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

Toxicological Sciences

Volumn 108, Issue 2, 2009, Pages 377-388

  Schneider, Dina ^a,b   Manzan, Maria A ^b   Yoo, Byung Sun ^c   Crawford, Robert B ^a   Kaminski, Norbert ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Kyonggi University   (South Korea)

Author keywords

AP 1; B cell; Blimp 1; LPS; Pax5; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; IMMUNOGLOBULIN M; LIPOPOLYSACCHARIDE; MESSENGER RNA; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR PAX5;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CONTROLLED STUDY; FEMALE; HUMORAL IMMUNITY; IMMUNE DEFICIENCY; IMMUNE DYSREGULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; B-CELL-SPECIFIC ACTIVATOR PROTEIN; B-LYMPHOCYTES; CELL LINE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; IMMUNOGLOBULIN M; IMMUNOSUPPRESSIVE AGENTS; KINETICS; LIPOPOLYSACCHARIDES; LUCIFERASES; MICE; PLASMIDS; PROMOTER REGIONS, GENETIC; RECEPTORS, ARYL HYDROCARBON; RESPONSE ELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN; TETRACHLORODIBENZODIOXIN; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS; TRANSFECTION;

MURINAE;

EID: 64349123334     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp028     Document Type: Article

References (40)

1. Angelin-Duclos, C., Cattoretti, G., Lin, K. I., and Calame, K. (2000). Commitment of B lymphocytes to a plasma cell fate is associated with Blimp-1 expression in vivo. J. Immunol. 165, 5462-5471.
2. 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.
3. Denison, M. S., and Yao, E. F. (1991). Characterization of the interaction of transformed rat hepatic cytosolic Ah receptor with a dioxin responsive transcriptional enhancer. Arch. Biochem. Biophys. 284, 158-166.
4. Dooley, R. K., and Holsapple, M. P. (1988). Elucidation of the cellular targets responsible for 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced suppression of the antibody response: I. The role of the B lymphocyte. Immunopharmacology 16, 167-180.
5. Faubert, B. L., and Kaminski, N. E. (2000). AP-1 activity is negatively regulated by cannabinol through inhibition of its protein components, c-fos and c-jun. J. Leuk. Biol. 67, 259-266.
6. Hankinson, O. (1995). The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 35, 307-340.
7. 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.
8. Kallies, A., and Nutt, S. L. (2007). Terminal differentiation of lymphocytes depends on Blimp-1. Curr. Opin. Immunol. 19, 156-162.
9. Karin, M., Liu, Z., and Zandi, E. (1997). AP-1 function and regulation. Curr. Opin. Cell. Biol. 9, 240-246.
10. Kerkvliet, N. I., Steppan, L. B., Brauner, J. A., Deyo, J. A., Henderson, M. C., Tomar, R. S., and Buhler, D. R. (1990). Influence of the Ah locus on the humoral immunotoxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin: Evidence for Ah-receptor-dependent and Ah-receptor-independent mechanisms of immunosuppression. Toxicol. Appl. Pharmacol. 105, 26-36.
11. Lees, M. J., and Whitelaw, M. L. (2002). Effect of ARA9 on dioxin receptor mediated transcription. Toxicology 181-182, 143-146.
12. 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.
13. Mora-Lopez, F., Reales, E., Brieva, J. A., and Campos-Caro, A. (2007). Human BSAP and BLIMP1 conform an autoregulatory feedback loop. Blood 110, 3150-3157.
14. Neurath, M. F., Strober, W., and Wakatsuki, Y. (1994). The murine Ig 3′ alpha enhancer is a target site with repressor function for the B cell lineage-specific transcription factor BSAP (NF-HB, S alpha-BP). J. Immunol. 153, 730-742.
15. Novak, T. J., White, P. M., and Rothenberg, E. V. (1990). Regulatory anatomy of the murine interleukin-2 gene. Nucleic Acids Res. 18 4523-4533.
16. Ohkubo, Y., Arima, M., Arguni, E., Okada, S., Yamashita, K., Asari, S., Obata, S., Sakamoto, A., Hatano, M., O-Wang, J., et al. (2005). A role for c-fos/activator protein 1 in B lymphocyte terminal differentiation. J. Immunol. 174, 7703-7710.
