TLR7 stimulation of APCs results in inhibition of IL-5 through type i IFN and notch signaling pathways in human peripheral blood mononuclear cells

Journal of Immunology

Volumn 190, Issue 6, 2013, Pages 2585-2592

  Edwards, Susan ^a   Jones, Carolyn ^a,c   Leishman, Andrew J ^a   Young, Barbara W ^a   Matsui, Hiroyuki ^b   Tomizawa, Hideyuki ^b   Murray, Clare M ^a   Biffen, Mark ^a  

^a ASTRAZENECA   (United Kingdom)

^b Pharmacology Research Laboratory Dainippon Sumitomo Pharma   (Japan)

^c MRC TOXICOLOGY UNIT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; AZ 12441970; CD28 ANTIGEN; CD3 ANTIGEN; GAMMA SECRETASE INHIBITOR; INTERLEUKIN 13; INTERLEUKIN 5; MESSENGER RNA; NOTCH RECEPTOR; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ADULT; AGED; ANTIGEN PRESENTING CELL; ARTICLE; ASTHMA; B LYMPHOCYTE; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH2 CELL;

ANTIGEN-PRESENTING CELLS; CELLS, CULTURED; HUMANS; INTERFERON TYPE I; INTERLEUKIN-5; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 7;

EID: 84874916817     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200780     Document Type: Article

References (46)

