The aryl hydrocarbon receptor has a role in the in vivo maturation of murine bone marrow B lymphocytes and their response to 2,3,7,8- tetrachlorodibenzo-p-dioxin

Toxicology and Applied Pharmacology

Volumn 165, Issue 3, 2000, Pages 227-236

  Thurmond, T Scott ^a   Staples, J Erin ^b   Silverstone, Allen E ^b   Gasiewicz, Thomas A ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

2,3,7,8 Tetrachlorodibenzo p dioxin; Aryl hydrocarbon receptor; B lymphopoiesis; Bone marrow; Chimeras

Indexed keywords

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

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; BONE MARROW; CELL MATURATION; CONTROLLED STUDY; IMMUNOTOXICITY; LYMPHOPOIESIS; MOUSE; NONHUMAN; RADIATION CHIMERA;

ANIMALIA; MURINAE;

EID: 0034659489     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1006/taap.2000.8942     Document Type: Article

References (73)

1. Abbott B. D., Birnbaum L. S., Perdew G. H. Developmental expression of two members of a new class of transcription factors: I. Expression of aryl hydrocarbon receptor in the C57BL/6N mouse embryo. Dev. Dyn. 204:1995;133-143.
2. Ackermann M. F., Gasiewicz T. A., Lamm K. R., Germolec D. R., Luster M. I. Selective inhibition of polymorphonuclear neutrophil activity by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 101:1989;470-480.
3. Barberis A., Widenhorn K., Vitelli L., Busslinger M. A novel B-cell lineage-specific transcription factor present at early but not late stages of differentiation. Genes Dev. 4:1990;849-859.
4. Blank J. A., Tucker A. N., Sweatlock J., Gasiewicz T. A., Luster M. I. Alpha-naphthoflavone antagonism of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced murine lymphocyte ethoxyresorufin-O-deethylase activity and immunosuppression. Mol. Pharmacol. 32:1987;169-172.
5. Crawford R. B., Holsapple M. P., Kaminski N. E. Leukocyte activation induces aryl hydrocarbon receptor up-regulation, DNA binding, and increased Cyp1a1 expression in the absence of exogenous ligand. Mol. Pharmacol. 52:1997;921-927.
6. Crews S. T. Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev. 12:1998;607-620.
7. Denison M. S., Fisher J. M., Whitlock J. P. Jr. The DNA recognition site for the dioxin-Ah receptor complex. Nucleotide sequence and functional analysis. J. Biol. Chem. 263:1988;17221-17224.
8. Dey A., Nebert D. W. Markedly increased constitutive CYP1A1 and mRNA levels in the fertilized ovum of the mouse. Biochem. Biophys. Res. Commun. 251:1998;657-661.
9. Dohr O., Abel J. Transforming growth factor-beta1 coregulates mRNA expression of aryl hydrocarbon receptor and cell-cycle-regulating genes in human cancer cell lines. Biochem. Biophys. Res. Commun. 241:1997;86-91.
10. Dohr O., Vogel C., Abel J. Modulation of growth factor expression by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Exp. Clin. Immunogenet. 11:1994;142-148.
11. Eltom S. E., Larsen M. C., Jefcoate C. R. Expression of CYP1B1 but not CYP1A1 by primary cultured human mammary stromal fibroblasts constitutively and in response to dioxin exposure: Role of the Ah receptor. Carcinogenesis. 19:1998;1437-1444.
12. Fernandez-Salguero P., Pineau T., Hilbert D. M., McPhail T., Lee S. S., Kimura S., Nebert D. W., Rudikoff S., Ward J. M., Gonzalez F. J. Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science. 268:1995;722-726.
13. Fine J. S., Silverstone A. E., Gasiewicz T. A. Impairment of prothymocyte activity of 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Immunol. 144:1990;1169-1176.
14. Frazier D. E. Jr., Silverstone A. E., Gasiewicz T. A. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced thymic atrophy and lymphocyte stem cell alterations by mechanisms independent of the estrogen receptor. Biochem. Pharmacol. 47:1994a;2039-2048.
