biopharm. Stat. 14 (2004) 647-670
13. Efron B., and Tibshirani R. Empirical Bayes methods and false discovery rates for microarrays. Genet. Epidemiol. 23 (2002) 70-86
14. Frericks M., Temchura V.V., Majora M., Stutte S., and Esser C. Transcriptional signatures of immune cells in aryl hydrocarbon receptor (AHR)-proficient and AHR-deficient mice. Biol. Chem. 387 (2006) 1219-1226
15. Gautier L., Cope L., Bolstad B.M., and Irizarry R.A. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20 (2004) 307-315
16. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., Ellis B., Gautier L., Ge Y., Gentry J., Hornik K., Hothorn T., Huber W., Iacus S., Irizarry R., Leisch F., Li C., Maechler M., Rossini A.J., Sawitzki G., Smith C., Smyth G., Tierney L., Yang J.Y., and Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5 (2004) R80
17. Good K.L., and Tangye S.G. Decreased expression of Kruppel-like factors in memory B cells induces the rapid response typical of secondary antibody responses. Proc. Natl. Acad. Sci. U. S. A 104 (2007) 13420-13425
18. Gray D.H., Ueno T., Chidgey A.P., Malin M., Goldberg G.L., Takahama Y., and Boyd R.L. Controlling the thymic microenvironment. Curr. Opin. Immunol. 17 (2005) 137-143
19. Gutierrez J.C., and Palacios R. Heterogeneity of thymic epithelial cells in promoting T-lymphocyte differentiation in vivo. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 642-646
20. Hale L.P., Braun R.D., Gwinn W.M., Greer P.K., and Dewhirst M.W. Hypoxia in the thymus: role of oxygen tension in thymocyte survival. Am. J. Physiol Heart Circ. Physiol. 282 (2002) H1467-H1477
21. Hankinson O. Role of coactivators in transcriptional activation by the aryl hydrocarbon receptor. Arch. Biochem. Biophys. 433 (2005) 379-386
22. Huang G., and Elferink C.J. Multiple mechanisms are involved in Ah receptor-mediated cell cycle arrest. Mol. Pharmacol. 67 (2005) 88-96
23. Jin B., and Ryu D.Y. Regulation of CYP1A2 by histone deacetylase inhibitors in mouse hepatocytes. J. Biochem. Mol. Toxicol. 18 (2004) 131-132
24. Kerkvliet N.I. Recent advances in understanding the mechanisms of TCDD immunotoxicity. Int. Immunopharmacol. 2 (2002) 277-291
25. Kobayashi A., Sogawa K., and Fujii-Kuriyama Y. Cooperative interaction between AhR.Arnt and Sp1 for the drug-inducible expression of CYP1A1 gene. J. Biol. Chem. 271 (1996) 12310-12316
26. Kohle C., and Bock K.W. Coordinate regulation of Phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2. Biochem. Pharmacol. 73 (2007) 1853-1862
27. Kremer J., Gleichmann E., and Esser C. Thymic stroma exposed to arylhydrocarbon receptor-binding xenobiotics fails to support proliferation of early thymocytes but induces differentiation. J. Immunol. 153 (1994) 2778-2786
28. Lai Z.W., Pineau T., and Esser C. Identification of dioxin-responsive elements (DREs) in the 5¢ regions of putative dioxin-inducible genes. Chem. Biol. Interact. 100 (1996) 97-112
29. Laiosa M.D., Lai Z.W., Thurmond T.S., Fiore N.C., DeRossi C., Holdener B.C., Gasiewicz T.A., and Silverstone A.E. 2,3,7,8-tetrachlorodibenzo-p-dioxin causes alterations in lymphocyte development and thymic atrophy in hemopoietic chimeras generated from mice deficient in ARNT2. Toxicol. Sci. 69 (2002) 117-124
30. Lee K., Burgoon L.D., Lamb L., Dere E., Zacharewski T.R., Hogenesch J.B., and LaPres J.J. Identification and characterization of genes susceptible to transcriptional cross-talk between the hypoxia and dioxin signaling cascades. Chem. Res. Toxicol. 19 (2006) 1284-1293
31. Ma Q., and Whitlock Jr. J.P. A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Biol. Chem. 272 (1997) 8878-8884
32. Mainiero F., Colombara M., Antonini V., Strippoli R., Merola M., Poffe O., Tridente G., and Ramarli D. p38 MAPK is a critical regulator of the constitutive and the beta4 integrin-regulated expression of IL-6 in human normal thymic epithelial cells. Eur. J. Immunol. 33 (2003) 3038-3048
33. Majora M., Frericks M., Temchura V., Reichmann G., and Esser C. Detection of a novel population of fetal thymocytes characterized by preferential emigration and a TCRgammadelta+ T cell fate after dioxin exposure. Int. Immunopharmacol. 5 (2005) 1659-1674
34. Martin D., Brun C., Remy E., Mouren P., Thieffry D., and Jacq B. GOToolBox: functional analysis of gene datasets based on gene ontology. Genome Biol. 5 (2004) R101
35. Matthews J., and Gustafsson J.A. Estrogen receptor and aryl hydrocarbon receptor signaling pathways. Nucl. Recept. Signal. 4 (2006) e016
36. Matys V., Fricke E., Geffers R., Gossling E., Haubrock M., Hehl R., Hornischer K., Karas D., Kel A.E., Kel-Margoulis O.V., Kloos D.U., Land S., Lewicki-Potapov B., Michael H., Munch R., Reuter I., Rotert S., Saxel H., Scheer M., Thiele S., and Wingender E. TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res. 31 (2003) 374-378
