Neonatal exposure to low-dose 2,3,7,8-tetrachlorodibenzo-p-dioxin causes autoimmunity due to the disruption of T cell tolerance

Journal of Immunology

Volumn 182, Issue 10, 2009, Pages 6576-6586

  Ishimaru, Naozumi ^a   Takagi, Atsuya ^b   Kohashi, Masayuki ^a   Yamada, Akiko ^a   Arakaki, Rieko ^a   Kanno, Jun ^b   Hayashi, Yoshio ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; AUTOANTIBODY; GAMMA INTERFERON; INTERLEUKIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CELL DISRUPTION; CYTOKINE PRODUCTION; EXPOSURE; FEMALE; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SJOEGREN SYNDROME; T LYMPHOCYTE; THYMUS FUNCTION; TISSUE DIFFERENTIATION;

ANIMALS; ANIMALS, NEWBORN; AUTOANTIGENS; AUTOIMMUNITY; CELL PROLIFERATION; CYTOKINES; DISEASE MODELS, ANIMAL; ENVIRONMENTAL POLLUTANTS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNE TOLERANCE; MICE; MICE, MUTANT STRAINS; MICROSCOPY, CONFOCAL; RECEPTORS, ARYL HYDROCARBON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SJOGREN'S SYNDROME; T-LYMPHOCYTES; TETRACHLORODIBENZODIOXIN; THYMUS GLAND;

EID: 77649190726     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0802289     Document Type: Article

References (61)

