An integrated genomic analysis of aryl hydrocarbon receptor-mediated inhibition of B-cell differentiation

Toxicological Sciences

Volumn 118, Issue 2, 2010, Pages 454-469

  De Abrew, K Nadira ^a   Kaminski, Norbert E ^b   Thomas, Russell S ^a  

^a HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

2,3,7,8 tetrachlorodibenzo p dioxin; Aryl hydrocarbon receptor; B cell differentiation; Chromatin immunoprecipitation; Gene expression microarrays

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; LIPOPOLYSACCHARIDE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CHROMATIN IMMUNOPRECIPITATION; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; GENOME ANALYSIS; GENOMICS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN BINDING;

ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE, TUMOR; DRUG THERAPY, COMBINATION; ENVIRONMENTAL POLLUTANTS; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOMICS; IMMUNOSUPPRESSIVE AGENTS; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, ARYL HYDROCARBON; SPLEEN; TETRACHLORODIBENZODIOXIN;

EID: 78549239910     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq265     Document Type: Article

References (62)

1. Barhoover, M.A., Hall, J.M., Greenlee, W.F., and Thomas, R.S. (2010). Aryl hydrocarbon receptor regulates cell cycle progression in human breast cancer cells via a functional interaction with cyclin-dependent kinase 4. Mol. Pharmacol. 77, 195-201.
2. Battistini, A. (2009). Interferon regulatory factors in hematopoietic cell differentiation and immune regulation. J. Interferon Cytokine Res. 29, 765-780.
3. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J.R. Stat. Soc. Ser. B 57, 289-300.
4. Bishop, G.A., and Haughton, G. (1986). Induced differentiation of a transformed clone of Ly-1+ B cells by clonal T cells and antigen. Proc. Natl. Acad. Sci. U.S.A. 83, 7410-7414.
5. Calame, K. (2008). Activation-dependent induction of Blimp-1. Curr. Opin. Immunol. 20, 259-264.
6. Calnan, D.R., and Brunet, A. (2008). The FoxO code. Oncogene 27, 2276-2288.
7. Chen, Y., Blackwell, T.W., Chen, J., Gao, J., Lee, A.W., and States, D.J. (2007). Integration of genome and chromatin structure with gene expression profiles to predict c-MYC recognition site binding and function. PLoS Comput. Biol. 3, e63.
8. Chung, J.B., Silverman, M., and Monroe, J.G. (2003). Transitional B cells: step by step towards immune competence. Trends Immunol. 24, 343-349.
9. Dabir, P., Marinic, T.E., Krukovets, I., and Stenina, O.I. (2008).Aryl hydrocarbon receptor is activated by glucose and regulates the thrombospondin-1 gene promoter in endothelial cells. Circ Res. 102, 1558-1565.
10. Dean, J., Hashimoto, K., Tsuji, T., Gautier, V., Hall, W.W., and Sheehy, N. (2009). Functional interaction of HTLV-1 tax protein with the POZ domain of the transcriptional repressor BCL6. Oncogene 28, 3723-3734.
11. Desrivieres, S., Kunz, C., Barash, I., Vafaizadeh, V., Borghouts, C., and Groner, B. (2006). The biological functions of the versatile transcription factors STAT3 and STAT5 and new strategies for their targeted inhibition. J. Mamm. Gland Biol. Neoplasia 11, 75-87.
12. Diehl, S.A., Schmidlin, H., Nagasawa, M., van Haren, S.D., Kwakkenbos, M.J., Yasuda, E., Beaumont, T., Scheeren, F.A., and Spits, H. (2008). STAT3-mediated up-regulation of BLIMP1 Is coordinated with BCL6 down-regulation to control human plasma cell differentiation. J Immunol 180, 4805-4815.
13. Dijkstra, E.W. (1959). A note on two problems in connexion with graphs. Numerische Mathematik 1, 269-271.
