Benzimidazoisoquinolines: A new class of rapidly metabolized Aryl hydrocarbon Receptor (AhR) ligands that induce AhR-dependent tregs and prevent murine graft-versus-host disease

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Punj, Sumit ^a   Kopparapu, Prasad ^a   Jang, Hyo Sang ^a   Phillips, Jessica L ^a   Pennington, Jamie ^a   Rohlman, Diana ^a   O'Donnell, Edmond ^a   Iversen, Patrick L ^a   Kolluri, Siva Kumar ^a   Kerkvliet, Nancy I ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

10 CHLORO 7H BENZIMIDAZO[2,1 A]BENZO[DE]ISO QUINOLIN 7 ONE; 2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INDUCIBLE T CELL COSTIMULATOR LIGAND; INTERLEUKIN 2 RECEPTOR ALPHA; ISOQUINOLINE DERIVATIVE; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; 10-CHLORO-7H-BENZIMIDAZO(2,1-A)BENZO(DE)ISOQUINOLIN-7-ONE; BENZIMIDAZOLE DERIVATIVE; LIGAND;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; DRUG BLOOD LEVEL; DRUG METABOLISM; GRAFT VERSUS HOST REACTION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; STRUCTURE ACTIVITY RELATION; ANIMAL; CHEMISTRY; DRUG EFFECTS; GRAFT VS HOST DISEASE; IMMUNOLOGY; IMMUNOTHERAPY; KINETICS; METABOLISM;

ANIMALS; BENZIMIDAZOLES; GRAFT VS HOST DISEASE; IMMUNOTHERAPY; ISOQUINOLINES; KINETICS; LIGANDS; MICE; RECEPTORS, ARYL HYDROCARBON; STRUCTURE-ACTIVITY RELATIONSHIP; T-LYMPHOCYTES, REGULATORY;

EID: 84896776715     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088726     Document Type: Article

References (43)

