Microarray analysis of the AHR system: Tissue-specific flexibility in signal and target genes

Toxicology and Applied Pharmacology

Volumn 220, Issue 3, 2007, Pages 320-332

  Frericks, Markus ^a   Meissner, Marc ^a   Esser, Charlotte ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Aryl hydrocarbon receptor; CYP1A1; Meta analysis; Microarray; PAS bHLH; T cells

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CYTOCHROME P450 1A1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; LIGAND; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL LINEAGE; COMPUTER MODEL; DENDRITIC CELL; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC DATABASE; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VALIDATION PROCESS;

ANIMALS; CELL LINEAGE; GENE EXPRESSION PROFILING; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MALE; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, ARYL HYDROCARBON; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TISSUE ARRAY ANALYSIS;

MURINAE;

EID: 34247240980     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2007.01.014     Document Type: Article

References (81)

1. Abbott B.D., Held G.A., Wood C.R., Buckalew A.R., Brown J.G., and Schmid J. AhR, ARNT, and CYP1A1 mRNA quantitation in cultured human embryonic palates exposed to TCDD and comparison with mouse palate in vivo and in culture. Toxicol. Sci. 47 (1999) 62-75
2. Abbott B.D., Schmid J.E., Brown J.G., Wood C.R., White R.D., Buckalew A.R., and Held G.A. RT-PCR quantification of AHR, ARNT, GR, and CYP1A1 mRNA in craniofacial tissues of embryonic mice exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin and hydrocortisone. Toxicol. Sci. 47 (1999) 76-85
3. Adachi J., Mori Y., Matsui S., Takigami H., Fujino J., Kitagawa H., Miller III C.A., Kato T., Saeki K., and Matsuda T. Indirubin and indigo are potent aryl hydrocarbon receptor ligands present in human urine. J. Biol. Chem. 276 (2001) 31475-31478
4. Baldock R.A., Bard J.B., Burger A., Burton N., Christiansen J., Feng G., Hill B., Houghton D., Kaufman M., Rao J., Sharpe J., Ross A., Stevenson P., Venkataraman S., Waterhouse A., Yang Y., and Davidson D.R. EMAP and EMAGE: a framework for understanding spatially organized data. Neuroinformatics 1 (2003) 309-325
5. Barrett T., Suzek T.O., Troup D.B., Wilhite S.E., Ngau W.C., Ledoux P., Rudnev D., Lash A.E., Fujibuchi W., and Edgar R. NCBI GEO: mining millions of expression profiles-database and tools. Nucleic Acids Res. 33 (2005) D562-D566
6. Barrow L.L., Wines M.E., Romitti P.A., Holdener B.C., and Murray J.C. Aryl hydrocarbon receptor nuclear translocator 2 (ARNT2): structure, gene mapping, polymorphisms, and candidate evaluation for human orofacial clefts. Teratology 66 (2002) 85-90
7. Bono H., Kasukawa T., Hayashizaki Y., and Okazaki Y. READ: RIKEN Expression Array Database. Nucleic Acids Res. 30 (2002) 211-213
8. Brazma A., Hingamp P., Quackenbush J., Sherlock G., Spellman P., Stoeckert C., Aach J., Ansorge W., Ball C.A., Causton H.C., Gaasterland T., Glenisson P., Holstege F.C., Kim I.F., Markowitz V., Matese J.C., Parkinson H., Robinson A., Sarkans U., Schulze-Kremer S., Stewart J., Taylor R., Vilo J., and Vingron M. Minimum information about a microarray experiment (MIAME)-Toward standards for microarray data. Nat. Genet. 29 (2001) 365-371
9. Brazma A., Parkinson H., Sarkans U., Shojatalab M., Vilo J., Abeygunawardena N., Holloway E., Kapushesky M., Kemmeren P., Lara G.G., Oezcimen A., Rocca-Serra P., and Sansone S.A. ArrayExpress-A public repository for microarray gene expression data at the EBI. Nucleic Acids Res. 31 (2003) 68-71
