Regulation of Bach2 by the aryl hydrocarbon receptor as a mechanism for suppression of B-cell differentiation by 2,3,7,8-tetrachlorodibenzo-p-dioxin

Toxicology and Applied Pharmacology

Volumn 252, Issue 2, 2011, Pages 150-158

  De Abrew, K Nadira ^a   Phadnis, Ashwini S ^b   Crawford, Robert B ^b   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; AHR; B cell differentiation; Bach2

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; IMMUNOGLOBULIN M; LIPOPOLYSACCHARIDE; PROTEIN BACH2; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BACH2 GENE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE; IMMUNOGLOBULIN PRODUCTION; INTRON; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN DNA BINDING; QUANTITATIVE ANALYSIS; RECEPTOR AFFINITY; RNA INTERFERENCE; TRANSCRIPTION REGULATION; VALIDATION PROCESS;

ANIMALS; B-LYMPHOCYTES; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE, TUMOR; GENE KNOCKOUT TECHNIQUES; GROWTH INHIBITORS; MICE; PROTEIN BINDING; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN;

EID: 79953698712     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.01.020     Document Type: Article

References (32)

1. Andrews N.C., Faller D.V. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 1991, 19:2499.
2. Bishop G.A., Haughton G. Induced differentiation of a transformed clone of Ly-1+ B cells by clonal T cells and antigen. Proc. Natl Acad. Sci. USA 1986, 83:7410-7414.
3. Calame K. Activation-dependent induction of Blimp-1. Curr. Opin. Immunol. 2008, 20:259-264.
4. Chen Y., Blackwell T.W., Chen J., Gao J., Lee A.W., States D.J. Integration of genome and chromatin structure with gene expression profiles to predict c-MYC recognition site binding and function. PLoS Comput. Biol. 2007, 3:e63.
5. Chung J.B., Silverman M., Monroe J.G. Transitional B cells: step by step towards immune competence. Trends Immunol. 2003, 24:343-349.
6. De Abrew K.N., Kaminski N.E., Thomas R.S. An integrated genomic analysis of aryl hydrocarbon receptor-mediated inhibition of B-cell differentiation 2010, Toxicol Sci.
7. Dean J., Hashimoto K., Tsuji T., Gautier V., Hall W.W., Sheehy N. Functional interaction of HTLV-1 tax protein with the POZ domain of the transcriptional repressor BCL6. Oncogene 2009, 28:3723-3734.
8. Denison M.S., Yao E.F. Characterization of the interaction of transformed rat hepatic cytosolic Ah receptor with a dioxin responsive transcriptional enhancer. Arch. Biochem. Biophys. 1991, 284:158-166.
9. Dooley R.K., Holsapple M.P. Elucidation of cellular targets responsible for tetrachlorodibenzo-p-dioxin (TCDD)-induced suppression of antibody responses: I. The role of the B lymphocyte. Immunopharmacology 1988, 16:167-180.
10. Gu Y.Z., Hogenesch J.B., Bradfield C.A. The PAS superfamily: sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 2000, 40:519-561.
11. Hardy R.R., Hayakawa K. B cell development pathways. Annu. Rev. Immunol. 2001, 19:595-621.
12. Holsapple M.P., Dooley R.K., McNerney P.J., McCay J.A. Direct suppression of antibody responses by chlorinated dibenzodioxins in cultured spleen cells from (C57BL/6 x C3H)F1 and DBA/2 mice. Immunopharmacology 1986, 12:175-186.
13. Igarashi K., Ochiai K., Muto A. Architecture and dynamics of the transcription factor network that regulates B-to-plasma cell differentiation. J. Biochem. 2007, 141:783-789.
14. Ku S.C., Lee J., Lau J., Gurumurthy M., Ng R., Lwa S.H., Klase Z., Kashanchi F., Chao S.H. 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. 2008, 82:4343-4353.