1. Larché, M., D. S. Robinson, and A. B. Kay. 2003. The role of T lymphocytes in the pathogenesis of asthma. J. Allergy Clin. Immunol. 111: 450-463, quiz 464
2. Holgate, S. T. 2008. Pathogenesis of asthma. Clin. Exp. Allergy 38: 872-897
3. Pearce, N., N. Aït-Khaled, R. Beasley, J. Mallol, U. Keil, E. Mitchell, and C. Robertson. 2007. Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax 62: 758-766
4. Braun-Fahrländer, C., J. Riedler, U. Herz,W. Eder, M.Waser, L. Grize, S. Maisch, D. Carr, F. Gerlach, A. Bufe, et al. 2002. Environmental exposure to endotoxin and its relation to asthma in school-age children. N. Engl. J. Med. 347: 869-877
5. Gern, J. E. 2011. Barnyard microbes and childhood asthma. N. Engl. J. Med. 364: 769-770
6. Romagnani, S. 2004. The increased prevalence of allergy and the hygiene hypothesis: missing immune deviation, reduced immune suppression, or both? Immunology 112: 352-363
7. Busse, W. W., R. F. Lemanske, Jr., and J. E. Gern. 2010. Role of viral respiratory infections in asthma and asthma exacerbations. Lancet 376: 826-834
8. Iwasaki, A., and R. Medzhitov. 2010. Regulation of adaptive immunity by the innate immune system. Science 327: 291-295
9. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21: 335-376
10. Diebold, S. S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531
11. Lund, J. M., L. Alexopoulou, A. Sato, M. Karow, N. C. Adams, N. W. Gale, A. Iwasaki, and R. A. Flavell. 2004. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 101: 5598-5603
12. Camateros, P., M. Tamaoka, M. Hassan, R. Marino, J. Moisan, D. Marion, M. C. Guiot, J. G. Martin, and D. Radzioch. 2007. Chronic asthma-induced airway remodeling is prevented by Toll-like receptor-7/8 ligand S28463. Am. J. Respir. Crit. Care Med. 175: 1241-1249
13. Vultaggio, A., F. Nencini, P. M. Fitch, L. Filì, L. Maggi, P. Fanti, A. deVries, E. Beccastrini, F. Palandri, C. Manuelli, et al. 2009. Modified adenine (9-benzyl- 2-butoxy-8-hydroxyadenine) redirects Th2-mediated murine lung inflammation by triggering TLR7. J. Immunol. 182: 880-889
14. Xirakia, C., O. Koltsida, A. Stavropoulos, A. Thanassopoulou, V. Aidinis, P. Sideras, and E. Andreakos. 2010. Toll-like receptor 7-triggered immune response in the lung mediates acute and long-lasting suppression of experimental asthma. Am. J. Respir. Crit. Care Med. 181: 1207-1216
15. Grela, F., A. Aumeunier, E. Bardel, L. P. Van, E. Bourgeois, J. Vanoirbeek, M. Leite-de-Moraes, E. Schneider, M. Dy, A. Herbelin, and N. Thieblemont. 2011. The TLR7 agonist R848 alleviates allergic inflammation by targeting invariant NKT cells to produce IFN-g. J. Immunol. 186: 284-290
16. Kurimoto, A., K. Hashimoto, T. Nakamura, K. Norimura, H. Ogita, H. Takaku, R. Bonnert, T. McInally, H. Wada, and Y. Isobe. 2010. Synthesis and biological evaluation of 8-oxoadenine derivatives as Toll-like receptor 7 agonists introducing the antedrug concept. J. Med. Chem. 53: 2964-2972
17. Moisan, J., P. Camateros, T. Thuraisingam, D. Marion, H. Koohsari, P. Martin, M. L. Boghdady, A. Ding, M. Gaestel, M. C. Guiot, et al. 2006. TLR7 ligand prevents allergen-induced airway hyperresponsiveness and eosinophilia in allergic asthma by a MYD88-dependent and MK2-independent pathway. Am. J. Physiol. Lung Cell. Mol. Physiol. 290: L987-L995
18. Sel, S., M. Wegmann, S. Sel, S. Bauer, H. Garn, G. Alber, and H. Renz. 2007. Immunomodulatory effects of viral TLR ligands on experimental asthma depend on the additive effects of IL-12 and IL-10. J. Immunol. 178: 7805-7813
19. Fidock, M. D., B. E. Souberbielle, C. Laxton, J. Rawal, O. Delpuech-Adams, T. P. Corey, P. Colman, V. Kumar, J. B. Cheng, K. Wright, et al. 2011. The innate immune response, clinical outcomes, and ex vivo HCV antiviral efficacy of a TLR7 agonist (PF-4878691). Clin. Pharmacol. Ther. 89: 821-829
20. Dudek, A. Z., C. Yunis, L. I. Harrison, S. Kumar, R. Hawkinson, S. Cooley, J. P. Vasilakos, K. S. Gorski, and J. S. Miller. 2007. First in human phase I trial of 852A, a novel systemic Toll-like receptor 7 agonist, to activate innate immune responses in patients with advanced cancer. Clin. Cancer Res. 13: 7119-7125
21. Pockros, P. J., D. Guyader, H. Patton, M. J. Tong, T. Wright, J. G. McHutchison, and T. C. Meng. 2007. Oral resiquimod in chronic HCV infection: safety and efficacy in 2 placebo-controlled, double-blind phase IIa studies. J. Hepatol. 47: 174-182
22. Biffen, M., H. Matsui, S. E. Edwards, A. J. Leishman, K. Eiho, E. Holness, G. Satterthwaite, I. Doyle, H. Wada, N. J. Fraser, et al. 2012. Biological characterization of a novel class of Toll-like receptor 7 agonists designed to have reduced systemic activity. Br. J. Pharmacol. 166: 573-586
23. Wagner, T. L., C. L. Ahonen, A. M. Couture, S. J. Gibson, R. L. Miller, R. M. Smith, M. J. Reiter, J. P. Vasilakos, and M. A. Tomai. 1999. Modulation of TH1 and TH2 cytokine production with the immune response modifiers, R-848 and imiquimod. Cell. Immunol. 191: 10-19