10. Carver L.A., Hogenesch J.B., and Bradfield C.A. Tissue specific expression of the rat Ah-receptor and ARNT mRNAs. Nucleic Acids Res. 22 (1994) 3038-3044
11. Carver L.A., Jackiw V., and Bradfield C.A. The 90-kDa heat shock protein is essential for Ah receptor signaling in a yeast expression system. J. Biol. Chem. 269 (1994) 30109-30112
12. Chen H.S., and Perdew G.H. Subunit composition of the heteromeric cytosolic aryl hydrocarbon receptor complex. J. Biol. Chem. 269 (1994) 27554-27558
13. Cope L.M., Irizarry R.A., Jaffee H.A., Wu Z., and Speed T.P. A benchmark for Affymetrix GeneChip expression measures. Bioinformatics 20 (2004) 323-331
14. Dalton T.P., Puga A., and Shertzer H.G. Induction of cellular oxidative stress by aryl hydrocarbon receptor activation. Chem. Biol. Interact. 141 (2002) 77-95
15. Döhr O., Li W., Donat S., Vogel C., and Abel J. Aryl hydrocarbon receptor mRNA levels in different tissues of 2,3,7,8-tetrachlorodibenzo-p-dioxin-responsive and nonresponsive mice. Adv. Exp. Med. Biol. 387 (1996) 447-459
16. Edgar R., Domrachev M., and Lash A.E. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30 (2002) 207-210
17. Elferink C.J., Ge N.L., and Levine A. Maximal aryl hydrocarbon receptor activity depends on an interaction with the retinoblastoma protein. Mol. Pharmacol. 59 (2001) 664-673
18. Esser C. The role of the Ah-Receptor in the immune system: heading from toxicology to immunology. Recent Res. Dev. Mol. Pharmacol. 1 (2002) 141-155
19. Fitzgerald C.T., Fernandez-Salguero P., Gonzalez F.J., Nebert D.W., and Puga A. Differential regulation of mouse Ah receptor gene expression in cell lines of different tissue origins. Arch. Biochem. Biophys. 333 (1996) 170-178
20. Fitzgerald C.T., Nebert D.W., and Puga A. Regulation of mouse Ah receptor (Ahr) gene basal expression by members of the Sp family of transcription factors. DNA Cell Biol. 17 (1998) 811-822
21. Fletcher N., Wahlstrom D., Lundberg R., Nilsson C.B., Nilsson K.C., Stockling K., Hellmold H., and 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. 207 (2005) 1-24
22. Forkert P.G. Coexpression of Ah receptor and CYP1A1 in hepatocytes of C57BL/6J and DBA/2J mice. Toxicol. Appl. Pharmacol. 142 (1997) 69-78
23. 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
24. + cells with characteristics of regulatory T cells. J. Immunol. 175 (2005) 4184-4188
25. Ge N.L., and Elferink C.J. A direct interaction between the aryl hydrocarbon receptor and retinoblastoma protein. Linking dioxin signaling to the cell cycle. J. Biol. Chem. 273 (1998) 22708-22713
26. Gonzalez F.J., and Fernandez-Salguero P. The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab. Dispos. 26 (1998) 1194-1198
27. Hankinson O. Role of coactivators in transcriptional activation by the aryl hydrocarbon receptor. Arch. Biochem. Biophys. 433 (2005) 379-386
28. Hanlon P.R., Zheng W., Ko A.Y., and Jefcoate C.R. Identification of novel TCDD-regulated genes by microarray analysis. Toxicol. Appl. Pharmacol. 202 (2005) 215-228
29. Hekstra D., Taussig A.R., Magnasco M., and Naef F. Absolute mRNA concentrations from sequence-specific calibration of oligonucleotide arrays. Nucleic Acids Res. 31 (2003) 1962-1968
30. Held G.A., Grinstein G., and Tu Y. Relationship between gene expression and observed intensities in DNA microarrays-a modeling study. Nucleic Acids Res. 34 (2006) 70
31. Hishiki T., Kawamoto S., Morishita S., and Okubo K. BodyMap: a human and mouse gene expression database. Nucleic Acids Res. 28 (2000) 136-138