15. Frazier D. E. Jr., Silverstone A. E., Soults J. A., Gasiewicz T. A. The thymus does not mediate 2,3,7,8-tetrachlorodibenzo-p-dioxin-elicited alterations in bone marrow lymphocyte stem cells. Toxicol. Appl. Pharmacol. 124:1994b;242-247.
16. Gasiewicz T. A. Dioxins and the Ah receptor: Probes to uncover processes in neuroendocrine development. Neurotoxicology. 18:1997;393-413.
17. Gasiewicz T. A., Rucci G. Cytosolic receptor for 2,3,7,8-tetrachlorodibenzo-p-dioxin. Evidence for a homologous nature among various mammalian species. Mol. Pharmacol. 26:1984;90-98.
18. Gengozian N., Urso I. R., Congdon C. C., Conger A. D., Makinodan T. Thymus specificity in lethally irradiated mice treated with rat bone marrow. Proc. Soc. Exp. Biol. Med. 96:1957.
19. Geraci J. L., Jackson K. L., Christensen G. M., Thrower P. D., Weyer B. J. Acute and late damage in the mouse small intestine following multiple fractionations of neutrons or x-rays. J. Radiol. Oncol. Biol. Phys. 2:1977.
20. Gonzalez F. J., Fernandez-Salguero P., Lee S. S. T., Pineau T., Ward J. M. Xenobiotic receptor knockout mice. Toxicol. Lett. 82/83:1995;117.
21. Grassman J. A., Masten S. A., Walker N. J., Lucier G. W. Animal models of human response to dioxins. Environ. Health Perspect. 106:1998;761-775.
22. Hahn M. E. The aryl hydrocarbon receptor: A comparative perspective. Comp. Biochem. Physiol. C Comp. Pharmacol. Toxicol. 121:1998;23-53.
23. Hardy R. R., Carmack C. E., Shinton S. A., Kemp J. D., Hayakawa K. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173:1991;1213-1225.
24. Harper N., Connor K., Steinberg M., Safe S. An enzyme-linked immunosorbent assay (ELISA) specific for antibodies to TNP-LPS detects alterations in serum immunoglobulins and isotype switching in C57BL/6 and DBA/2 mice exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds. Toxicology. 92:1994;155-167.
25. Hayashi S., Okabe-Kado J., Honma Y., Kawajiri K. Expression of Ah receptor (TCDD receptor) during human monocytic differentiation. Carcinogenesis. 16:1995;1403-1409.
26. Hempel J., Harper K., Lindahl R. Inducible (class 3) aldehyde dehydrogenase from rat hepatocellular carcinoma and 2,3,7,8-tetrachlorodibenzo-p-dioxin-treated liver: Distant relationship to the class 1 and 2 enzymes from mammalian liver cytosol/mitochondria. Biochemistry. 28:1989.
27. Israel D. I., Whitlock J. P. J. Regulation of cytochrome P1-450 gene transcription by 2,3,7,8-tetrachlorodibenzo-p-dioxin in wild type and variant mouse hepatoma cells. J. Biol. Chem. 259:1984.
28. Jain S., Maltepe E., Lu M. M., Simon C., 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.
29. Jandl R. C., Adirim T. A., Schur P. H. Stimulation of B cell differentiation by adherent mononuclear cells in systemic lupus erythematosus. Arthritis Rheum. 30:1987;761-768.
30. Kerkvliet N. I. Immunotoxicology of dioxins and related chemicals. Schecter E. Dioxins and Health. 1994;199-225 Plenum Press, New York.
31. Kerkvliet N. I., Brauner J. A. Mechanisms of 1,2,3,4,6,7,8-heptachlorodibenzo-p-dioxin (HpCDD)-induced humoral immune suppression: Evidence of primary defect in T-cell regulation. Toxicol. Appl. Pharmacol. 87:1987;18-31.
32. Knapp W., Baumgartner G. Monocyte-mediated suppression of human B lymphocyte differentiation in vitro. J. Immunol. 121:1978;1177-1183.
33. Kolluri S. K., Weiss C., Koff A., Gottlicher M. p27(Kip1) induction and inhibition of proliferation by the intracellular Ah receptor in developing thymus and hepatoma cells. Genes Dev. 13:1999;1742-1753.
34. Lai Z. W., Fiore N. C., Gasiewicz T. A., Silverstone A. E. 2,3,7,8-Tetrachlorodibenzo-p-dioxin and diethylstilbestrol affect thymocytes at different stages of development in fetal thymus organ culture. Toxicol. Appl. Pharmacol. 149:1998;167-177.
