2,3,7,8-Tetrachlorodibenzo-p-dioxin-mediated impairment of B cell differentiation involves dysregulation of paired box 5 (Pax5) isoform, Pax5a

Journal of Pharmacology and Experimental Therapeutics

Volumn 326, Issue 2, 2008, Pages 463-474

  Schneider, Dina ^a,b   Manzan, Maria A ^b   Crawford, Robert B ^a   Chen, Weimin ^c   Kaminski, Norbert E ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; IMMUNOGLOBULIN M; ISOPROTEIN; LIPOPOLYSACCHARIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR PAX5A; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; HUMORAL IMMUNITY; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL;

ANIMALS; ANTIBODY FORMATION; B-CELL-SPECIFIC ACTIVATOR PROTEIN; B-LYMPHOCYTES; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL LINE, TUMOR; CLONING, MOLECULAR; DNA-BINDING PROTEINS; ENVIRONMENTAL POLLUTANTS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOGLOBULIN M; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED STRAINS; NUCLEAR PROTEINS; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN; TETRACHLORODIBENZODIOXIN;

EID: 47949125190     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.108.139857     Document Type: Article

References (44)

1. Bell DR and Poland A (2000) Binding of aryl hydrocarbon receptor (AhR) to AhR-interacting protein. The role of hsp90. J Biol Chem 275:36407-36414.
2. + B cells by clonal T cells and antigen. Proc Natl Acad Sci U S A 83:7410-7414.
3. Burbach KM, Poland A, and Bradfield CA (1992) Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor. Proc Natl Acad Sci U S A 89:8185-8189.
4. Calame KL, Lin KI, and Tunyaplin C (2003) Regulatory mechanisms that determine the development and function of plasma cells. Annu Rev Immunol 21:205-230.
5. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, and Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92-96.
6. Cozma D, Yu D, Hodawadekar S, Azvolinsky A, Grande S, Tobias JW, Metzgar MH, Paterson J, Erikson J, Marafioti T, et al. (2007) B cell activator PAX5 promotes lymphomagenesis through stimulation of B cell receptor signaling. J Clin Invest 117:2602-2610.
7. de Rie MA, Schumacher TN, van Schijndel GM, van Lier RA, and Miedema F (1989) Regulatory role of CD19 molecules in B-cell activation and differentiation. Cell Immunol 118:368-381.
8. Dellabona P, Latron F, Maffei A, Scarpellino L, and Accolla RS (1989) Transcriptional control of MHC class II gene expression during differentiation from B cells to plasma cells. J Immunol 142:2902-2910.
9. Engel LS, Laden F, Andersen A, Strickland PT, Blair A, Needham LL, Barr DB, Wolff MS, Helzlsouer K, Hunter DJ, et al. (2007) Polychlorinated biphenyl levels in peripheral blood and non-Hodgkin's lymphoma: a report from three cohorts. Cancer Res 67:5545-5552.
10. Floret N, Mauny F, Challier B, Arveux P, Cahn JY, and Viel JF (2003) Dioxin emissions from a solid waste incinerator and risk of non-Hodgkin lymphoma. Epidemiology 14:392-398.
11. Gaidano G, Pasqualucci L, Capello D, Berra E, Deambrogi C, Rossi D, Maria Larocca L, Gloghini A, Carbone A, and Dalla-Favera R (2003) Aberrant somatic hypermutation in multiple subtypes of AIDS-associated non-Hodgkin lymphoma. Blood 102:1833-1841.
12. Hankinson O (1995) The aryl hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol 35:307-340.
13. Hardell L, Lindstrom G, van Bavel B, Fredrikson M, and Liljegren G (1998) Some aspects of the etiology of non-Hodgkin's lymphoma. Environ Health Perspect 106 (Suppl 2):679-681.
14. Holsapple MP, Dooley RK, McNerney PJ, and McCay JA (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.
15. Horcher M, Souabni A, and Busslinger M (2001) Pax5/BSAP maintains the identity of B cells in late B lymphopoiesis. Immunity 14:779-790.
16. Kaminski NE and Stevens WD (1992) The role of metabolism in carbon tetrachloride-mediated immunosuppression. In vitro studies. Toxicology 75:175-188.
17. Kerkvliet NI, Steppan LB, Brauner JA, Deyo JA, Henderson MC, Tomar RS, and Buhler DR (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.
18. Kozmik Z, Wang S, Dorfler P, Adams B, and Busslinger M (1992) The promoter of the CD19 gene is a target for the B-cell-specific transcription factor BSAP. Mol Cell Biol 12:2662-2672.
19. Krenacs L, Himmelmann AW, Quintanilla-Martinez L, Fest T, Riva A, Wellmann A, Bagdi E, Kehrl JH, Jaffe ES, and Raffeld M (1998) Transcription factor B-cell-specific activator protein (BSAP) is differentially expressed in B cells and in subsets of B-cell lymphomas. Blood 92:1308-1316.