1. Kiss EA, Vonarbourg C, Kopfmann S, Hobeika E, Finke D, et al. (2011) Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science. 334: 1561-1565.
2. Qiu J, Heller JJ, Guo X, Chen ZM, Fish K, et al. (2012) The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36: 92-104.
3. 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.
4. Funatake CJ, Marshall NB, Steppan LB, Mourich DV, Kerkvliet NI (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. (Pubitemid 41361950)
5. 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)
6. Rodriguez-Sosa M, Elizondo G, Lopez-Duran RM, Rivera I, Gonzalez FJ, et al. (2005) Over-production of IFN-gamma and IL-12 in AhR-null mice. FEBS Lett 579: 6403-6410. (Pubitemid 41612159)
7. Elizondo G, Rodriguez-Sosa M, Estrada-Muniz E, Gonzalez FJ, Vega L (2011) Deletion of the aryl hydrocarbon receptor enhances the inflammatory response to Leishmania major infection. Int J Biol Sci 7: 1220-1229.
8. 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.
9. 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.
10. Kerkvliet NI (2012) TCDD: an environmental immunotoxicant reveals a novel pathway of immunoregulation-a 30-year odyssey. Toxicol Pathol 40: 138-142.
11. Kerkvliet NI, Shepherd DM, Baecher-Steppan L (2002) T lymphocytes are direct, aryl hydrocarbon receptor (AhR)-dependent targets of 2,3,7,8-tetrachlo-rodibenzo-p-dioxin (TCDD): AhR expression in both CD4+ and CD8+ T cells is necessary for full suppression of a cytotoxic T lymphocyte response by TCDD. Toxicol Appl Pharmacol 185: 146-152. (Pubitemid 36062805)
12. Funatake CJ, Marshall NB, Kerkvliet NI (2008) 2,3,7,8-Tetrachlorodibenzo- p-dioxin alters the differentiation of alloreactive CD8+ T cells toward a regulatory T cell phenotype by a mechanism that is dependent on aryl hydrocarbon receptor in CD4+ T cells. J Immunotoxicol 5: 81-91. (Pubitemid 351431256)
13. Marshall NB, Vorachek WR, Steppan LB, Mourich DV, Kerkvliet NI (2008) Functional characterization and gene expression analysis of CD4+ CD25+ regulatory T cells generated in mice treated with 2,3,7,8-tetrachlorodibenzo-p- dioxin. J Immunol 181: 2382-2391.
14. Kerkvliet NI, Baecher-Steppan L, Shepherd DM, Oughton JA, Vorderstrasse BA, et al. (1996) Inhibition of TC-1 cytokine production, effector cytotoxic T lymphocyte development and alloantibody production by 2,3,7,8-tetrachlorodi- benzo-p-dioxin. J Immunol 157: 2310-2319. (Pubitemid 126450440)
15. 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.
16. 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.
17. Koller A, Denhaerynck K, Moons P, Steiger J, Bock A, et al. (2010) Distress associated with adverse effects of immunosuppressive medication in kidney transplant recipients. Prog Transplant 20: 40-46.
18. Leslie M (2011) Immunology. Regulatory T cells get their chance to shine. Science 332: 1020-1021.
19. Marshall NB, Kerkvliet NI (2010) Dioxin and immune regulation: emerging role of aryl hydrocarbon receptor in the generation of regulatory T cells. Ann N Y Acad Sci 1183: 25-37.
20. O'Donnell EF, Saili KS, Koch DC, Kopparapu PR, Farrer D, et al. (2010) The anti-inflammatory drug leflunomide is an agonist of the aryl hydrocarbon receptor. PLoS One 5.
21. Gasiewicz TA, Neal RA (1982) The examination and quantitation of tissue cytosolic receptors for 2,3,7,8-tetrachlorodibenzo-p-dioxin using hydroxylapatite. Anal Biochem 124: 1-11. (Pubitemid 13250008)
22. O'Donnell EF, Kopparapu PR, Koch DC, Jang HS, Phillips JL, et al. (2012) The aryl hydrocarbon receptor mediates leflunomide-induced growth inhibition of melanoma cells. PLoS One 7: e40926.
23. Denison MS, Soshilov AA, He G, DeGroot DE, Zhao B (2011) Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol Sci 124: 1-22.
24. Zhang Y, Huo M, Zhou J, Xie S (2010) PKSolver: An add-in program for pharmacokinetic and pharmacodynamic data analysis in Microsoft Excel. Comput Methods Programs Biomed 99: 306-314.
25. Vocanson M, Rozieres A, Hennino A, Poyet G, Gaillard V, et al. (2010) Inducible costimulator (ICOS) is a marker for highly suppressive antigen-specific T cells sharing features of TH17/TH1 and regulatory T cells. J Allergy Clin Immunol 126: 280-289, 289 e281-287.
