Differential influences of the aryl hydrocarbon receptor on Th17 mediated responses in vitro and in vivo

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Duarte, João H ^a   Di Meglio, Paola ^a   Hirota, Keiji ^a,b   Ahlfors, Helena ^a   Stockinger, Brigitta ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARBAZOLES; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENVIRONMENTAL POLLUTANTS; GENE EXPRESSION REGULATION; IMMUNITY, CELLULAR; IMMUNOLOGIC FACTORS; INTERLEUKIN-17; INTERLEUKINS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; RECEPTORS, ARYL HYDROCARBON; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TETRACHLORODIBENZODIOXIN; TH17 CELLS;

EID: 84893938271     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079819     Document Type: Article

References (51)

1. Ivanov, II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, et al. (2006) The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133. (Pubitemid 44380299)
2. Yang XO, Pappu BP, Nurieva R, Akimzhanov A, Kang HS, et al. (2008) T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 28: 29-39.
3. Peck A, Mellins ED (2010) Precarious balance: Th17 cells in host defense. Infect Immun 78: 32-38.
4. Di Cesare A, Di Meglio P, Nestle FO (2009) The IL-23/Th17 axis in the immunopathogenesis of psoriasis. J Invest Dermatol 129: 1339-1350.
5. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, et al. (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103: 1345-1352. (Pubitemid 29218305)
6. Christensen JR, Bornsen L, Ratzer R, Piehl F, Khademi M, et al. (2013) Systemic inflammation in progressive multiple sclerosis involves follicular T-helper, Th17- and activated B-cells and correlates with progression. PLoS One 8: e57820.
7. Tzartos JS, Friese MA, Craner MJ, Palace J, Newcombe J, et al. (2008) Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 172: 146-155. (Pubitemid 351186376)
8. Schmidt JV, Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Dev Biol 12: 55-89. (Pubitemid 26422709)
9. Quintana FJ, Basso AS, Iglesias AH, Korn T, Farez MF, et al. (2008) Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453: 65-71. (Pubitemid 351630328)
10. Veldhoen M, Hirota K, Westendorf AM, Buer J, Dumoutier L, et al. (2008) The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453: 106-109. (Pubitemid 351630329)
11. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, et al. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201: 233-240. (Pubitemid 40189432)
12. Rannug A, Rannug U, Rosenkranz HS, Winqvist L, Westerholm R, et al. (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.
13. Zhang L, Ma J, Takeuchi M, Usui Y, Hattori T, et al. (2010) Suppression of experimental autoimmune uveoretinitis by inducing differentiation of regulatory T cells via activation of aryl hydrocarbon receptor. Invest Ophthalmol Vis Sci 51: 2109-2117.
14. Gandhi R, Kumar D, Burns EJ, Nadeau M, Dake B, et al. (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.
15. Apetoh L, Quintana FJ, Pot C, Joller N, Xiao S, et al. (2010) The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol 11: 854-861.
16. Nguyen NT, Kimura A, Nakahama T, Chinen I, Masuda K, et al. (2010) Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism. Proc Natl Acad Sci U S A 107: 19961-19966.
17. Quintana FJ, Murugaiyan G, Farez MF, Mitsdoerffer M, Tukpah AM, et al. (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.
18. Jin GB, Moore AJ, Head JL, Neumiller JJ, Lawrence BP (2010) Aryl hydrocarbon receptor activation reduces dendritic cell function during influenza virus infection. Toxicol Sci 116: 514-522.
19. Miniero R, De Felip E, Ferri F, di Domenico A (2001) An overview of TCDD half-life in mammals and its correlation to body weight. Chemosphere 43: 839-844. (Pubitemid 32405538)
20. Bergander L, Wincent E, Rannug A, Foroozesh M, Alworth W, et al. (2004) Metabolic fate of the Ah receptor ligand 6-formylindolo[3,2-b]carbazole. Chem Biol Interact 149: 151-164. (Pubitemid 39402931)
21. McCormack MP, Forster A, Drynan L, Pannell R, Rabbitts TH (2003) The LMO2 T-cell oncogene is activated via chromosomal translocations or retroviral insertion during gene therapy but has no mandatory role in normal T-cell development. Molecular and cellular biology 23: 9003-9013. (Pubitemid 37499791)
22. Caton ML, Smith-Raska MR, Reizis B (2007) Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. The Journal of experimental medicine 204: 1653-1664. (Pubitemid 47048031)
23. Schmidt JV, Su GH, Reddy JK, Simon MC, Bradfield CA (1996) Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci U S A 93: 6731-6736. (Pubitemid 26230378)
24. Wang Y, Kissenpfennig A, Mingueneau M, Richelme S, Perrin P, et al. (2008) Th2 lymphoproliferative disorder of LatY136F mutant mice unfolds independently of TCR-MHC engagement and is insensitive to the action of Foxp3+ regulatory T cells. J Immunol 180: 1565-1575.