24. Brugnolo, F., S. Sampognaro, F. Liotta, L. Cosmi, F. Annunziato, C. Manuelli, P. Campi, E. Maggi, S. Romagnani, and P. Parronchi. 2003. The novel synthetic immune response modifier R-848 (resiquimod) shifts human allergen-specific CD4+ TH2 lymphocytes into IFN-g-producing cells. J. Allergy Clin. Immunol. 111: 380-388
25. Filì, L., S. Ferri, F. Guarna, S. Sampognaro, C. Manuelli, F. Liotta, L. Cosmi, A. Matucci, A. Vultaggio, F. Annunziato, et al. 2006. Redirection of allergenspecific TH2 responses by a modified adenine through Toll-like receptor 7 interaction and IL-12/IFN release. J. Allergy Clin. Immunol. 118: 511-517
26. Camateros, P., C. Kanagaratham, J. Henri, R. Sladek, T. J. Hudson, and D. Radzioch. 2009. Modulation of the allergic asthma transcriptome following resiquimod treatment. Physiol. Genomics 38: 303-318
27. Liotta, F., F. Frosali, V. Querci, A. Mantei, L. Fili, L. Maggi, B. Mazzinghi, R. Angeli, E. Ronconi, V. Santarlasci, et al. 2008. Human immature myeloid dendritic cells trigger a TH2-polarizing program via Jagged-1/Notch interaction. J. Allergy Clin. Immunol. 121: 1000-1005.e8
28. Napolitani, G., A. Rinaldi, F. Bertoni, F. Sallusto, and A. Lanzavecchia. 2005. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 6: 769-776
29. Amsen, D., J. M. Blander, G. R. Lee, K. Tanigaki, T. Honjo, and R. A. Flavell. 2004. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 117: 515-526
30. Fang, T. C., Y. Yashiro-Ohtani, C. Del Bianco, D. M. Knoblock, S. C. Blacklow, and W. S. Pear. 2007. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 27: 100-110
31. Sun, J., C. J. Krawczyk, and E. J. Pearce. 2008. Suppression of Th2 cell development by Notch ligands Delta1 and Delta4. J. Immunol. 180: 1655-1661
32. Schandené, L., G. F. Del Prete, E. Cogan, P. Stordeur, A. Crusiaux, B. Kennes, S. Romagnani, and M. Goldman. 1996. Recombinant interferon-a selectively inhibits the production of interleukin-5 by human CD4+ T cells. J. Clin. Invest. 97: 309-315
33. Shibuya, H., and S. Hirohata. 2005. Differential effects of IFN-a on the expression of various TH2 cytokines in human CD4+ T cells. J. Allergy Clin. Immunol. 116: 205-212
34. Huber, J. P., H. J. Ramos, M. A. Gill, and J. D. Farrar. 2010. Cutting edge: type I IFN reverses human Th2 commitment and stability by suppressing GATA3. J. Immunol. 185: 813-817
35. Pritchard, A. L., O. J. White, J. G. Burel, and J. W. Upham. 2012. Innate interferons inhibit allergen and microbial specific T(H)2 responses. Immunol. Cell Biol. 90: 974-977
36. Sabat, R., G. Grütz, K. Warszawska, S. Kirsch, E. Witte, K. Wolk, and J. Geginat. 2010. Biology of interleukin-10. Cytokine Growth Factor Rev. 21: 331-344
37. Gorden, K. B., K. S. Gorski, S. J. Gibson, R. M. Kedl, W. C. Kieper, X. Qiu, M. A. Tomai, S. S. Alkan, and J. P. Vasilakos. 2005. Synthetic TLR agonists reveal functional differences between human TLR7 and TLR8. J. Immunol. 174: 1259-1268
38. Hanten, J. A., J. P. Vasilakos, C. L. Riter, L. Neys, K. E. Lipson, S. S. Alkan, and W. Birmachu. 2008. Comparison of human B cell activation by TLR7 and TLR9 agonists. BMC Immunol. 9: 39
39. Maillard, I., T. Fang, andW. S. Pear. 2005. Regulation of lymphoid development, differentiation, and function by the Notch pathway. Annu. Rev. Immunol. 23: 945-974
40. Jang, S., M. Schaller, A. A. Berlin, and N. W. Lukacs. 2010. Notch ligand deltalike 4 regulates development and pathogenesis of allergic airway responses by modulating IL-2 production and Th2 immunity. J. Immunol. 185: 5835-5844
41. Schaller, M. A., R. Neupane, B. D. Rudd, S. L. Kunkel, L. E. Kallal, P. Lincoln, J. B. Lowe, Y. Man, and N. W. Lukacs. 2007. Notch ligand Delta-like 4 regulates disease pathogenesis during respiratory viral infections by modulating Th2 cytokines. J. Exp. Med. 204: 2925-2934
42. Jurk, M., F. Heil, J. Vollmer, C. Schetter, A. M. Krieg, H. Wagner, G. Lipford, and S. Bauer. 2002. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat. Immunol. 3: 499
43. Kassner, N., M. Krueger, H. Yagita, A. Dzionek, A. Hutloff, R. Kroczek, A. Scheffold, and S. Rutz. 2010. Cutting edge: plasmacytoid dendritic cells induce IL-10 production in T cells via the Delta-like-4/Notch axis. J. Immunol. 184: 550-554
44. Van, L. P., E. Bardel, S. Gregoire, J. Vanoirbeek, E. Schneider, M. Dy, and N. Thieblemont. 2011. Treatment with the TLR7 agonist R848 induces regulatory T-cell-mediated suppression of established asthma symptoms. Eur. J. Immunol. 41: 1992-1999
45. Jackson, D. J., and S. L. Johnston. 2010. The role of viruses in acute exacerbations of asthma. J. Allergy Clin. Immunol. 125: 1178-1187, quiz 1188-1189
46. Reuter, S., N. Dehzad, H. Martin, L. Böhm, M. Becker, R. Buhl, M. Stassen, and C. Taube. 2012. TLR3 but not TLR7/8 ligand induces allergic sensitization to inhaled allergen. J. Immunol. 188: 5123-5131