Thymic alterations induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin are strictly dependent on aryl hydrocarbon receptor activation in hemopoietic cells

Journal of Immunology

Volumn 160, Issue 8, 1998, Pages 3844-3854

  Staples, J Erin ^a   Murante, Francis G ^b   Fiore, Nancy C ^a   Gasiewicz, Thomas A ^b   Silverstone, Allen E ^a  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; DNA BINDING PROTEIN; HELIX LOOP HELIX PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL POPULATION; CONTROLLED STUDY; HEMATOPOIETIC CELL; IMMUNE SYSTEM; IMMUNOMODULATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE; THYMUS ATROPHY;

ANIMALS; ANTIGENS, CD44; ATROPHY; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOCHROME P-450 CYP1A1; HEMATOPOIESIS; IMMUNOSUPPRESSIVE AGENTS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; RADIATION CHIMERA; RECEPTORS, ARYL HYDROCARBON; RECEPTORS, INTERLEUKIN-2; T-LYMPHOCYTE SUBSETS; TETRACHLORODIBENZODIOXIN; THYMUS GLAND;

EID: 0032522828     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (74)

1. Okey, A. B., D. S. Riddick, and P. A. Harper. 1994. Molecular biology of the aromatic hydrocarbon (dioxin) receptor. Trends Pharmacol Sci. 15:226.
2. Hogenesch, J. B., W. K. Chan, V. H. Jackiw, R. C. Brown, Y.-Z. Gu, M. Pray-Grant, G. H. Perdew, and C. A. Bradfield. 1997. Characterization of a subset of the basic-helix-loop-helix-PAS superfamily that interacts with components of the dioxin signaling pathway. J. Biol. Chem. 272:8581.
3. Schmidt, J. V., and C. A. Bradfield. 1996. Ah receptor signaling pathways. Annu. Rev. Cell Dev. Biol. 12:55.
4. Fernandez-Salguero, P., T. Pineau, D. M. Hilbert, T. McPhail, S. S. T. Lee, S. Kimura, D. W. Nebert, S. Rudikoff, J. M. Ward, and F. J. Gonzalez. 1995. Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268:722.
5. Gonzalez, F. J., P. Fernandez-Salguero, S. S. T. Lee, T. Pineau, and J. M. Ward. 1995. Xenobiotic receptor knockout mice. Toxicol. Lett. 82/83:117.
6. Brenner, D. A. 1996. New functions for the aryl hydrocarbon receptor. Hepatology 23:379.
7. Schmidt, J. V., G. H.-T. Su, J. K. Reddy, M. C. Simon, and C. A. Bradfield. 1996. Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc. Natl. Acad. Sci. USA 93:6731.
8. Kerkvielt, N. I. 1994. Immunotoxicology of dioxins and related chemicals. In Dioxins and Health. A. Schecter, ed. Plenum Press, New York, p. 199.
9. Holsapple, M. P., D. L. Morris, S. C. Wood, and N. K. Snyder. 1991. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced changes in immunocompetence: possible mechanisms. Annu. Rev. Pharmacol Toxicol. 31:73.
10. Carlstedt-Duke, J. M. B. 1979. Tissue distribution of the receptor for 2,3,7,8-tetrachlorodibenzo-p-dioxin in the rat. Cancer Res. 39:3172.
11. Li, W., S. Donat, O. Döhr, K. Unfried, and J. Abel. 1994. Ah receptor in different tissues of C57BL/6J and DBA/2J mice: use of competitive polymerase chain reaction to measure Ah-receptor mRNA expression. Arch. Biochem. Biophys. 315:279.
12. Carver, L. A., J. B. Hogenesch, and C. A. Bradfield. 1994. Tissue expression of the rat Ah-receptor and ARNT mRNAs. Nucleic Acids Res. 22:3038.
13. Gasiewicz, T. A., and G. Rucci. 1984. Cylosolic receptor for 2.3,7,8-tetrachlorobibenzo-p-dioxin: evidence for a homologous nature among various mammalian species. Mol. Pharmacol. 26:90.
14. Chen, H.-S., and G. Perdew. 1994. Subunit composition of the heteromeric cytosolic aryl hydrocarbon receptor complex. J. Biol. Chem. 269:27554.