25. Kerkvliet NI, Steppan LB, Vorachek W, Oda S, Farrer D, et al. (2009) Activation of aryl hydrocarbon receptor by TCDD prevents diabetes in NOD mice and increases Foxp3 + T cells in pancreatic lymph nodes. Immunotherapy 1: 539-547.
26. Veldhoen M, Hirota K, Christensen J, O'Garra A, 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.
27. Schiffenbauer J, Streit WJ, Butfiloski E, LaBow M, Edwards C, 3rd, et al. (2000) The induction of EAE is only partially dependent on TNF receptor signaling but requires the IL-1 type I receptor. Clinical immunology 95: 117-123. (Pubitemid 30317821)
28. Sutton C, Brereton C, Keogh B, Mills KH, Lavelle EC (2006) A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. The Journal of experimental medicine 203: 1685-1691. (Pubitemid 44036274)
29. Poland A, Palen D, Glover E (1994) Analysis of the four alleles of the murine aryl hydrocarbon receptor. Mol Pharmacol 46: 915-921. (Pubitemid 24364105)
30. Walisser JA, Glover E, Pande K, Liss AL, Bradfield CA (2005) Aryl hydrocarbon receptor-dependent liver development and hepatotoxicity are mediated by different cell types. Proceedings of the National Academy of Sciences of the United States of America 102: 17858-17863. (Pubitemid 41803587)
31. Kimura A, Naka T, Nohara K, Fujii-Kuriyama Y, Kishimoto T (2008) Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc Natl Acad Sci U S A 105: 9721-9726. (Pubitemid 352031367)
32. Esser C, Rannug A, Stockinger B (2009) The aryl hydrocarbon receptor in immunity. Trends Immunol 30: 447-454.
33. Nguyen LP, Bradfield CA (2008) The search for endogenous activators of the aryl hydrocarbon receptor. Chem Res Toxicol 21: 102-116. (Pubitemid 351219712)
34. Denison MS, Nagy SR (2003) Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 43: 309-334. (Pubitemid 37372644)
35. Veldhoen M, Brucklacher-Waldert V (2012) Dietary influences on intestinal immunity. Nature reviews Immunology 12: 696-708.
36. Connor KT, Aylward LL (2006) Human response to dioxin: aryl hydrocarbon receptor (AhR) molecular structure, function, and dose-response data for enzyme induction indicate an impaired human AhR. J Toxicol Environ Health B Crit Rev 9: 147-171.
37. Hirota K, Duarte JH, Veldhoen M, Hornsby E, Li Y, et al. (2011) Fate mapping of IL-17-producing T cells in inflammatory responses. Nature immunology 12: 255-263.
38. Stockinger B, Hirota K, Duarte J, Veldhoen M (2011) External influences on the immune system via activation of the aryl hydrocarbon receptor. Semin Immunol 23: 99-105.
39. Banz A, Pontoux C, Papiernik M (2002) Modulation of Fas-dependent apoptosis: a dynamic process controlling both the persistence and death of CD4 regulatory T cells and effector T cells. J Immunol 169: 750-757. (Pubitemid 34753430)
40. Singh N, Yamamoto M, Takami M, Seki Y, Takezaki M, et al. (2010) CD4(+)CD25(+) regulatory T cells resist a novel form of CD28- and Fas-dependent p53-induced T cell apoptosis. J Immunol 184: 94-104.
41. Belghith M, Bluestone JA, Barriot S, Megret J, Bach JF, et al. (2003) TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 9: 1202-1208. (Pubitemid 37173706)
42. Bourgeois C, Stockinger B (2006) T cell homeostasis in steady state and lymphopenic conditions. Immunol Lett 107: 89-92. (Pubitemid 44779812)
43. Chatenoud L (2005) CD3-specific antibodies restore self-tolerance: mechanisms and clinical applications. Curr Opin Immunol 17: 632-637.
44. Puga A, Xia Y, Elferink C (2002) Role of the aryl hydrocarbon receptor in cell cycle regulation. Chem Biol Interact 141: 117-130. (Pubitemid 35223208)
45. Funatake CJ, Ao K, Suzuki T, Murai H, Yamamoto M, et al. (2009) Expression of constitutively-active aryl hydrocarbon receptor in T-cells enhances the down-regulation of CD62L, but does not alter expression of CD25 or suppress the allogeneic CTL response. J Immunotoxicol 6: 194-203.
46. Mimura J, Ema M, Sogawa K, Fujii-Kuriyama Y (1999) Identification of a novel mechanism of regulation of Ah (dioxin) receptor function. Genes Dev 13: 20-25. (Pubitemid 29045112)
47. Davarinos NA, Pollenz RS (1999) Aryl hydrocarbon receptor imported into the nucleus following ligand binding is rapidly degraded via the cytosplasmic proteasome following nuclear export. J Biol Chem 274: 28708-28715.
48. Bock KW, Kohle C (2006) Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem Pharmacol 72: 393-404. (Pubitemid 44061741)
49. Mitchell KA, Elferink CJ (2009) Timing is everything: consequences of transient and sustained AhR activity. Biochem Pharmacol 77: 947-956.
50. Jux B, Kadow S, Esser C (2009) Langerhans cell maturation and contact hypersensitivity are impaired in aryl hydrocarbon receptor-null mice. J Immunol 182: 6709-6717.
51. Mezrich JD, Fechner JH, Zhang X, Johnson BP, Burlingham WJ, et al. (2010) An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J Immunol 185: 3190-3198.