1. Kerkvliet, N. I. 2001. Recent advances in understanding the mechanisms of TCDD immunotoxicity. Int. Immunopharmacol. 2: 277-291.
2. Wormley, D. D., A. Ramesh, and D. B. Hood. 2004. Environmental contaminantmixture effects on CNS development, plasticity, and behavior. Toxicol. Appl. Pharmacol. 197: 49-65.
3. Schecter, A., L. Birnbaum, J. J. Ryan, and J. D. Constable. 2006. Dioxins: an overview. Environ. Res. 101: 419-428.
4. Laiosa, M. D., A. Wyman, F. G. Murante, N. C. Fiore, J. E. Staples, T. A. Gasiewicz, and A. E. Silverstone. 2003. Cell proliferation arrest within intrathymic lymphocyte progenitor cells causes thymic atrophy mediated by the aryl hydrocarbon receptor. J. Immunol. 171: 4582-4591.
5. Gehrs, B. C., and R. J. Smialowicz. 1999. Persistent suppression of delayed-type hypersensitivity in adult F344 rats after perinatal exposure to 2,3,7,8-tetrachlo-rodibenzo-p-dioxin. Toxicology 134: 79-88.
6. Walker, D. B., W. C. Williams, C. B. Copeland, and R. J. Smialowicz. 2004. Persistent suppression of contact hypersensitivity, and altered T-cell parameters in F344 rats exposed perinatally to 2,3,7,8-tetrachlorodibenzo-p- dioxin (TCDD). Toxicology 197: 57-66.
7. Prell, R. A., E. Dearstyne, L. G. Steppan, A. T. Vella, and N. I. Kerkvliet. 2000. CTL hyporesponsiveness induced by 2,3,7,8-tetrachlorodibenzo-p- dioxin: role of cytokines and apoptosis. Toxicol. Appl. Pharmacol. 166: 214-221.
8. Prell, R. A., J. A. Oughton, and N. I. Kerkvliet. 1995. Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on anti-CD3-induced changes in T-cell subsets and cytokine production. Int. J. Immunopharmacol. 17: 951-961.
9. Shepherd, D. M., E. A. Dearstyne, and N. I. Kerkvliet. 2000. The effects of TCDD on the activation of ovalbumin (OVA)-specific DO11.10 transgenic CD4(+) T cells in adoptively transferred mice. Toxicol. Sci. 56: 340-350.
10. Morris, D. L., J. G. Karras, and M. P. Holsapple. 1993. Direct effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on responses to lipopolysaccharide (LPS) by isolated murine B-cells. Immunopharmacology 26: 105-112.
11. Karras, J. G., and M. P. Holsapple. 1994. Inhibition of calcium-dependent B cell activation by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 125: 264-270. (Pubitemid 24142301)
12. Dooley, R. K., D. L. Morris, and M. P. Holsapple. 1990. Elucidation of cellular targets responsible for tetrachlorodibenzo-p-dioxin (TCDD)-induced suppression of antibody responses. II. The role of the T-lymphocyte. Immunopharmacology 19: 47-58.
13. Gotter, J., and B. Kyewski. 2004. Regulating self-tolerance by deregulating gene expression. Curr. Opin. Immunol. 16: 741-745. (Pubitemid 39423663)
14. Anderton, S., C. Burkhart, B. Metzler, and D. Wraith. 1999. Mechanisms of central and peripheral T-cell tolerance: lessons from experimental models of multiple sclerosis. Immunol. Rev. 169: 123-127. (Pubitemid 29338728)
15. Miller, J. F., and R. A. Flavell. 1994. T-cell tolerance and autoimmunity in transgenic models of central and peripheral tolerance. Curr. Opin. Immunol. 6: 892-899.
16. Kruize, A. A., R. J. Sweenk, and L. Kater. 1995. Diagnostic criteria and immunopathogenesis of Sjögren's syndrome: implications for therapy. Immunol. Today 16: 557-559.
17. Fox, R. I., M. Stern, and P. Michelson. 2000. Update in Sjögren syndrome. Curr. Opin. Rheumatol. 12: 391-398.
18. Fox, R. I. 2005. Sjögren's syndrome. Lancet 366: 321-331.
19. Haneji, N., H. Hamano, K. Yanagi, and Y. Hayashi. 1994. A new animal model for primary Sjögren's syndrome in NFS/sld mutant mice. J. Immunol. 153: 2769-2777. (Pubitemid 24278146)
20. Haneji, N., T. Nakamura, K. Takio, K. Yanagi, H. Higashiyama, I. Saito, S. Noji, H. Sugino, and Y. Hayashi. 1997. Identification of α-fodrin as a candidate autoantigen in primary Sjögren's syndrome. Science 275: 604-607. (Pubitemid 27193686)
21. Saegusa, K., N. Ishimaru, K. Yanagi, K. Mishima, R. Arakaki, T. Suda, I. Saito, and Y. Hayashi. 2002. Prevention and induction of autoimmune exocrinopathy is dependent on pathogenic autoantigen cleavage in murine Sjögren's syndrome. J. Immunol. 169: 1050-1057. (Pubitemid 34753465)
22. Suri-Payer, E., K. Wei, and K. Tung. 2001. The day-3 thymectomy model for induction of multiple organ-specific autoimmune diseases. Curr. Protoc. Immunol. 15: 15-16.