15. Ma, Q., and J. P. Whitlock, Jr. 1997. A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Biol. Chem. 272:8878.
16. Rowlands, J. C., and J. Å. Gustafsson. 1997. Aryl hydrocarbon receptor-mediated signal transduction. Crit. Rev. Toxicol. 27:109.
17. Okey, A. B., D. S. Riddick, and P. A. Harper. 1994. The Ah receptor: mediator of the toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and related compounds. Toxicol. Lett. 70:1.
18. Hankinson, O. 1995. The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 35:307.
19. Lai, Z.-W., T. Pineau, and C. Esser. 1996. Identification of dioxin-responsive elements (DREs) in the 5′ regions of putative dioxin-inducible genes. Chem. Biol. Interact. 100:97.
20. Döhr, O., C. Vogel, and J. Abel. 1994. Modulation of growth factor expression by 2.3,7,8-tetrachlorodibenzo-p-dioxin. Exp. Clin. Immunogenet. 11:142.
21. Kerkvliet, N. I. 1995. Immunological effects of chlorinated dibenzo-p-dioxins. Environ. Health Perspect. 103(Suppl. 9):47.
22. Lundberg, K., K.-O. Grönvik, T. J. Goldschmidt, L. Klareskog, and L. Dencker. 1990. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) alters intrathymic T-cell development in mice. Chem. Biol. Interact. 74:179.
23. De Heer, C., E. J. De Waal, H. -J. Schuurman, J. G. Vos, and H. Van Loveren. 1994. The intrathymic target cell for the thymotoxic action of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Exp. Clin. Immunogenet. 11:86.
24. Kremer, J., E. Gleichmann, and C. Esser. 1994. Thymic stroma exposed to arylhydrocarbon receptor-binding xenobiotics fails to support proliferation of early thymocytes but induces differentiation. J. Immunol. 153:2778.
25. Greenlee, W. F., K. M. Dold, R. D. Irons, and R. Osborne. 1985. Evidence for direct action of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on thymic epithelium. Toxicol. Appl. Pharmacol. 79:112.
26. De Waal, E. J., H.-J. Schuurman, J. G. Loeber, H. Van Loveren, and J. G. Vos. 1992. Alterations in the cortical epithelium of rats after in vivo exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD): an (immuno)histological study. Toxicol. Appl. Pharmacol. 115:80.
27. 2+-mediated endonuclease activation. Science 242:256.
28. Kurl, R. N., M. Abraham, and M. J. Olnes. 1993. Early effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on rat thymocytes in vitro. Toxicology 77:103.
29. Rhile, M. J., M. Nagarkatti, and P. S. Nagarkatti. 1996. Role of Fas apoptosis and MHC genes in 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced immunotoxicity of T cells. Toxicology 110:153.
30. Kamath, A. B., H. Xu, P. S. Nagarkatti, and M. Nagarkatti. 1997. Evidence for the induction of apoptosis in thymocytes by 2,3,7,8-tetrachlorodibenzo-p-dioxin in vivo. Toxicol. Appl. Pharmacol. 142:367.
31. Fine, J. S., A. E. Silverstone, and T. A. Gasiewicz. 1990. Impairment of prothymocyte activity by 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Immunol 144:1169.
32. Kerkvliet, N. I., and J. A. Brauner. 1990. Flow cytometric analysis of lymphocyte subpopulations in the spleen and thymus of mice exposed to an acute immunosuppressive dose of 2,3.7,8-tetrachlorodibenzo-p-dioxin (TCDD). Environ. Res. 52:146.
33. Kremer, J., Z.-W. Lai, and C. Esser. 1995. Evidence for the promotion of positive selection of thymocytes by Ah receptor agonist 2,3,7,8-tetiachlorodibenzo-p-dioxin. Ear. J. Pharmacol. 293:413.
34. Boyd, R. L., C. L. Tucek, D. I. Godfrey, D. J. Izon, T. J. Wilson, N. J. Davidson, A. G. D. Bean, H. M. Ladyman, M. A. Ritter, and P. Hugo. 1993. The thymic microenvironment. Immunol. Today 14:445.