32. Ikeo K., Ishi-i J., Tamura T., Gojobori T., and Tateno Y. CIBEX: center for information biology gene expression database. C.R. Biol. 326 (2003) 1079-1082
33. Irizarry R.A., Warren D., Spencer F., Kim I.F., Biswal S., Frank B.C., Gabrielson E., Garcia J.G., Geoghegan J., Germino G., Griffin C., Hilmer S.C., Hoffman E., Jedlicka A.E., Kawasaki E., Martinez-Murillo F., Morsberger L., Lee H., Petersen D., Quackenbush J., Scott A., Wilson M., Yang Y., Ye S.Q., and Yu W. Multiple-laboratory comparison of microarray platforms. Nat. Methods 2 (2005) 345-350
34. Jain S., Maltepe E., Lu M.M., Simon C., and Bradfield C.A. Expression of ARNT, ARNT2, HIF1 alpha, HIF2 alpha and Ah receptor mRNAs in the developing mouse. Mech. Dev. 73 (1998) 117-123
35. Karyala S., Guo J., Sartor M., Medvedovic M., Kann S., Puga A., Ryan P., and Tomlinson C.R. Different global gene expression profiles in benzo[a]pyrene- and dioxin-treated vascular smooth muscle cells of AHR-knockout and wild-type mice. Cardiovasc. Toxicol. 4 (2004) 47-73
36. Kerkvliet N.I. Recent advances in understanding the mechanisms of TCDD immunotoxicity. Int. Immunopharmacol. 2 (2002) 277-291
37. Kinoshita K., Kikuchi Y., Sasakura Y., Suzuki M., Fujii-Kuriyama Y., and Sogawa K. Altered DNA binding specificity of Arnt by selection of partner bHLH-PAS proteins. Nucleic Acids Res. 32 (2004) 3169-3179
38. Kong S.W., Hwang K.B., Kim R.D., Zhang B.T., Greenberg S.A., Kohane I.S., and Park P.J. CrossChip: a system supporting comparative analysis of different generations of Affymetrix arrays. Bioinformatics 21 (2005) 2116-2117
39. Lai Z.W., Hundeiker C., Gleichmann E., and Esser C. Cytokine gene expression during ontogeny in murine thymus on activation of the aryl hydrocarbon receptor by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Mol. Pharmacol. 52 (1997) 30-37
40. Laiosa M.D., Wyman A., Murante F.G., Fiore N.C., Staples J.E., Gasiewicz T.A., and Silverstone A.E. Cell proliferation arrest within intrathymic lymphocyte progenitor cells causes thymic atrophy mediated by the aryl hydrocarbon receptor. J. Immunol. 171 (2003) 4582-4591
41. Larkin J.E., Frank B.C., Gavras H., Sultana R., and Quackenbush J. Independence and reproducibility across microarray platforms. Nat. Methods 2 (2005) 337-344
42. Laupeze B., Amiot L., Sparfel L., Le Ferrec E., Fauchet R., and Fardel O. Polycyclic aromatic hydrocarbons affect functional differentiation and maturation of human monocyte-derived dendritic cells. J. Immunol. 168 (2002) 2652-2658
43. Lawrence B.P., Leid M., and Kerkvliet N.I. Distribution and behavior of the Ah receptor in murine T lymphocytes. Toxicol. Appl. Pharmacol. 138 (1996) 275-284
44. Li W., Donat S., Döhr O., Unfried K., and Abel J. Ah receptor in different tissues of C57BL/6J and DBA/2J mice: use of competitive polymerase chain reaction to measure Ah-receptor mRNA expression. Arch. Biochem. Biophys. 315 (1994) 279-284
45. Liu X., and Jefcoate C. 2,3,7,8-Tetrachlorodibenzo-p-dioxin and epidermal growth factor cooperatively suppress peroxisome proliferator-activated receptor-{gamma}1 stimulation and restore focal adhesion complexes during adipogenesis: selective contributions of Src, Rho, and Erk distinguish these overlapping processes in C3H10T1/2 cells. Mol. Pharmacol. 70 (2006) 1902-1915
46. Lockhart D.J., and Winzeler E.A. Genomics, gene expression and DNA arrays. Nature 405 (2000) 827-836
47. Ma Q., and Baldwin K.T. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced degradation of aryl hydrocarbon receptor (AhR) by the ubiquitin-proteasome pathway. Role of the transcription activation and DNA binding of AhR. J. Biol. Chem. 275 (2000) 8432-8438
