Immunomodulation by subchronic low dose 2,3,7,8-tetrachlorodibenzo-p-dioxin in experimental autoimmune encephalomyelitis in the absence of pertussis toxin

Toxicological Sciences

Volumn 151, Issue 1, 2016, Pages 35-43

  Yang, Eun Ju ^a   Stokes, John V ^a   Kummari, Evangel ^a   Eells, Jeffrey ^a   Kaplan, Barbara L F ^a  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

EAE; IFN ; IL 17; Immunomodulation; TCDD; Tregs

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A1; FREUND ADJUVANT; GAMMA INTERFERON; INTERLEUKIN 17; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PERTUSSIS TOXIN; AHR PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; IFNG PROTEIN, MOUSE; IL17A PROTEIN, MOUSE; IMMUNOSUPPRESSIVE AGENT; MYELIN OLIGODENDROCYTE GLYCOPROTEIN (35-55); PEPTIDE FRAGMENT; POLYCHLORINATED DIBENZODIOXIN;

ADJUVANT THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEMYELINATION; DRUG WITHDRAWAL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOMODULATION; LIVER; LOW DRUG DOSE; MOUSE; MYELITIS; NONHUMAN; PATHOGENICITY; REGULATORY T LYMPHOCYTE; SPLEEN; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; AGONISTS; ANIMAL; C57BL MOUSE; CELL CULTURE; DOSE RESPONSE; DRUG EFFECTS; GENETICS; IMMUNOLOGY; METABOLISM; TIME FACTOR;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELLS, CULTURED; CYTOCHROME P-450 CYP1A1; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; IMMUNOSUPPRESSIVE AGENTS; INTERFERON-GAMMA; INTERLEUKIN-17; MICE, INBRED C57BL; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; POLYCHLORINATED DIBENZODIOXINS; RECEPTORS, ARYL HYDROCARBON; TH1 CELLS; TH17 CELLS; TIME FACTORS;

EID: 84978897536     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfw020     Document Type: Article

References (24)