37. McMillan B.J., McMillan S.N., Glover E., and Bradfield C.A. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces premature activation of the KLF2 regulon during thymocyte development. J. Biol. Chem. 282 (2007) 12590-12597
38. Nohara K., Pan X., Tsukumo S., Hida A., Ito T., Nagai H., Inouye K., Motohashi H., Yamamoto M., Fujii-Kuriyama Y., and Tohyama C. Constitutively active aryl hydrocarbon receptor expressed specifically in T-lineage cells causes thymus involution and suppresses the immunization-induced increase in splenocytes. J. Immunol. 174 (2005) 2770-2777
39. Palacios R., Studer S., Samaridis J., and Pelkonen J. Thymic epithelial cells induce in vitro differentiation of PRO-T lymphocyte clones into TCR alpha,beta/T3+ and TCR gamma,delta/T3+ cells. EMBO J. 8 (1989) 4053-4063
40. Quintana F.J., Basso A.S., Iglesias A.H., Korn T., Farez M.F., Bettelli E., Caccamo M., Oukka M., and Weiner H.L. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453 (2008) 65-71
41. Ribot J., Enault G., Pilipenko S., Huchenq A., Calise M., Hudrisier D., Romagnoli P., and van Meerwijk J.P. Shaping of the autoreactive regulatory T cell repertoire by thymic cortical positive selection. J. Immunol. 179 (2007) 6741-6748
42. Roepcke S., Grossmann S., Rahmann S., and Vingron M. T-Reg Comparator: an analysis tool for the comparison of position weight matrices. Nucleic Acids Res. 33 (2005) W438-W441
43. Rozen S., and Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132 (2000) 365-386
44. Sandelin A., Alkema W., Engstrom P., Wasserman W.W., and Lenhard B. JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res. 32 (2004) D91-D94
45. Sempowski G.D., Rhein M.E., Scearce R.M., and Haynes B.F. Leukemia inhibitory factor is a mediator of Escherichia coli lipopolysaccharide-induced acute thymic atrophy. Eur. J. Immunol. 32 (2002) 3066-3070
46. Staples J.E., Murante F.G., Fiore N.C., Gasiewicz T.A., and Silverstone A.E. Thymic alterations induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin are strictly dependent on aryl hydrocarbon receptor activation in hemopoietic cells. J. Immunol. 160 (1998) 3844-3854
47. Suh J., Jeon Y.J., Kim H.M., Kang J.S., Kaminski N.E., and Yang K.H. Aryl hydrocarbon receptor-dependent inhibition of AP-1 activity by 2,3,7,8-tetrachlorodibenzo-p-dioxin in activated B cells. Toxicol. Appl. Pharmacol. 181 (2002) 116-123
48. Sulentic C.E., Kang J.S., Na Y.J., and Kaminski N.E. Interactions at a dioxin responsive element (DRE) and an overlapping kappaB site within the hs4 domain of the 3¢alpha immunoglobulin heavy chain enhancer. Toxicology 200 (2004) 235-246
49. Sun Y.V., Boverhof D.R., Burgoon L.D., Fielden M.R., and Zacharewski T.R. Comparative analysis of dioxin response elements in human, mouse and rat genomic sequences. Nucleic Acids Res. 32 (2004) 4512-4523
50. Tajima F. Determination of window size for analyzing DNA sequences. J. Mol. Evol. 33 (1991) 470-473
51. Teske S., Bohn A.A., Regal J.F., Neumiller J.J., and Lawrence B.P. Activation of the aryl hydrocarbon receptor increases pulmonary neutrophilia and diminishes host resistance to influenza A virus. Am. J. Physiol Lung Cell Mol. Physiol. 289 (2005) L111-L124
52. Uno S., Dalton T.P., Dragin N., Curran C.P., Derkenne S., Miller M.L., Shertzer H.G., Gonzalez F.J., and Nebert D.W. Oral benzo[a]pyrene in Cyp1 knockout mouse lines: CYP1A1 important in detoxication, CYP1B1 metabolism required for immune damage independent of total-body burden and clearance rate. Mol. Pharmacol. 69 (2006) 1103-1114
53. Uno, S., Dalton, T.P., Sinclair, P.R., Gorman, N., Wang, B., Smith, A.G., Miller, M.L., Shertzer, H.G., Nebert, D.W., 2004. Cyp1a1(-/-) male mice: protection against high-dose TCDD-induced lethality and wasting syndrome, and resistance to intrahepatocyte lipid accumulation and uroporphyria. 196, 410-421.
54. Velarde M.C., Zeng Z., McQuown J.R., Simmen F.A., and Simmen R.C. Kruppel-like factor 9 is a negative regulator of ligand-dependent estrogen receptor (alpha) signaling in Ishikawa endometrial adenocarcinoma cells. Mol. Endocrinol. 21 (2007) 2988-3001
55. Walhout A.J. Unraveling transcription regulatory networks by protein-DNA and protein-protein interaction mapping. Genome Res. 16 (2006) 1445-1454
56. Wang G.L., and Semenza G.L. Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J. Biol. Chem. 268 (1993) 21513-21518
57. Wilson, C. L., and Safe, S., 1998. Mechanisms of ligand-induced aryl hydrocarbon receptor-mediated biochemical and toxic responses. 26, 657-671.
58. Zoller A.L., and Kersh G.J. Estrogen induces thymic atrophy by eliminating early thymic progenitors and inhibiting proliferation of beta-selected thymocytes. J. Immunol. 176 (2006) 7371-7378
59. Zoller A.L., Schnell F.J., and Kersh G.J. Murine pregnancy leads to reduced proliferation of maternal thymocytes and decreased thymic emigration. Immunology 121 (2007) 207-215