48. 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
49. Mehrabi M.R., Steiner G.E., Dellinger C., Kofler A., Schaufler K., Tamaddon F., Plesch K., Ekmekcioglu C., Maurer G., Glogar H.D., and Thalhammer T. The arylhydrocarbon receptor (AhR), but not the AhR-nuclear translocator (ARNT), is increased in hearts of patients with cardiomyopathy. Virchows Arch. 441 (2002) 481-489
50. Meyer B.K., and Perdew G.H. Characterization of the AhR-hsp90-XAP2 core complex and the role of the immunophilin-related protein XAP2 in AhR stabilization. Biochemistry 38 (1999) 8907-8917
51. Mimura J., and Fujii-Kuriyama Y. Functional role of AhR in the expression of toxic effects by TCDD. Biochim. Biophys. Acta 1619 (2003) 263-268
52. Mimura J., Yamashita K., Nakamura K., Morita M., Takagi T.N., Nakao K., Ema M., Sogawa K., Yasuda M., Katsuki M., and Fujii-Kuriyama Y. Loss of teratogenic response to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice lacking the Ah (dioxin) receptor. Genes Cells 2 (1997) 645-654
53. Novosad J., Fiala Z., Borska L., and Krejsek J. Immunosuppressive effect of polycyclic aromatic hydrocarbons by induction of apoptosis of pre-B lymphocytes of bone marrow. Acta Medica.(Hradec. Kralove) 45 (2002) 123-128
54. Oishi K., Miyazaki K., Kadota K., Kikuno R., Nagase T., Atsumi G., Ohkura N., Azama T., Mesaki M., Yukimasa S., Kobayashi H., Iitaka C., Umehara T., Horikoshi M., Kudo T., Shimizu Y., Yano M., Monden M., Machida K., Matsuda J., Horie S., Todo T., and Ishida N. Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J. Biol. Chem. 278 (2003) 41519-41527
55. Okey A.B., Riddick D.S., and Harper P.A. The Ah receptor: mediator of the toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and related compounds. Toxicol. Lett. 70 (1994) 1-22
56. Park P.J., Cao Y.A., Lee S.Y., Kim J.W., Chang M.S., Hart R., and Choi S. Current issues for DNA microarrays: platform comparison, double linear amplification, and universal RNA reference. J. Biotechnol. 112 (2004) 225-245
57. Parkinson H., Sarkans U., Shojatalab M., Abeygunawardena N., Contrino S., Coulson R., Farne A., Lara G.G., Holloway E., Kapushesky M., Lilja P., Mukherjee G., Oezcimen A., Rayner T., Rocca-Serra P., Sharma A., Sansone S., and Brazma A. ArrayExpress-a public repository for microarray gene expression data at the EBI. Nucleic Acids Res. 33 (2005) D553-D555
58. Passey R.J., Williams E., Lichanska A.M., Wells C., Hu S., Geczy C.L., Little M.H., and Hume D.A. A null mutation in the inflammation-associated S100 protein S100A8 causes early resorption of the mouse embryo. J. Immunol. 163 (1999) 2209-2216
59. Puga A., Maier A., and Medvedovic M. The transcriptional signature of dioxin in human hepatoma HepG2 cells. Biochem. Pharmacol. 60 (2000) 1129-1142
60. Puga A., Xia Y., and Elferink C. Role of the aryl hydrocarbon receptor in cell cycle regulation. Chem. Biol. Interact. 141 (2002) 117-130
61. Rannug A., and Fritsche E. The aryl hydrocarbon receptor and light. Biol. Chem. 387 (2006) 1149-1157
62. Safe S., Wormke M., and Samudio I. Mechanisms of inhibitory aryl hydrocarbon receptor-estrogen receptor crosstalk in human breast cancer cells. J. Mammary. Gland. Biol. Neoplasia. 5 (2000) 295-306
63. Schmidt J.V., and Bradfield C.A. Ah receptor signaling pathways. Annu. Rev. Cell Dev. Biol. 12 (1996) 55-89
64. Sekine H., Mimura J., Yamamoto M., and Fujii-Kuriyama Y. Unique and overlapping transcriptional roles of Arnt (Arylhydrocarbon receptor nuclear translocator) and Arnt2 in xenobiotic and hypoxic responses. J. Biol. Chem (2006)