35. Murawska, M. B., A. M. Duijvestijn, F. A. Klatter, W. Ammerlaan, B. Meedendorp, and P. Nieuwenhuis. 1991. Differential kinetics of various subsets of thymic bone marrow-derived stromal cells in rat chimeras. Scand. J. Immunol. 33:473.
36. Lo, D., C. R. Reilly, L. C. Burkly, J. DeKoning, T. M. Laufer, and L. H. Glimcher. 1997. Thymic stromal cell specialization and the T-cell receptor repertoire Immunol. Res. 16:3.
37. DeKoning, J., L. DiMolfetto, C. Reilly, Q. Wei, W. L. Havran, and D. Lo. 1997. Thymic cortical epithelium is sufficient for the development of mature T cells in relB-deficient mice. J. Immunol. 158:2558.
38. Fort, M. M., and D. M. Pardoll. 1996. Can bone marrow-derived thymic stromal cells mediate the positive selection of class I-restricted T cells? Cell. Immunol. 171:74.
39. Duijvestijn, A. M., M. B. Murawska, B. Meedendorp, F. A. Klatter, J. Kampinga, and P. Nieuwenhuis. 1988. Kinetics of rat thymic dendritic cells in bone marrow-reconstituted radiation chimeras. Adv. Exp. Med. Biol. 237:277.
40. Screpanti, I., A. Modesti, and A. Gulino. 1993. Heterogeneity of thymic stromal cells and thymocytes differentiation: a cell culture approach. J. Cell Sci. 105:601.
41. Ardavin, C., L. Wu, and K. Shortman. 1993. Thymic dendritic cells and T cells develop simultaneously in the thymus from a common precursor population. Nature 362:761.
42. Wu, L., C.-L. Li, and K. Shortman. 1996. Thymic dendritic cells precursors: relationships to the T lymphocyte lineage and phenotype of the dendritic cell progeny. J. Exp. Med. 184:903.
43. Brocker, T., M. Riedinger, and K. Karjalainen. 1997. Targeted expression of major histocompatibility complex (MHC) class II molecules demonstrates that dendritic cells can induce negative but not positive selection of thymocytes in vivo. J. Exp. Med. 185:541.
44. Roberts, J. L., S. O. Sharrow, and A. Singer. 1990. Clonal deletion and clonal anergy in the thymus induced by cellular elements with different radiation sensitivities. J. Exp. Med. 171:935.
45. Fernandez-Salguero, P. M., D. M. Hilbert, S. Rudikoff, J. M. Ward, and F. J. Gonzalez. 1996. Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol. Appl. Pharmacol. 140:173.
46. National Research Council, Committee to Review the Outer Continental Shelf Environmental Studies Program Staff. 1996. The Guide for the Care and Use of Laboratory Animals. National Academy Press, Washington, D.C.
47. Geraci, J. P., K. L. Jackson, G. M. Christensen, P. D. Thrower, and B. J. Weyer. 1977. Acute and late damage in the mouse small intestine following multiple fractionations of neutrons or x-rays. J. Radiol. Oncol Biol. Physiol. 2:693.
48. Spangrude, G. J. 1994. Assessment of lymphocyte development in radiation bone marrow chimeras. In Current Protocols in Immunology. J. E. Coligan, A. M. Kruisbeck, D. H. Margulies, E. M. Shevach, and W. Strober, eds. John Wiley and Sons, Inc., New York, p. 4.6.1.
49. Gengozian, N., I. R. Urso, C. C. Congdon, A. D. Conger, and T. Makinodan. 1957. Thymus specificity in lethally irradiated mice treated with rat bone marrow. Proc. Soc. Exp. Biol. Med. 96:714.
50. Spangrude, G. J., and I. L. Weissman. 1988. Mature T cells generated from single thymic clones are phenotypically and functionally heterogenous. J. Immunol. 141:1877.
51. Dudov, K. P., and R. P. Perry. 1984. The gene family encoding the mouse ribosomal protein L32 contains a uniquely expressed intron-containing gene and an unmutated processed gene. Cell 37:457.