1. Almeida, A. R., Zaragoza, B., and Freitas, A. A. (2006). Indexation as a novel mechanism of lymphocyte homeostasis: The number of CD4+CD25+ regulatory T cells is indexed to the number of IL-2-producing cells. J. Immunol. 177, 192-200.
2. Boule, L. A., Burke, C. G., Fenton, B. M., Thevenet-Morrison, K., Jusko, T. A., and Lawrence, B. P. (2015). Developmental activation of the AHR increases effector CD4+ T Cells and exacerbates symptoms in autoimmune disease-prone Gnaq +/- Mice. Toxicol. Sci. 148, 555-566.
3. Duarte, J. H., Di Meglio, P., Hirota, K., Ahlfors, H., and Stockinger, B. (2013). Differential influences of the aryl hydrocarbon receptor on Th17 mediated responses in vitro and in vivo. PLoS One 8, e79819.
4. Fletcher, J. M., Lalor, S. J., Sweeney, C. M., Tubridy, N., and Mills, K. H. (2010). T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin. Exp. Immunol. 162, 1-11.
5. Funatake, C. J., Marshall, N. B., Steppan, L. B., Mourich, D. V., and Kerkvliet, N. I. (2005). Cutting edge: Activation of the aryl hydrocarbon receptor by 2,3,7,8-tetrachlorodibenzo-p-dioxin generates a population of CD4+ CD25+ cells with characteristics of regulatory T cells. J. Immunol. 175, 4184-4188.
6. Hanieh, H., and Alzahrani, A. (2013). MicroRNA-132 suppresses autoimmune encephalomyelitis by inducing cholinergic anti-inflammation: A new Ahr-based exploration. Eur. J. Immunol. 43, 2771-2782.
7. Hofstetter, H. H., Grau, C., Buttmann, M., Forsthuber, T. G., Gaupp, S., Toyka, K. V., and Gold, R. (2007). The PLPp-specific T-cell population promoted by pertussis toxin is characterized by high frequencies of IL-17-producing cells. Cytokine 40, 35-43.
8. Hogaboam, J. P., Moore, A. J., and Lawrence, B. P. (2008). The aryl hydrocarbon receptor affects distinct tissue compartments during ontogeny of the immune system. Toxicol. Sci. 102, 160-170.
9. Koch, M. W., Metz, L. M., Agrawal, S. M., and Yong, V. W. (2013). Environmental factors and their regulation of immunity in multiple sclerosis. J. Neurol. Sci. 324, 10-16.
10. Lassmann, H. (2010). Axonal and neuronal pathology in multiple sclerosis: What have we learnt from animal models. Exp. Neurol. 225, 2-8.
11. Legroux, L., and Arbour, N. (2015). Multiple sclerosis and T lymphocytes: An entangled story. J. Neuroimmune Pharmacol. 10, 528-546.
12. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
13. Malek, T. R. (2008). The biology of interleukin-2. Annu. Rev. Immunol. 26, 453-479.
14. Naugler, W. E., and Karin, M. (2008). The wolf in sheep's clothing: The role of interleukin-6 in immunity, inflammation and cancer. Trends Mol. Med. 14, 109-119.
15. Quintana, F. J., Basso, A. S., Iglesias, A. H., Korn, T., Farez, M. F., Bettelli, E., Caccamo, M., Oukka, M., and Weiner, H. L. (2008). Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453, 65-71.
16. Quintana, F. J., Murugaiyan, G., Farez, M. F., Mitsdoerffer, M., Tukpah, A. M., Burns, E. J., and Weiner, H. L. (2010). An endogenous aryl hydrocarbon receptor ligand acts on dendritic cells and T cells to suppress experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U.S.A. 107, 20768-20773.
17. Rannug, A., Rannug, U., Rosenkranz, H. S., Winqvist, L., Westerholm, R., Agurell, E., and Grafstrom, A. K. (1987). Certain photooxidized derivatives of tryptophan bind with very high affinity to the Ah receptor and are likely to be endogenous signal substances. J. Biol. Chem. 262, 15422-15427.
18. Santostefano, M. J., Wang, X., Richardson, V. M., Ross, D. G., DeVito, M. J., and Birnbaum, L. S. (1998). A pharmacodynamic analysis of TCDD-induced cytochrome P450 gene expression in multiple tissues: Dose- and time-dependent effects. Toxicol. Appl. Pharmacol. 151, 294-310.
19. Setoguchi, R., Hori, S., Takahashi, T., and Sakaguchi, S. (2005). Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J. Exp. Med. 201, 723-735.
20. Thellin, O., Zorzi, W., Lakaye, B., De Borman, B., Coumans, B., Hennen, G., Grisar, T., Igout, A., and Heinen, E. (1999). Housekeeping genes as internal standards: Use and limits. J. Biotechnol. 75, 291-295.
21. Van den Berg, M., Birnbaum, L., Bosveld, A. T., Brunstrom, B., Cook, P., Feeley, M., Giesy, J. P., Hanberg, A., Hasegawa, R., Kennedy, S. W., et al. (1998). Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ. Health Perspect. 106, 775-792.
22. Veldhoen, M., Hirota, K., Westendorf, A. M., Buer, J., Dumoutier, L., Renauld, J. C., and Stockinger, B. (2008). The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453, 106-109.
23. Vorderstrasse, B. A., Cundiff, J. A., and Lawrence, B. P. (2004). Developmental exposure to the potent aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin impairs the cell-mediated immune response to infection with influenza a virus, but enhances elements of innate immunity. J. Immunotoxicol. 1, 103-112.
24. Wheeler, J. L., Martin, K. C., Resseguie, E., and Lawrence, B. P. (2014). Differential consequences of two distinct AhR ligands on innate and adaptive immune responses to influenza A virus. Toxicol. Sci. 137, 324-334.