14. Dooley, R.K., and Holsapple, M.P. (1988). Elucidation of cellular targets responsible for tetrachlorodibenzo-p-dioxin (TCDD)-induced suppression of antibody responses: I. The role of the B lymphocyte. Immunopharmacology 16, 167-180.
15. Fernandez de Mattos, S., Essafi, A., Soeiro, I., Pietersen, A.M., Birkenkamp, K.U., Edwards, C.S., Martino, A., Nelson, B.H., Francis, J.M., Jones, M.C., et al. (2004). FoxO3a and BCR-ABL regulate cyclin D2 transcription through a STAT5/BCL6-dependent mechanism. Mol. Cell Biol. 24, 10058-10071.
16. Freedman, J.A., Chang, J.T., Jakoi, L., and Nevins, J.R. (2009). A combinatorial mechanism for determining the specificity of E2F activation and repression. Oncogene 28, 2873-2881.
17. Gasiewicz, T.A., Singh, K.P., and Casado, F.L. (2010). The aryl hydrocarbon receptor has an important role in the regulation of hematopoiesis: implications for benzene-induced hematopoietic toxicity. Chem. Biol. Interact. 184, 246-251.
18. Gu, Y.Z., Hogenesch, J.B., and Bradfield, C.A. (2000). The PAS superfamily: sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40, 519-561.
19. Gururajan, M., Simmons, A., Dasu, T., Spear, B.T., Calulot, C., Robertson, D.A., Wiest, D.L., Monroe, J.G., and Bondada, S. (2008). Early growth response genes regulate B cell development, proliferation, and immune response. J. Immunol. 181, 4590-4602.
20. Hardy, R.R., and Hayakawa, K. (2001). B cell development pathways. Annu. Rev. Immunol. 19, 595-621.
21. Hasbold, J., Lyons, A.B., Kehry, M.R., and Hodgkin, P.D. (1998). Cell division number regulates IgG1 and IgE switching of B cells following stimulation by CD40 ligand and IL-4. Eur. J. Immunol. 28, 1040-1051.
22. Holsapple, M.P., Dooley, R.K., McNerney, P.J., and McCay, J.A. (1986). Direct suppression of antibody responses by chlorinated dibenzodioxins in cultured spleen cells from (C57BL/6 x C3H)F1 and DBA/2 mice. Immunopharmacology 12, 175-186.
23. Holsapple, M.P., Snyder, N.K., Wood, S.C., and Morris, D.L. (1991). A review of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced changes in immunocompetence: 1991 update. Toxicology 69, 219-255.
24. Irizarry, R.A., Bolstad, B.M., Collin, F., Cope, L.M., Hobbs, B., and Speed, T.P. (2003). Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15.
25. Ji, H., Jiang, H., Ma, W., Johnson, D.S., Myers, R.M., and Wong, W.H. (2008). An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat. Biotechnol. 26, 1293-1300.
26. Johnson, K., Hashimshony, T., Sawai, C.M., Pongubala, J.M., Skok, J.A., Aifantis, I., and Singh, H. (2008). Regulation of immunoglobulin light-chain recombination by the transcription factor IRF-4 and the attenuation of interleukin-7 signaling. Immunity 28, 335-345.
27. Klein, B., Tarte, K., Jourdan, M., Mathouk, K., Moreaux, J., Jourdan, E., Legouffe, E., De Vos, J., and Rossi, J.F. (2003). Survival and proliferation factors of normal and malignant plasma cells. Int. J. Hematol. 78, 106-113.
28. Ku, S.C., Lee, J., Lau, J., Gurumurthy, M., Ng, R., Lwa, S.H., Klase, Z., Kashanchi, F., and Chao, S.H. (2008). XBP-1, a novel human T-lymphotropic virus type 1 (HTLV-1) tax binding protein, activates HTLV-1 basal and tax-activated transcription. J. Virol. 82, 4343-4353.
29. Lee, C.H., Melchers, M., Wang, H., Torrey, T.A., Slota, R., Qi, C.F., Kim, J.Y., Lugar, P., Kong, H.J., Farrington, L., et al. (2006a). Regulation of the germinal center gene program by interferon (IFN) regulatory factor 8/IFN consensus sequence-binding protein. J. Exp. Med. 203, 63-72.