52. Shortman, K., and L. Wu. 1996. Early T lymphocyte progenitors. Annu. Rev. Immunol. 14:29.
53. Silverstone, A. E., D. E. Frazier, Jr., N. C. Fiore, J. A. Soults, and T. A. Gasiewicz. 1994. Dexamethasone, β-estradiol, and 2,3,7,8-tetrachlorodibenzo-p-dioxin elicit thymic atrophy through different cellular targets. Toxicol. Appl. Pharmacol. 126:248.
54. (low/-) hemopoietic stem cells. J. Immunol. 156:3207.
55. Yuan, I. L. 1996. Day 11 mouse fetal thymus: phenotype and search for the point of commitment. Differentiation 61:53.
56. Kawamoto, H., K. Ohmura, N. Hattori, and Y. Katsura. 1997. Hemopoietic progenitors in the murine fetal liver capable of rapidly generating T cells. J. Immunol. 158:3118.
57. Marcos, M. A., S. Morales-Alcelay, I. E. Godin, F. Dieterlen-Lievre, S. G. Copin, and M. L. Gaspar. 1997. Antigenic phenotype and gene expression pattern of lymphopoietic progenitors during early mouse ontogeny. J. Immunol. 158:2627.
58. Li, C. L., L. Wu, M. Antica, K. Shortman, and G. R. Johnson. 1995. Purified murine long-term in vivo hematopoietic repopulating cells are not prothymocytes Exp. Hematol. 23:21.
59. Spangrude, G. J., S. Heimfeld, and I. L. Weissman. 1988. Purification and characterization of mouse hemopoietic stem cells. Science 241:58.
60. Okada, S., H. Nakauchi, K. Nagayoshi, S. Nishikawa, Y. Miura, and T. Suda. 1992. In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells. Blood 80:3044.
61. Ikuta, K., and I. L. Weissman. 1992. Evidence that hemopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc. Natl. Acad. Sci. USA 89:1502.
62. Fine, J. S., T. A. Gasiewicz, and A. E. Silverstone. 1988. Lymphocyte stem cell alterations following perinatal exposure to 2,3.7,8-tetrachlorodibenzo-p-dioxon. Mol. Pharmacol. 35:18.
63. Funseth, E., and N. G. Ilback. 1992. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on blood and spleen natural killer (NK) cell activity in the mouse. Toxicol. Lett. 60:247.
64. Morrison, S. J., D. E. Wright, S. H. Cheshier, and I. L. Weissman. 1997. Hematopoietic stem cells: challenges to expectations. Curr. Opin. Immunol. 9:216.
65. Nishi, N., M. Osawa, R. Ishikawa, M. Nishikawa, H. Tsumura, H. Inoue, and T. Sudo. 1995. Hematopoietic stem cells found in lineage-positive subsets in the bone marrow of 5-fluorouracil-treated mice. Stem Cells 13:517.
66. Prell, R. A., J. A. Oughton, and N. I. Kerkvliet. 1995. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on anti-CD3-induced changes in T-cell subsets and cytokine production. Int. J. Immunopharmacol. 17:951.
67. Sprent, J., D. Lo, E.-K. Gao, and Y. Ron. 1988. T cell selection in the thymus. Immunol. Rev. 101:73.
68. + T cells in M1s-1a mice following exposure to a thymotoxic dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicology 103:195.
69. Silkworth, J. B., L. Antrim, and G. Sack. 1986. Ah receptor mediated suppression of the antibody response in mice is primarily dependent on the Ah phenotype of lymphoid tissue. Toxicol. Appl. Pharmacol. 86:380.
70. Morris, D. L., H. G. Jeong, W. D. Stevens, Y. J. Chun, J. G. Karras, and M. P. Holsapple. 1994. Serum modulation of the effects of TCDD on the in vitro antibody response and on enzyme induction in primary hepatocytes. Immunopharmacology 27:93.
71. Wilder, R. L. 1995. Neuroendocrine-immune system interactions and autoimmunity. Annu. Rev. Immunol. 13:307.
72. Kraal, G., L. Avis, J. Wijffels, K. Hoeben, and H. ter Hart. 1990. Different cpitopes on the dendritic cell-associated NLDC-45 molecule during ontogeny. Immunobiology 181:388.
73. Birnbaum, L. S. 1995. Developmental effects of dioxins. Environ. Health ferspect. 103(Suppl. 7):89.