35. Lavin A. L., Hahn D. J., Gasiewicz T. A. Expression of functional aromatic hydrocarbon receptor and aromatic hydrocarbon nuclear translocator proteins in murine bone marrow stromal cells. Arch. Biochem. Biophys. 352:1998;9-18.
36. Li Y. S., Hayakawa K., Hardy R. R. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J. Exp. Med. 178:1993;951-960.
37. Luster M. I., Germolec D. R., Clark G., Wiegand G., Rosenthal G. J. Selective effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and corticosteroid on in vitro lymphocyte maturation. J. Immunol. 140:1988;928-935.
38. Ma Q., Whitlock J. P. Jr. The aromatic hydrocarbon receptor modulates the Hepa 1c1c7 cell cycle and differentiated state independently of dioxin. Mol. Cell. Biol. 16:1996;2144-2150.
39. Masten S. A., Shiverick K. T. The Ah receptor recognizes DNA binding sites for the B cell transcription factor, BSAP: A possible mechanism for dioxin-mediated alteration of CD19 gene expression in human B lymphocytes. Biochem. Biophys. Res. Commun. 212:1995;27-34.
40. Montazeri G., Chiorazzi N., Fu S. M., Kunkel H. G. Regulatory role of circulating monocytes in the differentiative and proliferative response of human B lymphocytes. Clin. Immunol. Immunopathol. 16:1980;1-10.
41. Morrison A. M., Nutt S. L., Thevenin C., Rolink A., Busslinger M. Loss- and gain-of-function mutations reveal an important role of BSAP (Pax-5) at the start and end of B cell differentiation. Semin. Immunol. 10:1998;133-142.
42. National Research Council Committee to Review the Outer Continental Shelf Environmental Studies Program Staff. The Guide for the Care and Use of Laboratory Animals. 1996;Academy Press, Washington.
43. Nebert D. W., Gonzalez F. J. P450 genes: Structure, evolution and regulation. Annu. Rev. Biochem. 56:1987.
44. Paulson K. E., Darnell J. Jr., Rushmore T., Pickett C. B. Analysis of the upstream elements of the xenobiotic compound-inducible and positionally regulated glutathione S-transferase Ya gene. Mol. Cell. Biol. 10:1990.
45. Peterson R. E., Theobald H. M., Kimmel G. L. Developmental and reproductive toxicity of dioxins and related compounds: Cross-species comparisons. Crit. Rev. Toxicol. 23:1993;283-335.
46. Phelan D., Winter G. M., Rogers W. J., Lam J. C., Denison M. S. Activation of the Ah receptor signal transduction pathway by bilirubin and biliverdin. Arch. Biochem. Biophys. 357:1998;155-163.
47. Poland A., Knutson J. C. 2,3,7,8-tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: Examination of the mechanism of toxicity. Annu. Rev. Pharmacol. Toxicol. 22:1982;517-554.
48. Rannug U., Rannug A., Sjoberg U., Li H., Westerholm R., Bergman J. Structure elucidation of two tryptophan-derived, high affinity Ah receptor ligands. Chem. Biol. 2:1995;841-845.
49. Reick M., Robertson R. W., Pasco D. S., Fagan J. B. Down-regulation of nuclear aryl hydrocarbon receptor DNA-binding and transactivation functions: Requirement for a labile or inducible factor. Mol. Cell. Biol. 14:1994;5653-5660.
50. Reiners J. J., Jones C. L., Hong N., Clift R. E., Elferink C. Downregulation of aryl hydrocarbon receptor function and cytochrome P450 1a1 induction by expression of Ha-Ras oncogenes. Mol. Carcinog. 19:1997;91-100.
51. Reyes H., Reiz-Porszasz S., Hankinson O. Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science. 256:1992.
52. Rushmore T. H., King R. G., Paulson K. E., Pickett C. B. Regulation of glutathione S-transferase Ya subunit gene expression: Identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc. Natl. Acad. Sci. USA. 87:1990.
53. Savas U., Bhattacharyya K. K., Christou M., Alexander D. L., Jefcoate C. R. Mouse cytochrome P-450EF, representative of a new 1B subfamily of cytochrome P-450s. Cloning, sequence determination, and tissue expression. J. Biol. Chem. 269:1994.
54. 4: A new class of ligand for the Ah receptor. Biochemistry. 38:1999;7594-7600.