17. Perdew, G. H. (1988). Association of the Ah receptor with the 90-kDa heat shock protein. J. Biol. Chem. 263, 13802-13805.
18. Puga, A., Nebert, D. W., and Carrier, F. (1992). Dioxin induces expression of c-fos and c-jun proto-oncogenes and a large increase in transcription factor AP-1. DNA Cell Biol. 11, 269-281.
19. Reimold, A. M., Ponath, P. D., Li, Y. S., Hardy, R. R., David, C. S., Strominger, J. L., and Glimcher, L. H. (1996). Transcription factor B cell lineage-specific activator protein regulates the gene for human X-box binding protein 1. J. Exp. Med. 183, 393-401.
20. Rinkenberger, J. L., Wallin, J. J., Johnson, K. W., and Koshland, M. E. (1996). An interleukin-2 signal relieves BSAP (Pax5)-mediated repression of the immunoglobulin J chain gene. Immunity 5, 377-386.
21. Safe, S., Wang, F., Porter, W., Duan, R., and McDougal, A. (1998). Ah receptor agonists as endocrine disruptors: Antiestrogenic activity and mechanisms. Toxicol. Lett. 102-103, 343-347.
22. Safe, S., Wormke, M., and Samudio, I. (2000). Mechanisms of inhibitory aryl hydrocarbon receptor-estrogen receptor crosstalk in human breast cancer cells. J. Mammary Gland Biol. Neoplasia 5, 295-306.
23. Savitsky, D., and Calame, K. (2006). B-1 B lymphocytes require Blimp-1 for immunoglobulin secretion. J. Exp. Med. 203, 2305-2314.
24. 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.
25. Shaffer, A. L., Peng, A., and Schlissel, M. S. (1997). In vivo occupancy of the kappa light chain enhancers in primary pro- and pre-B cells: A model for kappa locus activation. Immunity 6, 131-143.
26. Singh, M., and Birshtein, B. K. (1993). NF-HB (BSAP) is a repressor of the murine immunoglobulin heavy-chain 3′ alpha enhancer at early stages of B-cell differentiation. Mol. Cell. Biol. 13, 3611-3622.
27. 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.
28. Sulentic, C. E., Holsapple, M. P., and Kaminski, N. E. (1998). Aryl hydrocarbon receptor-dependent suppression by 2,3,7,8-tetrachlorodibenzo-p-dioxin of IgM secretion in activated B cells. Mol. Pharmacol. 53, 623-629.
29. 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/ dioxin-responsive enhancer signaling pathway. J. Pharmacol. Exp. Ther. 295, 705-716.
30. 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.
31. 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.
32. Sun, Y. V., Boverhof, D. R., Burgoon, L. D., Fielden, M. R., and Zacharewski, T. R. (2004). Comparative analysis of dioxin response elements in human, mouse and rat genomic sequences. Nucleic Acids Res. 32, 4512-4523.
33. Swanson, H. I., Tullis, K., and Denison, M. S. (1993). Binding of transformed Ah receptor complex to a dioxin responsive transcriptional enhancer: Evidence for two distinct heteromeric DNA-binding forms. Biochemistry 32, 12841-12849.
34. Tucker, A. N., Vore, S. J., and Luster, M. I. (1986). Suppression of B cell differentiation by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Mol. Pharmacol. 29, 372-377.
35. Tunyaplin, C., Shapiro, M. A., and Calame, K. L. (2000). Characterization of the B lymphocyte-induced maturation protein-1 (Blimp-1) gene, mRNA isoforms and basal promoter. Nucleic Acids Res. 28, 4846-4855.
36. Turner, C. A., Jr., Mack, D. H., and Davis, M. M. (1994). Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 77, 297-306.
37. Vasanwala, F. H., Kusam, S., Toney, L. M., and Dent, A. L. (2002). Repression of AP-1 function: A mechanism for the regulation of Blimp-1 expression and B lymphocyte differentiation by the B cell lymphoma-6 protooncogene. J. Immunol. 169, 1922-1929.
38. 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.
39. Yao, E. F., and Denison, M. S. (1992). DNA sequence determinants for binding of transformed Ah receptor to a dioxin-responsive enhancer. Biochemistry 31, 5060-5067.
40. 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.