Differential regulation of Th17 and T regulatory cell differentiation by aryl hydrocarbon receptor dependent xenobiotic response element dependent and independent pathways

Toxicological Sciences

Volumn 145, Issue 2, 2015, Pages 233-243

  Mohinta, Sonia ^a,d   Kannan, Arun K ^a,e   Gowda, Krishne ^b   Amin, Shantu G ^b   Perdew, Gary H ^c   August, Avery ^a  

^a Cornell University ^*  (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e BIOGEN   (United States)

Author keywords

AHR; SAhRMs; Th17; Treg

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A1; INTERLEUKIN 17; INTERLEUKIN 22; MESSENGER RNA; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; AHR PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; IL17A PROTEIN, MOUSE; LIGAND;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; BACTERIAL SHEDDING; CD4+ T LYMPHOCYTE; CITROBACTER RODENTIUM; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DISEASE SEVERITY; ENTEROBACTERIACEAE INFECTION; ENZYME INHIBITION; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOCYTOPOIESIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TH17 CELL; UPREGULATION; WEIGHT REDUCTION; XENOBIOTIC METABOLISM; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; DISEASE MODEL; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; TIME FACTOR;

CITROBACTER RODENTIUM;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELLS, CULTURED; CITROBACTER RODENTIUM; DISEASE MODELS, ANIMAL; ENTEROBACTERIACEAE INFECTIONS; GENE EXPRESSION REGULATION; INTERLEUKIN-17; LIGANDS; LYMPHOCYTE ACTIVATION; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ARYL HYDROCARBON; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TIME FACTORS;

EID: 84930701732     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv046     Document Type: Article

References (52)