20. Lee M, Yang KH, and Kaminski NE (1995) Effects of putative cannabinoid receptor ligands, anandamide and 2-arachidonyl-glycerol, on immune function in B6C3F1 mouse splenocytes. J Pharmacol Exp Ther 275:529-536.
21. Lin KI, Angelin-Duclos C, Kuo TC, 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.
22. Lowen M, Scott G, and Zwollo P (2001) Functional analyses of two alternative isoforms of the transcription factor Pax-5. J Biol Chem 276:42565-42574.
23. Luster MI, Germolec DR, Clark G, Wiegand G, and Rosenthal GJ (1988) Selective effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and corticosteroid on in vitro lymphocyte maturation. J Immunol 140:928-935.
24. Nera KP, Kohonen P, Narvi E, Peippo A, Mustonen L, Terho P, Koskela K, Buerstedde JM, and Lassila O (2006) Loss of Pax5 promotes plasma cell differentiation. Immunity 24:283-293.
25. Neurath MF, 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.
26. Petrulis JR and Perdew GH (2002) The role of chaperone proteins in the aryl hydrocarbon receptor core complex. Chem Biol Interact 141:25-40.
27. Reimold AM, Iwakoshi NN, Manis J, Vallabhajosyula P, Szomolanyi-Tsuda E, Gravallese EM, Friend D, Grusby MJ, Alt F, and Glimcher LH (2001) Plasma cell differentiation requires the transcription factor XBP-1. Nature 412:300-307.
28. Reimold AM, Ponath PD, Li YS, Hardy RR, David CS, Strominger JL, and Glimcher LH (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.
29. Rinkenberger JL, Wallin JJ, Johnson KW, and Koshland ME (1996) An interleukin-2 signal relieves BSAP (Pax5)-mediated repression of the immunoglobulin J chain gene. Immunity 5:377-386.
30. Rothman N, Cantor KP, Blair A, Bush D, Brock JW, Helzlsouer K, Zahm SH, Needham LL, Pearson GR, Hoover RN, et al. (1997) A nested case-control study of non-Hodgkin lymphoma and serum organochlorine residues. Lancet 350:240-244.
31. Rowlands JC and Gustafsson JA (1997) Aryl hydrocarbon receptor-mediated signal transduction. Crit Rev Toxicol 27:109-134.
32. Sato H, Saito-Ohara F, Inazawa J, and Kudo A (2004) Pax-5 is essential for kappa sterile transcription during Ig kappa chain gene rearrangement. J Immunol 172: 4858-4865.
33. Sato H, Wang D, and Kudo A (2001) Dissociation of Pax-5 from KI and KII sites during kappa-chain gene rearrangement correlates with its association with the underphosphorylated form of retinoblastoma. J Immunol 166:6704-6710.
34. Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, Lee AH, Qian SB, Zhao H, Yu X, Yang L, Tan BK, Rosenwald A, et al. (2004) XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21:81-93.
35. Singh M and Birshtein BK (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.
36. Sulentic CE, Holsapple MP, and Kaminski NE (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.
37. Sulentic CE, Holsapple MP, and Kaminski NE (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.
38. Vecchi A, Sironi M, Canegrati MA, Recchia M, and Garattini S (1983) Immunosuppressive effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin in strains of mice with different susceptibility to induction of aryl hydrocarbon hydroxylase. Toxicol Appl Pharmacol 68:434-441.
39. Viel JF, Arveux P, Baverel J, and Cahn JY (2000) Soft-tissue sarcoma and non-Hodgkin's lymphoma clusters around a municipal solid waste incinerator with high dioxin emission levels. Am J Epidemiol 152:13-19.
40. Weaver D and Baltimore D (1987) B lymphocyte-specific protein binding near an immunoglobulin kappa-chain gene J segment. Proc Natl Acad Sci U S A 84:1516-1520.
41. Whitelaw ML, McGuire J, Picard D, Gustafsson JA, and Poellinger L (1995) Heat shock protein hsp90 regulates dioxin receptor function in vivo. Proc Natl Acad Sci U S A 92:4437-4441.
42. Yoo BS, Boverhof DR, Shnaider D, Crawford RB, Zacharewski TR, and Kaminski NE (2004) 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) alters the regulation of Pax5 in lipopolysaccharide-activated B cells. Toxicol Sci 77:272-279.
43. Yu D, Allman D, Goldschmidt MH, Atchison ML, Monroe JG, and Thomas-Tikhonenko A (2003) Oscillation between B-lymphoid and myeloid lineages in Myc-induced hematopoietic tumors following spontaneous silencing/reactivation of the EBF/Pax5 pathway. Blood 101:1950-1955.
44. Zwollo P, Arrieta H, Ede K, Molinder K, Desiderio S, and Pollock R (1997) The Pax-5 gene is alternatively spliced during B-cell development. J Biol Chem 272:10160-10168.