30. Lee, K.A., Burgoon, L.D., Lamb, L., Dere, E., Zacharewski, T.R., Hogenesch, J.B., and LaPres, J.J. (2006b). Identification and characterization of genes susceptible to transcriptional cross-talk between the hypoxia and dioxin signaling cascades. Chem. Res. Toxicol. 19, 1284-1293.
31. Li, X.Y., MacArthur, S., Bourgon, R., Nix, D., Pollard, D.A., Iyer, V.N., Hechmer, A., Simirenko, L., Stapleton, M., Luengo Hendriks, C.L., et al. (2008). Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol. 6, e27.
32. Lin, B., Wang, J., Hong, X., Yan, X., Hwang, D., Cho, J.H., Yi, D., Utleg, A.G., Fang, X., Schones, D.E., et al. (2009). Integrated expression profiling and ChIP-seq analyses of the growth inhibition response program of the androgen receptor. PLoS ONE 4, e6589.
33. Lin, K.I., Angelin-Duclos, C., Kuo, T.C., and Calame, K. (2002). Blimp-1-dependent repression of Pax-5 is required for differentiation of B cells to immunoglobulin M-secreting plasma cells. Mol. Cell Biol. 22, 4771-4780.
34. Marcus, R.S., Holsapple, M.P., and Kaminski, N.E. (1998). Lipopolysaccharide activation of murine splenocytes and splenic B cells increased the expression of aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator. J. Pharmacol. Exp. Ther. 287, 1113-1118.
35. Martins, G., and Calame, K. (2008). Regulation and functions of Blimp-1 in T and B lymphocytes. Annu. Rev. Immunol. 26, 133-169.
36. McMahon, S.B., and Monroe, J.G. (1996). The role of early growth response gene 1 (egr-1) in regulation of the immune response. J. Leukoc. Biol. 60, 159-166.
37. Mora-Lopez, F., Pedreno-Horrillo, N., Delgado-Perez, L., Brieva, J.A., and Campos-Caro, A. (2008). Transcription of PRDM1, the master regulator for plasma cell differentiation, depends on an SP1/SP3/EGR-1 GC-box. Eur. J. Immunol. 38, 2316-2324.
38. Morris, D.L., Karras, J.G., and Holsapple, M.P. (1993). Direct effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on responses to lipopolysaccharide (LPS) by isolated murine B-cells. Immunopharmacology 26, 105-112.
39. Morse, R.H. (2007). Transcription factor access to promoter elements. J. Cell. Biochem. 102, 560-570.
40. North, C.M., Crawford, R.B., Lu, H., and Kaminski, N.E. (2009). Simultaneous in vivo time course and dose response evaluation for TCDDinduced impairment of the LPS-stimulated primary IgM response. Toxicol. Sci. 112, 123-132.
41. Patel, R.D., Murray, I.A., Flaveny, C.A., Kusnadi, A., and Perdew, G.H. (2009). Ah receptor represses acute-phase response gene expression without binding to its cognate response element. Lab. Invest. 89, 695-707.
42. Petrulis, J.R., and Perdew, G.H. (2002). The role of chaperone proteins in the aryl hydrocarbon receptor core complex. Chem. Biol. Interact. 141, 25-40.
43. 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, 517-554.
44. Reymann, S., and Borlak, J. (2006). Transcriptome profiling of human hepatocytes treated with Aroclor 1254 reveals transcription factor regulatory networks and clusters of regulated genes. BMC Genomics 7, 217.
45. Riley, R.L., Van der Put, E., King, A.M., Frasca, D., and Blomberg, B.B. (2005). Deficient B lymphopoiesis in murine senescence: potential roles for dysregulation of E2A, Pax-5, and STAT5. Semin. Immunol. 17, 330-336.
46. Sartor, M.A., Schnekenburger, M., Marlowe, J.L., Reichard, J.F., Wang, Y., Fan, Y., Ma, C., Karyala, S., Halbleib, D., Liu, X., et al. (2009). Genomewide analysis of aryl hydrocarbon receptor binding targets reveals an extensive array of gene clusters that control morphogenetic and developmental programs. Environ. Health Perspect. 117, 1139-1146.