1. Assi, K., Bergstrom, K., Vallance, B., Owen, D., Salh, B. (2013). Requirement of epithelial integrin-linked kinase for facilitation of Citrobacter rodentium-induced colitis. BMC Gastroenterol. 13, 137.
2. Baba, N., Rubio, M., Kenins, L., Regairaz, C., Woisetschlager, M., Carballido, J. M., and Sarfati, M. (2012). The aryl hydrocarbon receptor (AhR) ligand VAF347 selectively acts on monocytes and naive CD4(+) Th cells to promote the development of IL-22-secreting Th cells. Hum. Immunol. 73, 795-800.
3. Baban, B., Liu, J. Y., and Mozaffari, M. S. (2012). Aryl hydrocarbon receptor agonist, leflunomide, protects the ischemic-reperfused kidney: role of Tregs and stem cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303, R1136-R1146.
4. Basu, R., O'Quinn, D. B., Silberger, D. J., Schoeb, T. R., Fouser, L., Ouyang, W., Hatton, R. D., and Weaver, C. T. (2012). Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 37, 1061-1075.
5. Beischlag, T. V., Luis Morales, J., Hollingshead, B. D., and Perdew, G. H. (2008). The aryl hydrocarbon receptor complex and the control of gene expression. Crit. Rev. Eukaryot. Gene Expr. 18, 207-250.
6. Benson, J. M., and Shepherd, D. M. (2011). Aryl hydrocarbon receptor activation by TCDD reduces inflammation associated with Crohn's disease. Toxicol. Sci. 120, 68-78.
7. Carver, L. A., and Bradfield, C. A. (1997). Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. J. Biol. Chem. 272, 11452-11456.
8. Carver, L. A., Jackiw, V., and Bradfield, C. A. (1994). The 90-kDa heat shock protein is essential for Ah receptor signaling in a yeast expression system. J. Biol. Chem. 269, 30109-30112.
9. Cui, G., Qin, X., Wu, L., Zhang, Y., Sheng, X., Yu, Q., Sheng, H., Xi, B., Zhang, J. Z., and Zang, Y. Q. (2011). Liver X receptor (LXR) mediates negative regulation of mouse and human Th17 differentiation. J. Clin. Invest. 121, 658-670.
10. Deguchi, A., Tomita, T., Omori, T., Komatsu, A., Ohto, U., Takahashi, S., Tanimura, N., Akashi-Takamura, S., Miyake, K., and Maru, Y. (2013). Serum amyloid A3 binds MD-2 to activate p38 and NF-kappaB pathways in a MyD88-dependent manner. J. Immunol. 191, 1856-1864.
11. Denis, M., Cuthill, S., Wikstrom, A. C., Poellinger, L., and Gustafsson, J. A. (1988). Association of the dioxin receptor with the Mr 90,000 heat shock protein: a structural kinship with the glucocorticoid receptor. Biochem. Biophys. Res. Commun. 155, 801-807.
12. Fontenot, J. D., Rasmussen, J. P., Williams, L. M., Dooley, J. L., Farr, A. G., and Rudensky, A. Y. (2005). Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22, 329-341.
13. Gandhi, R., Kumar, D., Burns, E. J., Nadeau, M., Dake, B., Laroni, A., Kozoriz, D.,Weiner, H. L., and Quintana, F. J. (2010). Activation of the aryl hydrocarbon receptor induces human type 1 regulatory T cell-like and Foxp3(+) regulatory T cells. Nat. Immunol. 11, 846-853.
14. Hahn, M. E. (2002). Aryl hydrocarbon receptors: diversity and evolution. Chem. Biol. Interact. 141, 131-160.
15. Higgins, L. M., Frankel, G., Douce, G., Dougan, G., and MacDonald, T. T. (1999). Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect. Immun. 67, 3031-3039.
16. Honda, K. (2012). IL-22 from T cells: better late than never. Immunity 37, 952-954.
17. Ishigame, H., Kakuta, S., Nagai, T., Kadoki, M., Nambu, A., Komiyama, Y., Fujikado, N., Tanahashi, Y., Akitsu, A., Kotaki, H., et al. (2009). Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30, 108-119.
18. Jeong, K. T., Hwang, S. J., Oh, G. S., and Park, J. H. (2012). FICZ, a tryptophan photoproduct, suppresses pulmonary eosinophilia and Th2-type cytokine production in a mouse model of ovalbumin-induced allergic asthma. Int. Immunopharmacol. 13, 377-385.
19. Josefowicz, S. Z., Lu, L. F., and Rudensky, A. Y. (2012). Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30, 531-564.
20. Kannan, A. K., Sahu, N., Mohanan, S., Mohinta, S., and August, A. (2013). IL-2-inducible T-cell kinase modulates TH2-mediated allergic airway inflammation by suppressing IFN-gamma in naive CD4+ T cells. J. Allergy Clin. Immunol. 132, 811-20 e1-e5.
21. Kerkvliet, N. I. (2002). Recent advances in understanding the mechanisms of TCDD immunotoxicity. Int. Immunopharmacol. 2, 277-291.
22. Kim, E. Y., Suda, T., Tanabe, S., Batoev, V. B., Petrov, E. A., and Iwata, H. (2011). Evaluation of relative potencies for in vitro transactivation of the baikal seal aryl hydrocarbon receptor by dioxin-like compounds. Environ. Sci. Technol. 45, 1652-1658.
23. Kimura, A., Naka, T., Nohara, K., Fujii-Kuriyama, Y., and Kishimoto, T. (2008). Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc. Natl. Acad. Sci. USA. 105, 9721-9726.
24. Lahvis, G. P., Lindell, S. L., Thomas, R. S., McCuskey, R. S., Murphy, C., Glover, E., Bentz, M., Southard, J., and Bradfield, C. A. (2000). Portosystemic shunting and persistent fetal vascular structures in aryl hydrocarbon receptor-deficient mice. Proc. Natl. Acad. Sci. USA. 97, 10442-10447.
25. Lee, Y., Awasthi, A., Yosef, N., Quintana, F. J., Xiao, S., Peters, A., Wu, C., Kleinewietfeld, M., Kunder, S., Hafler, D. A., et al. (2012). Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 13, 991-999.