65. Severgnini M., Bicciato S., Mangano E., Scarlatti F., Mezzelani A., Mattioli M., Ghidoni R., Peano C., Bonnal R., Viti F., Milanesi L., De Bellis G., and Battaglia C. Strategies for comparing gene expression profiles from different microarray platforms: application to a case-control experiment. Anal. Biochem. 353 (2006) 43-56
66. Shimada T., Sugie A., Shindo M., Nakajima T., Azuma E., Hashimoto M., and Inoue K. Tissue-specific induction of cytochromes P450 1A1 and 1B1 by polycyclic aromatic hydrocarbons and polychlorinated biphenyls in engineered C57BL/6J mice of arylhydrocarbon receptor gene. Toxicol. Appl. Pharmacol. 187 (2003) 1-10
67. Silverstone A.E., Frazier Jr. D.E., and Gasiewicz T.A. Alternate immune system targets for TCDD: lymphocyte stem cells and extrathymic T-cell development. Exp. Clin. Immunogenet. 11 (1994) 94-101
68. Sinal C.J., and Bend J.R. Aryl hydrocarbon receptor-dependent induction of cyp1a1 by bilirubin in mouse hepatoma hepa 1c1c7 cells. Mol. Pharmacol. 52 (1997) 590-599
69. Stoeckert Jr. C.J., Causton H.C., and Ball C.A. Microarray databases: standards and ontologies. Nat. Genet. 32 Suppl (2002) 469-473
70. 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
71. Swanson H.I. DNA binding and protein interactions of the AHR/ARNT heterodimer that facilitate gene activation. Chem. Biol. Interact. 141 (2002) 63-76
72. Temchura V.V., Frericks M., Nacken W., and Esser C. Role of the aryl hydrocarbon receptor in thymocyte emigration in vivo. Eur. J. Immunol. 35 (2005) 2738-2747
73. 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
74. Thackaberry E.A., Gabaldon D.M., Walker M.K., and Smith S.M. Aryl hydrocarbon receptor null mice develop cardiac hypertrophy and increased hypoxia-inducible factor-1alpha in the absence of cardiac hypoxia. Cardiovasc. Toxicol. 2 (2002) 263-274
75. Thomae T.L., Glover E., and Bradfield C.A. A maternal Ahr null genotype sensitizes embryos to chemical teratogenesis. J. Biol. Chem. 279 (2004) 30189-30194
76. Tijet N., Boutros P.C., Moffat I.D., Okey A.B., Tuomisto J., and Pohjanvirta R. Aryl hydrocarbon receptor regulates distinct dioxin-dependent and dioxin-independent gene batteries. Mol. Pharmacol. 69 (2006) 140-153
77. Vasquez A., Atallah-Yunes N., Smith F.C., You X., Chase S.E., Silverstone A.E., and Vikstrom K.L. A role for the aryl hydrocarbon receptor in cardiac physiology and function as demonstrated by AhR knockout mice. Cardiovasc. Toxicol. 3 (2003) 153-163
78. Vogel C., Donat S., Döhr O., Kremer J., Esser C., Roller M., and Abel J. Effect of subchronic 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on immune system and target gene responses in mice: calculation of benchmark doses for CYP1A1 and CYP1A2 related enzyme activities. Arch.Toxicol. 71 (1997) 372-382
79. Walker M.K., Pollenz R.S., and Smith S.M. Expression of the aryl hydrocarbon receptor (AhR) and AhR nuclear translocator during chick cardiogenesis is consistent with 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced heart defects. Toxicol. Appl. Pharmacol. 143 (1997) 407-419
80. Wood S.M., Gleadle J.M., Pugh C.W., Hankinson O., and Ratcliffe P.J. The role of the aryl hydrocarbon receptor nuclear translocator (ARNT) in hypoxic induction of gene expression. Studies in ARNT-deficient cells. J. Biol. Chem. 271 (1996) 15117-15123
81. Yamaguchi K., Near R.I., Matulka R.A., Shneider A., Toselli P., Trombino A.F., and Sherr D.H. Activation of the aryl hydrocarbon receptor/transcription factor and bone marrow stromal cell-dependent preB cell apoptosis. J. Immunol. 158 (1997) 2165-2173