26. Tokumitsu H, Inuzuka H, Ishikawa Y, Ikeda M, Saji I, et al. (2002) STO-609, a specific inhibitor of the Ca(2+)/calmodulin-dependent protein kinase kinase. J Biol Chem 277: 15813-15818. (Pubitemid 34967859)
27. Schulz VJ, Smit JJ, Willemsen KJ, Fiechter D, Hassing I, et al. (2011) Activation of the aryl hydrocarbon receptor suppresses sensitization in a mouse peanut allergy model. Toxicol Sci 123: 491-500.
28. Huang Z, Jiang Y, Yang Y, Shao J, Sun X, et al. (2013) 3,39-Diindolylmethane alleviates oxazolone-induced colitis through Th2/Th17 suppression and Treg induction. Mol Immunol 53: 335-344.
29. Monteiro P, Gilot D, Langouet S, Fardel O (2008) Activation of the aryl hydrocarbon receptor by the calcium/calmodulin-dependent protein kinase kinase inhibitor 7-oxo-7H-benzimidazo[2,1-a]benz[de]isoquinoline-3-carboxylic acid (STO-609). Drug Metab Dispos 36: 2556-2563.
30. Monteiro P, Gilot D, Le Ferrec E, Rauch C, Lagadic-Gossmann D, et al. (2008) Dioxin-mediated up-regulation of aryl hydrocarbon receptor target genes is dependent on the calcium/calmodulin/CaMKIalpha pathway. Mol Pharmacol 73: 769-777. (Pubitemid 351397882)
31. Vaeth M, Schliesser U, Muller G, Reissig S, Satoh K, et al. (2012) Dependence on nuclear factor of activated T-cells (NFAT) levels discriminates conventional T cells from Foxp3+ regulatory T cells. Proc Natl Acad Sci U S A 109: 16258-16263.
32. Bisson WH, Koch DC, O'Donnell EF, Khalil SM, Kerkvliet NI, et al. (2009) Modeling of the aryl hydrocarbon receptor (AhR) ligand binding domain and its utility in virtual ligand screening to predict new AhR ligands. J Med Chem 52: 5635-5641.
33. Hu W, Zhao J, Pei G (2013) Activation of aryl hydrocarbon receptor by Tranilast, an anti-allergy drug,promotes miR-302 expression and cell reprogramming. J Biol Chem.
34. Kobayashi Y, Matsuura Y, Kotani E, Fukuda T, Aoyagi T, et al. (1993) Structural requirements for the induction of hepatic microsomal cytochrome P450 by imidazole- and pyridine-containing compounds in rats. J Biochem 114: 697-701. (Pubitemid 23339349)
35. Paghdal KV, Schwartz RA (2009) Topical tar: back to the future. J Am Acad Dermatol 61: 294-302.
36. van den Bogaard EH, Bergboer JG, Vonk-Bergers M, van Vlijmen-Willems IM, Hato SV, et al. (2013) Coal tar induces AHR-dependent skin barrier repair in atopic dermatitis. J Clin Invest 123: 917-927.
37. Smith G, Ibbotson SH, Comrie MM, Dawe RS, Bryden A, et al. (2006) Regulation of cutaneous drug-metabolizing enzymes and cytoprotective gene expression by topical drugs in human skin in vivo. Br J Dermatol 155: 275-281. (Pubitemid 44050559)
38. Roelofzen JH, van der Valk PG, Godschalk R, Dettbarn G, Seidel A, et al. (2012) DNA adducts in skin biopsies and 1-hydroxypyrene in urine of psoriasis patients and healthy volunteers following treatment with coal tar. Toxicol Lett 213: 39-44.
39. Roelofzen JH, Aben KK, Oldenhof UT, Coenraads PJ, Alkemade HA, et al. (2010) No increased risk of cancer after coal tar treatment in patients with psoriasis or eczema. J Invest Dermatol 130: 953-961.
40. Foreman MI, Taylor M, Clark C, Devitt H, Hanlon G, et al. (1985) Isoquinoline is a possible anti-psoriatic agent in coal tar. Br J Dermatol 112: 323-328. (Pubitemid 15127312)
41. Karaca F, Morgan TJ, George A, Bull ID, Herod AA, et al. (2009) Molecular mass ranges of coal tar pitch fractions by mass spectrometry and size-exclusion chromatography. Rapid Commun Mass Spectrom 23: 2087-2098.
42. Yeste A, Nadeau M, Burns EJ, Weiner HL, Quintana FJ (2012) Nanoparticle-mediated codelivery of myelin antigen and a tolerogenic small molecule suppresses experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 109: 11270-11275.
43. Hauben E, Gregori S, Draghici E, Migliavacca B, Olivieri S, et al. (2008) Activation of the aryl hydrocarbon receptor promotes allograft-specific tolerance through direct and dendritic cell-mediated effects on regulatory T cells. Blood 112: 1214-1222.