47. Schneider, D., Manzan, M.A., Crawford, R.B., Chen, W., and Kaminski, N.E. (2008). 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD)-mediated impairment of B cell differentiation involves dysregulation of paired box 5 (Pax5) isoform, Pax5a. J. Pharmacol. Exp. Ther. 326, 463-474.
48. Schneider, D., Manzan, M.A., Yoo, B.S., Crawford, R.B., and Kaminski, N. (2009). Involvement of Blimp-1 and AP-1 dysregulation in the 2,3,7,8-tetrachlorodibenzo-p-dioxin-mediated suppression of the IgM response by B cells. Toxicol. Sci. 108, 377-388.
49. Sciammas, R., Shaffer, A.L., Schatz, J.H., Zhao, H., Staudt, L.M., and Singh, H. (2006). Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 25, 225-236.
50. Shaffer, A.L., Lin, K.I., Kuo, T.C., Yu, X., Hurt, E.M., Rosenwald, A., Giltnane, J.M., Yang, L., Zhao, H., Calame, K., et al. (2002). Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17, 51-62.
51. Shaffer, A.L., Yu, X., He, Y., Boldrick, J., Chan, E.P., and Staudt, L.M. (2000). BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity 13, 199-212.
52. Shapiro-Shelef, M., and Calame, K. (2005). Regulation of plasma-cell development. Nat. Rev. Immunol. 5, 230-242.
53. Suh, J., Jeon, Y.J., Kim, H.M., Kang, J.S., Kaminski, N.E., and Yang, K.H. (2002). 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, 116-123.
54. Sulentic, C.E., Holsapple, M.P., and Kaminski, N.E. (1998). Aryl hydrocarbon receptor-dependent suppression by 2,3,7, 8-tetrachlorodibenzop-dioxin of IgM secretion in activated B cells. Mol. Pharmacol. 53, 623-629.
55. Sulentic, C.E., Holsapple, M.P., and Kaminski, N.E. (2000). Putative link between transcriptional regulation of IgM expression by 2,3,7,8-tetrachlorodibenzo-p-dioxin and the aryl hydrocarbon receptor/dioxinresponsive enhancer signaling pathway. J. Pharmacol. Exp. Ther. 295, 705-716.
56. Sulentic, C.E., Kang, J.S., Na, Y.J., and Kaminski, N.E. (2004a). 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, 235-246.
57. Sulentic, C.E., Zhang, W., Na, Y.J., and Kaminski, N.E. (2004b). 2,3,7,8-tetrachlorodibenzo-p-dioxin, an exogenous modulator of the 3'alpha immunoglobulin heavy chain enhancer in the CH12.LX mouse cell line. J. Pharmacol. Exp. Ther. 309, 71-78.
58. Vorderstrasse, B.A., Steppan, L.B., Silverstone, A.E., and Kerkvliet, N.I. (2001). Aryl hydrocarbon receptor-deficient mice generate normal immune responses to model antigens and are resistant to TCDD-induced immune suppression. Toxicol. Appl. Pharmacol. 171, 157-164.
59. Watson, A.J., and Hankinson, O. (1992). Dioxin- and Ah receptor-dependent protein binding to xenobiotic responsive elements and G-rich DNA studied by in vivo footprinting. J. Biol. Chem. 267, 6874-6878.
60. Williams, C.E., Crawford, R.B., Holsapple, M.P., and Kaminski, N.E. (1996). Identification of functional aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator in murine splenocytes. Biochem. Pharmacol. 52, 771-780.
61. Yoo, B.S., Boverhof, D.R., Shnaider, D., Crawford, R.B., Zacharewski, T.R., and Kaminski, N.E. (2004). 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) alters the regulation of Pax5 in lipopolysaccharide-activated B cells. Toxicol. Sci. 77, 272-279.
62. Zhang, L., Savas, U., Alexander, D.L., and Jefcoate, C.R. (1998). Characterization of the mouse Cyp1B1 gene. Identification of an enhancer region that directs aryl hydrocarbon receptor-mediated constitutive and induced expression. J. Biol. Chem. 273, 5174-5183.