23. Kojima, A., Y. Tanaka-Kojima, T. Sakakura, and Y. Nishizuka. 1976. Spontaneous development of autoimmune thyroiditis in neonatally thymectomized mice. Lab. Invest. 34: 550-557.
24. Teague, P. O., E. J. Yunis, G. Rodey, A. J. Fish, O. Stutman, and R. A. Good. 1970. Autoimmune phenomena and renal disease in mice: role of thymectomy, aging, and involution of immunologic capacity. Lab. Invest. 22: 121-130.
25. Tung, K. S., S. Smith, P. Matzner, K. Kasai, J. Oliver, F. Feuchter, and R. E. Anderson. 1987. Murine autoimmune oophoritis, epididymoorchitis, and gastritis induced by day 3 thymectomy. Am. J. Pathol. 126: 303-314. (Pubitemid 17033855)
26. Safe, S. 2001. Molecular biology of the Ah receptor and its role in carcinogenesis. Toxicol. Lett. 120: 1-7. (Pubitemid 32375066)
27. Denison, M. S., and S. Heath-Pagliuso. 1998. The Ah receptor: a regulator of the biochemical and toxicological actions of structurally diverse chemicals. Bull. Environ. Contam. Toxicol. 61: 557-568.
28. Marlowe, J. L., and A. Puga. 2005. Aryl hydrocarbon receptor, cell cycle regulation, toxicity, and tumorigenesis. J. Cell. Biochem. 96: 1174-1184. (Pubitemid 41681860)
29. Nohara, K., H. Fujimaki, S. Tsukumo, K. Inouye, H. Sone, and C. Tohyama. 2002. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on T cell-derived cytokine production in ovalbumin (OVA)-immunized C57Bl/6 mice. Toxicology 172: 49-58. (Pubitemid 34159010)
30. Neff-LaFord, H. D., B. A. Vorderstrasse, and B. P. Lawrence. 2003. Fewer CTL, not enhanced NK cells, are sufficient for viral clearance from the lungs of immunocompromised mice. Cell. Immunol. 226: 54-64.
31. Tomita, S., H. B. Jiang, T. Ueno, S. Takagi, K. Tohi, S. Maekawa, A. Miyatake, A. Furukawa, F. J. Gonzalez, J. Takeda, T. Ichikawa, and Y. Takahama. 2003. T cell-specific disruption of arylhydrocarbon receptor nuclear translocator (Arnt) gene causes resistance to 2,3,7,8-tetrachlorodibenzo-p- dioxin-induced thymic involution. J. Immunol. 171: 4113-4120. (Pubitemid 37238687)
32. Camacho, I. A., N. Singh, V. L. Hegde, M. Nagarkatti, and P. S. Nagarkatti. 2005. Treatment of mice with 2,3,7,8-tetrachlorodibenzo-p-dioxin leads to aryl hydrocarbon receptor-dependent nuclear translocation of NF-κB and expression of Fas ligand in thymic stromal cells and consequent apoptosis in T cells. J. Immunol. 175: 90-103.
33. White, S. C., and G. W. Casarett. 1974. Induction of experimental autoallergic sialadenitis. J. Immunol. 112: 178-185.
34. Kohashi, M., N. Ishimaru, R. Arakaki, and Y. Hayashi. 2008. Effective treatment with oral administration of rebamipide in a mouse model for Sjogren's syndrome. Arthritis Rheum. 58: 389-400. (Pubitemid 351294874)
35. Rengarajan, J., S. J. Szabo, and L. H. Glimcher. 2000. Treanscriptional regulation oh Th1/Th2 polarization. Immunol. Today 21: 479-783.
36. Riddick, D. S., Y. Huang, P. A. Harper, and A. B. Okey. 1994. 2,3,7,8-Tetrachlorodibenzo-p-dioxin versus 3-methylcholanthrene: comparative studies of Ah receptor binding, transformation, and induction of CYP1A1. J. Biol. Chem. 269: 12118-12128. (Pubitemid 24196710)
37. Singh, N. P., M. Nagarkatti, and P. S. Nagarkatti. 2007. Role of dioxin response element and nuclear factor-κB motifs in 2,3,7,8- tetrachlorodibenzo-p-dioxin-mediated regulation of Fas and Fas ligand expression. Mol. Pharmacol. 71: 145-157.
38. Bonizzi, G., and M. Karin. 2004. The two NF-κB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25: 280-288. (Pubitemid 38610351)
39. Anderson, M. S., E. S. Venanzi, L. Klein, Z. Chen, S. P. Berzins, S. J. Turley, H. von Boehmer, R. Bronson, A. Dierich, C. Benoist, and D. Mathis. 2002. Protection of an immunological self shadow within the thymus by the aire protein. Science 298: 1395-1401.
40. Kuroda, N., T. Mitani, N. Takeda, N. Ishimaru, R. Arakaki, Y. Hayashi, Y. Bando, K. Izumi, T. Takahashi, T. Nomura, et al. 2005. Development of autoimmunity against transcriptionally unrepressed target antigen in the thymus of Aire-deficient mice. J. Immunol. 174: 1862-1870. (Pubitemid 40223925)
41. Ito, T., S. Tsukumo, N. Suzuki, H. Motohashi, M. Yamamoto, Y. Fujii-Kuriyama, J. Mimura, T. M. Lin, R. E. Peterson, C. Tohyama, and K. Nohara. 2004. A constitutively active arylhydrocarbon receptor induces growth inhibition of Jurkat T cells through changes in the expression of genes related to apoptosis and cell cycle arrest. J. Biol. Chem. 279: 25204-25210. (Pubitemid 38756771)