26. Mangan, P. R., Harrington, L. E., O'Quinn, D. B., Helms, W. S., Bullard, D. C., Elson, C. O., Hatton, R. D., Wahl, S. M., Schoeb, T. R., and Weaver, C. T. (2006). Transforming growth factorbeta induces development of the T(H)17 lineage. Nature 441, 231-234.
27. McInnes, I. B., Thompson, L., Giles, J. T., Bathon, J. M., Salmon, J. E., Beaulieu, A. D., Codding, C. E., Carlson, T. H., Delles, C., Lee, J. S., et al. (2015). Effect of interleukin-6 receptor blockade on surrogates of vascular risk in rheumatoid arthritis:MEASURE, a randomised, placebo-controlled study. Ann. Rheum. Dis. 74, 694-702.
28. Meyer, B. K., Pray-Grant, M. G., Vanden Heuvel, J. P., and Perdew, G. H. (1998). Hepatitis B virus X-associated protein 2 is a subunit of the unliganded aryl hydrocarbon receptor core complex and exhibits transcriptional enhancer activity. Mol. Cell. Biol. 18, 978-988.
29. Murray, I. A., Krishnegowda, G., DiNatale, B. C., Flaveny, C., Chiaro, C., Lin, J. M., Sharma, A. K., Amin, S., and Perdew, G. H. (2010). Development of a selective modulator of aryl hydrocarbon (Ah) receptor activity that exhibits anti-inflammatory properties. Chem. Res. Toxicol. 23, 955-966.
30. Nebert, D. W., and Karp, C. L. (2008). Endogenous functions of the aryl hydrocarbon receptor (AHR): intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. J. Biol. Chem. 283, 36061-36065.
31. Negishi, T., Kato, Y., Ooneda, O., Mimura, J., Takada, T., Mochizuki, H., Yamamoto, M., Fujii-Kuriyama, Y., and Furusako, S. (2005). Effects of aryl hydrocarbon receptor signaling on the modulation of TH1/TH2 balance. J. Immunol. 175, 7348-7356.
32. Patel, R. D., Hollingshead, B. D., Omiecinski, C. J., and Perdew, G. H. (2007). Aryl-hydrocarbon receptor activation regulates constitutive androstane receptor levels in murine and human liver. Hepatology 46, 209-218.
33. Patel, R. D., Murray, I. A., Flaveny, C. A., Kusnadi, A., and Perdew, G. H. (2009). Ah receptor represses acute-phase response gene expression without binding to its cognate response element. Lab. Invest. 89, 695-707.
34. Perdew, G. H. (1988). Association of the Ah receptor with the 90-kDa heat shock protein. J. Biol. Chem. 263, 13802-13805.
35. Pollenz, R. S., Sattler, C. A., and Poland, A. (1994). The aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator protein show distinct subcellular localizations in Hepa 1c1c7 cells by immunofluorescence microscopy. Mol. Pharmacol. 45, 428-438.
36. 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.
37. Quintana, F. J., Jin, H., Burns, E. J., Nadeau, M., Yeste, A., Kumar, D., Rangachari, M., Zhu, C., Xiao, S., Seavitt, J., et al. (2012). Aiolos promotes TH17 differentiation by directly silencing Il2 expression. Nat. Immunol. 13, 770-777.
38. 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. USA. 107, 20768-20773.
39. Reid-Yu, S. A., Small, C. L., and Coombes, B. K. (2013). CD3(-)NK1.1(+) cells aid in the early induction of a Th1 response to an attaching and effacing enteric pathogen. Eur. J. Immunol. 43, 2638-2649.
40. Reyes, H., Reisz-Porszasz, S., and Hankinson, O. (1992). Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science 256, 1193-1195.
41. Rohlman, D., Punj, S., Pennington, J., Bradford, S., and Kerkvliet, N. I. (2013). Suppression of acute graft-versus-host response by TCDD is independent of the CTLA-4-IFN-gamma-IDO pathway. Toxicol. Sci. 135, 81-90.
42. Schecter, A., Birnbaum, L., Ryan, J. J., and Constable, J. D. (2006). Dioxins: an overview. Environ. Res. 101, 419-428.
43. Schmidt, J. V., Su, G. H., Reddy, J. K., Simon, M. C., and Bradfield, C. A. (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.
44. Smith, K. J., Murray, I. A., Tanos, R., Tellew, J., Boitano, A. E., Bisson, W. H., Kolluri, S. K., Cooke, M. P., and Perdew, G. H. (2011). Identification of a high-affinity ligand that exhibits complete aryl hydrocarbon receptor antagonism. J. Pharmacol. Exp. Ther. 338, 318-327.
45. Stevens, E. A., and Bradfield, C. A. (2008). Immunology: T cells hang in the balance. Nature 453, 46-47.
46. Stockinger, B., Di Meglio, P., Gialitakis, M., and Duarte, J. H. (2014). The aryl hydrocarbon receptor: multitasking in the immune system. Annu. Rev. Immunol. 32, 403-432.
47. Stockinger, B., Veldhoen, M., and Martin, B. (2007). Th17 T cells:linking innate and adaptive immunity. Semin. Immunol. 19, 353-361.
48. Veldhoen, M., Hirota, K., Christensen, J., O'Garra, A., and Stockinger, B. (2009). Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of Th17 T cells. J. Exp. Med. 206, 43-49.
49. 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.
50. Wang, C., Xu, C. X., Bu, Y., Bottum, K. M., and Tischkau, S. A. (2014). Beta-naphthoflavone (DB06732) mediates estrogen receptor-positive breast cancer cell cycle arrest through AhR-dependent regulation of PI3K/AKT and MAPK/ERK signaling. Carcinogenesis 35, 703-713.
51. Wei, Y. D., Bergander, L., Rannug, U., and Rannug, A. (2000). Regulation of CYP1A1 transcription via the metabolism of the tryptophan-derived 6-formylindolo[3,2-b]carbazole. Arch. Biochem. Biophys. 383, 99-107.
52. Ziegler, S. F. (2006). FOXP3: of mice and men. Annu. Rev. Immunol. 24, 209-226.