55. Schmidt J. V., Bradfield C. A. Ah receptor signaling pathways. Annu. Rev. Cell Dev. Biol. 12:1996;55-89.
56. Schmidt J. V., Su G. H., Reddy J. K., Simon M. C., Bradfield C. A. Characterization of a murine Ahr null allele: Involvement of the Ah receptor in hepatic growth and development. Proc. Natl. Acad. Sci. USA. 93:1996;6731-6736.
57. Sewall C. H., Lucier G. W., Tritscher A. M., Clark G. C. TCDD-mediated changes in hepatic epidermal growth factor receptor may be a critical event in the hepatocarcinogenic action of TCDD. Carcinogenesis. 14:1993;1885-1893.
58. Shimba S., Todoroki K., Aoyagi T., Tezuka M. Depletion of arylhydrocarbon receptor during adipose differentiation in 3T3-L1 cells. Biochem. Biophys. Res. Commun. 249:1998;131-137.
59. Silverstone A. E., Frazier D. E. Jr., Fiore N. C., Soults J. A., Gasiewicz T. A. Dexamethasone, beta-estradiol, and 2,3,7,8-tetrachlorodibenzo-p-dioxin elicit thymic atrophy through different cellular targets. Toxicol. Appl. Pharmacol. 126:1994;248-259.
60. Sogawa K., Fujisawa-Sehara A., Yamane M., Fuji-Kuriyama Y. Location of regulatory elements responsible for drug induction in the rat cytochrome P-450c gene. Proc. Natl. Acad. Sci. USA. 83:1986.
61. Spangrude G. J. Assessment of lymphocyte development in radiation bone marrow chimeras. Coligan J. E., Kruisbeck A. M., Margulies D. H., Shevach E. M., Strober W. Current Protocols in Immunology. 1994;4.6.1 John Wiley and Sons, New York.
62. Spangrude G. J., Weissman L. L. Mature T cells generated from single thymic clones are phenotypically and functionally heterogenous. J. Immunol. 141:1988.
63. Staples J. E., Murante F. G., Fiore N. C., Gasiewicz T. A., Silverstone A. E. Thymic alterations induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin are strictly dependent on aryl hydrocarbon receptor activation in hemopoietic cells. J. Immunol. 160:1998;3844-3854.
64. Sulentic C. E. W., 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. 53:1998;623-629.
65. Sutter T. R., Tang Y. M., Hayes C. L., Wo Y. Y., Jabs E. W., Li X., Yin H., Cody C. W., Greenlee W. F. Complete cDNA sequence of a human dioxin-inducible mRNA identifies a new gene subfamily of cytochrome P450 that maps to chromosome 2. J. Biol. Chem. 269:1994.
66. Tucker A. N., Vore S. J., Luster M. I. Suppression of B cell differentiation by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Mol. Pharmacol. 29:1986;372-377.
67. Tukey R. H., Hannah R. R., Negishi M., Nebert D. W., Eisen H. J. The Ah locus: Correlation of intranuclear appearance of inducer-receptor complex with induction of cytochrome P-450 mRNA. Cell. 31:1982.
68. Tukey R. H., Nebert D. W. Regulation of mouse cytochrome P3-450 by the Ah receptor. Studies with a P3-450 cDNA clone. Biochemistry. 23:1984.
69. Vecchi A., Mantovani A., Sironi M., Luini W., Cairo M., Garattini S. Effect of acute exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin on humoral antibody production in mice. Chem.-Biol. Interact. 30:1980;337-342.
70. Weiss C., Kolluri S. K., Kiefer F., Gottlicher M. Complementation of Ah receptor deficiency in hepatoma cells: Negative feedback regulation and cell cycle control by the Ah receptor. Exp. Cell Res. 226:1996;154-163.
71. 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. 52:1996;771-780.
72. Yamaguchi K., Matulka R. A., Shneider A. M., Toselli P., Trombino A. F., Yang S., Hafer L. J., Mann K. K., Tao X., Tilly J. L., Near R. I., Sherr D. H. Induction of PreB cell apoptosis by 7,12-dimethlybenz[a]anthracene in long-term primary murine bone marrow cultures. Toxicol. Appl. Pharmacol. 147:1997a;190-203.
73. Yamaguchi K., Near R. I., Matulka R. A., Shneider A., Toselli P., Trombino A. F., Sherr D. H. Activation of the aryl hydrocarbon receptor/transcription factor and bone marrow stromal cell-dependent preB cell apoptosis. J. Immunol. 158:1997b;2165-2173.