15. 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., van der Zouwen B., Zhou J.X., Lougaris V., Lipsky P.E., Grammer A.C., Morse H.C. Regulation of the germinal center gene program by interferon (IFN) regulatory factor 8/IFN consensus sequence-binding protein. J. Exp. Med. 2006, 203:63-72.
16. Lin K.I., Angelin-Duclos C., Kuo T.C., Calame K. Blimp-1-dependent repression of Pax-5 is required for differentiation of B cells to immunoglobulin M-secreting plasma cells. Mol. Cell. Biol. 2002, 22:4771-4780.
17. Morris D.L., Karras J.G., Holsapple M.P. Direct effects of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) on responses to lipopolysaccharide (LPS) by isolated murine B-cells. Immunopharmacology 1993, 26:105-112.
18. Muto A., Hoshino H., Madisen L., Yanai N., Obinata M., Karasuyama H., Hayashi N., Nakauchi H., Yamamoto M., Groudine M., Igarashi K. Identification of Bach2 as a B-cell-specific partner for small maf proteins that negatively regulate the immunoglobulin heavy chain gene 3' enhancer. EMBO J. 1998, 17:5734-5743.
19. Ochiai K., Katoh Y., Ikura T., Hoshikawa Y., Noda T., Karasuyama H., Tashiro S., Muto A., Igarashi K. Plasmacytic transcription factor Blimp-1 is repressed by Bach2 in B cells. J. Biol. Chem. 2006, 281:38226-38234.
20. Ochiai K., Muto A., Tanaka H., Takahashi S., Igarashi K. Regulation of the plasma cell transcription factor Blimp-1 gene by Bach2 and Bcl6. Int. Immunol. 2008, 20:453-460.
21. Ohkubo Y., Arima M., Arguni E., Okada S., Yamashita K., Asari S., Obata S., Sakamoto A., Hatano M., J, O.W., Ebara M., Saisho H., Tokuhisa T. A role for c-fos/activator protein 1 in B lymphocyte terminal differentiation. J. Immunol. 2005, 174:7703-7710.
22. Petrulis J.R., Perdew G.H. The role of chaperone proteins in the aryl hydrocarbon receptor core complex. Chem. Biol. Interact. 2002, 141:25-40.
23. Probst M.R., Reisz-Porszasz S., Agbunag R.V., Ong M.S., Hankinson O. Role of the aryl hydrocarbon receptor nuclear translocator protein in aryl hydrocarbon (dioxin) receptor action. Mol. Pharmacol. 1993, 44:511-518.
24. Schneider D., Manzan M.A., Yoo B.S., Crawford R.B., Kaminski N. 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. 2009, 108:377-388.
25. 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., Staudt L.M. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 2002, 17:51-62.
26. Shaffer A.L., Yu X., He Y., Boldrick J., Chan E.P., Staudt L.M. BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity 2000, 13:199-212.
27. Sulentic C.E., Holsapple M.P., Kaminski N.E. Aryl hydrocarbon receptor-dependent suppression by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin of IgM secretion in activated B cells. Mol. Pharmacol. 1998, 53:623-629.
28. Sulentic C.E., Kang J.S., Na Y.J., 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 2004, 200:235-246.
29. Sulentic C.E., Zhang W., Na Y.J., Kaminski N.E. 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. 2004, 309:71-78.
30. Swanson H.I., Chan W.K., Bradfield C.A. DNA binding specificities and pairing rules of the Ah receptor, ARNT, and SIM proteins. J. Biol. Chem. 1995, 270:26292-26302.
31. Williams C.E., Crawford R.B., Holsapple M.P., Kaminski N.E. Identification of functional aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator in murine splenocytes. Biochem. Pharmacol. 1996, 52:771-780.
32. Yoo B.S., Boverhof D.R., Shnaider D., Crawford R.B., Zacharewski T.R., Kaminski N.E. 2, 3, 7, 8-Tetrachlorodibenzo-p-dioxin (TCDD) alters the regulation of Pax5 in lipopolysaccharide-activated B cells. Toxicol. Sci. 2004, 77:272-279.