42. Nagarkatti, P. S., G. D. Sweeney, J. Gauldie, and D. A. Clark. 1984. Sensitivity to suppression of cytotoxic T cell generation by 2,3,7,8-tetrachlorodibenzo-pdioxin (TCDD) is dependent on the Ah genotype of the murine host. Toxicol. Appl. Pharmacol. 72: 169-176.
43. Nohara, K., X. Pan, S. Tsukumo, A. Hida, T. Ito, H. Nagai, K. Inouye, H. Motohashi, M. Yamamoto, Y. Fujii-Kuriyama, and C. Tohyama. 2005. Constitutively active aryl hydrocarbon receptor expressed specifically in T-lineage cells causes thymus involution and suppresses the immunization-induced increase in splenocytes. J. Immunol. 174: 2770-2777. (Pubitemid 40279693)
44. Staples, J. E., F. G. Murante, N. C. Fiore, T. A. Gasiewicz, and A. E. Silverstone. 1998. 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: 3844-3854.
45. Ishimaru, N., T. Yoneda, K. Saegusa, K. Yanagi, N. Haneji, K. Moriyama, I. Saito, and Y. Hayashi. 2000. Severe destructive autoimmune lesions with aging in murine Sjögren's syndrome through Fas-mediated apoptosis. Am. J. Pathol. 156: 1557-1564. (Pubitemid 30646695)
46. Kobayashi, M., N. Yasui, N. Ishimaru, R. Arakaki, and Y. Hayashi. 2004. Development of autoimmune arthritis with aging via bystander T cell activation in the mouse model of Sjögren's syndrome. Arthritis Rheum. 50: 3974-3984. (Pubitemid 39643946)
47. Kerkvliet, N. I., and J. A. Brauner. 1987. 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: 47-58.
48. Luster, M. I., D. R. Germolec, G. Clark, G. Wiegand, and G. J. Rosenthal. 1998. Selective effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and corticosteroid on in vitro lymphocyte maturation. J. Immunol. 140: 928-935.
49. Schmidt, J. V., G. H. 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: 6731-6736.
50. Gu, Y. Z., J. B. Hogenesch, and C. A. Bradfield. 2000. The PAS superfamily: sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40: 519-561.
51. Umannova, L., J. Zatloukalova, M. Machala, P. Krcmar, Z. Majkova, B. Hennig, A. Kozubik, and J. Vondracek. 2007. Tumor necrosis factor-α modulates effects of aryl hydrocarbon receptor ligands on cell proliferation and expression of cytochrome P450 enzymes in rat liver "stem-like" cells. Toxicol. Sci. 99: 79-89.
52. Hoagland, M. S., E. Hoagland, and H. I. Swanson. 2005. The p53 inhibitor pifithrin-α is a potent agonist of aryl hydrocarbon receptor. J. Pharmacol. Exp. Ther. 314: 603-610.
53. Vogel, C. F., E. Sciullo, W. Li, P. Wong, G. Lazennec, and F. Matsumura. 2007. RelB, a new partner of aryl hydrocarbon receptor-mediated transcription. Mol. Endocrinol. 21: 2941-2955. (Pubitemid 350223506)
54. Vogel, C. F., E. Sciullo, and F. Matsumura. 2007. Involvement of RelB in aryl hydrocarbon receptor-mediated induction of chemokines. Biochem. Biophys. Res. Commun. 363: 722-726.
55. Gillard, G. O., and A. G. Farr. 2005. Contrasting models of promiscuous gene expression by thymic epithelium. J. Exp. Med. 202: 15-19. (Pubitemid 41002906)
56. Mandal, P. K. 2005. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J. Comp. Physiol. 175: 221-230.
57. Fan, F., B. Yan, G. Wood, M. Viluksela, and K. K. Rozman. 1997. Cytokines (IL-1β and TNFα) in relation to biochemical and immunological effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in rats. Toxicology 116: 9-16. (Pubitemid 27051267)
58. Vogel, C., S. Donat, O. Döhr, L. Kremer, C. Esser, M. Roller, and J. Abel. 1997. Effect of subchronic 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on immune system and target gene responses in mice: calculation of benchmark doses for CYP1A1 and CYP1A2 related enzyme activities. Arch. Toxicol. 71: 372-382. (Pubitemid 27214470)
59. Warren, T. K., K. A. Mitchell, and B. P. Lawrence. 2000. Exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) suppresses the humoral and cell-mediated immune responses to influenza A virus without affecting cytolytic activity in the lung. Toxicol. Sci. 56: 114-123.
60. Veldhoen, M., K. Hirota, A. M. Westendorf, J. Buer, L. Dumoutier, J. C. Renauld, and B. Stockinger. 2008. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453: 106-110. (Pubitemid 351630329)
61. Quintana, F. J., A. S. Basso, A. H. Iglesias, T. Korn, M. F. Farez, E. Bettelli, M. Caccamo, M. Oukka, and H. L. Weiner. 2008. Control of Treg and TH17 cell differentiation by the aryl hydrocarbon receptor. Nature 453: 65-72.