A GpC-rich oligonucleotide acts on plasmacytoid dendritic cells to promote immune suppression

Journal of Immunology

Volumn 189, Issue 5, 2012, Pages 2283-2289

  Volpi, Claudia ^a   Fallarino, Francesca ^a   Bianchi, Roberta ^a   Orabona, Ciriana ^a   De Luca, Antonella ^a   Vacca, Carmine ^a   Romani, Luigina ^a   Gran, Bruno ^b   Grohmann, Ursula ^a   Puccetti, Paolo ^a   Belladonna, Maria L ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GPC RICH OLIGONUCLEOTIDE; IMIQUIMOD; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOLEAMINE 2,3 DIOXYGENASE; MYELOID DIFFERENTIATION FACTOR 88; OLIGONUCLEOTIDE; SINGLE STRANDED RNA; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOCRINE EFFECT; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SKIN TEST;

ANIMALS; CELLS, CULTURED; DENDRITIC CELLS; FEMALE; HUMANS; IMMUNE TOLERANCE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON-BETA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; OLIGODEOXYRIBONUCLEOTIDES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, INTERLEUKIN-1; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 7; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 84865417147     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200497     Document Type: Article

References (45)

1. Krieg, A. M., A. K. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, and D. M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546-549.
2. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
3. Uhlmann, E., A. Ryte, and A. Peyman. 1997. Studies on the mechanism of stabilization of partially phosphorothioated oligonucleotides against nucleolytic degradation. Antisense Nucleic Acid Drug Dev. 7: 345-350.
4. Kline, J. N., and A. M. Krieg. 2008. Toll-like receptor 9 activation with CpG oligodeoxynucleotides for asthma therapy. Drug News Perspect. 21: 434-439.
5. Horner, A. A., J. H. Van Uden, J. M. Zubeldia, D. Broide, and E. Raz. 2001. DNA-based immunotherapeutics for the treatment of allergic disease. Immunol. Rev. 179: 102-118.
6. Becker, Y. 2005. CpG ODNs treatments of HIV-1 infected patients may cause the decline of transmission in high risk populations - a review, hypothesis and implications. Virus Genes 30: 251-266.
7. Krieg, A. M. 2006. Therapeutic potential of Toll-like receptor 9 activation. Nat. Rev. Drug Discov. 5: 471-484.
8. Jurk, M., and J. Vollmer. 2007. Therapeutic applications of synthetic CpG oligodeoxynucleotides as TLR9 agonists for immune modulation. BioDrugs 21: 387-401.
9. Murad, Y. M., and T. M. Clay. 2009. CpG oligodeoxynucleotides as TLR9 agonists: therapeutic applications in cancer. BioDrugs 23: 361-375.
10. Vollmer, J., and A. M. Krieg. 2009. Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists. Adv. Drug Deliv. Rev. 61: 195-204.
11. Gupta, G. K., and D. K. Agrawal. 2010. CpG oligodeoxynucleotides as TLR9 agonists: therapeutic application in allergy and asthma. BioDrugs 24: 225-235.
12. Matesic, D., A. Lenert, and P. Lenert. 2012. Modulating toll-like receptor 7 and 9 responses as therapy for allergy and autoimmunity. Curr. Allergy Asthma Rep. 12: 8-17.
13. Fallarino, F., C. Volpi, T. Zelante, C. Vacca, M. Calvitti, M. C. Fioretti, P. Puccetti, L. Romani, and U. Grohmann. 2009. IDO mediates TLR9-driven protection from experimental autoimmune diabetes. J. Immunol. 183: 6303-6312.
14. Celhar, T., R. Magalhães, and A. M. Fairhurst. 2012. TLR7 and TLR9 in SLE: when sensing self goes wrong. Immunol. Res. 10.1007/s12026-012-8270-1.
15. Hoshi, N., H. Watanabe, H. Kobayashi, H. Sekine, N. Hoshi, T. Sugino, T. Suzuki, Y. Sato, and H. Ohira. 2007. Inhibitory oligodeoxynucleotide improves glomerulonephritis and prolongs survival in MRL-lpr/lpr mice. Fukushima J. Med. Sci. 53: 70-84.
16. Wingender, G., N. Garbi, B. Schumak, F. Jüngerkes, E. Endl, D. von Bubnoff, J. Steitz, J. Striegler, G. Moldenhauer, T. Tüting, et al. 2006. Systemic application of CpG-rich DNA suppresses adaptive T cell immunity via induction of IDO. Eur. J. Immunol. 36: 12-20.
17. Klinman, D. M., D. Currie, I. Gursel, and D. Verthelyi. 2004. Use of CpG oligodeoxynucleotides as immune adjuvants. Immunol. Rev. 199: 201-216 (Review).
18. Fallarino, F., and P. Puccetti. 2006. Toll-like receptor 9-mediated induction of the immunosuppressive pathway of tryptophan catabolism. Eur. J. Immunol. 36: 8-11.
19. Puccetti, P. 2007. On watching the watchers: IDO and type I/II IFN. Eur. J. Immunol. 37: 876-879 (Review).
20. Avalos, A. M., and H. L. Ploegh. 2011. Competition by inhibitory oligonucleotides prevents binding of CpG to C-terminal TLR9. Eur. J. Immunol. 41: 2820-2827.
21. Ho, P. P., P. Fontoura, P. J. Ruiz, L. Steinman, and H. Garren. 2003. An immunomodulatory GpG oligonucleotide for the treatment of autoimmunity via the innate and adaptive immune systems. J. Immunol. 171: 4920-4926.
22. Graham, K. L., L. Y. Lee, J. P. Higgins, L. Steinman, P. J. Utz, and P. P. Ho. 2010. Treatment with a toll-like receptor inhibitory GpG oligonucleotide delays and attenuates lupus nephritis in NZB/W mice. Autoimmunity 43: 140-155.
23. Forsbach, A., U. Samulowitz, K. Völp, H. P. Hofmann, B. Noll, S. Tluk, C. Schmitz, T. Wader, C. Müller, A. Podszuweit, et al. 2011. Dual or triple activation of TLR7, TLR8, and/or TLR9 by single-stranded oligoribonucleotides. Nucleic Acid Ther 21: 423-436.
24. Kaminski, M. M., A. Ohnemus, M. Cornitescu, and P. Staeheli. 2012. Plasmacytoid dendritic cells and Toll-like receptor 7-dependent signalling promote efficient protection of mice against highly virulent influenza A virus. J. Gen. Virol. 93: 555-559.
25. Grohmann, U., R. Bianchi, C. Orabona, F. Fallarino, C. Vacca, A. Micheletti, M. C. Fioretti, and P. Puccetti. 2003. Functional plasticity of dendritic cell subsets as mediated by CD40 versus B7 activation. J. Immunol. 171: 2581-2587.
26. Grohmann, U., C. Volpi, F. Fallarino, S. Bozza, R. Bianchi, C. Vacca, C. Orabona, M. L. Belladonna, E. Ayroldi, G. Nocentini, et al. 2007. Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat. Med. 13: 579-586.
27. Romani, L., F. Fallarino, A. De Luca, C. Montagnoli, C. D'Angelo, T. Zelante, C. Vacca, F. Bistoni, M. C. Fioretti, U. Grohmann, et al. 2008. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451: 211-215.
28. Grohmann, U., C. Orabona, F. Fallarino, C. Vacca, F. Calcinaro, A. Falorni, P. Candeloro, M. L. Belladonna, R. Bianchi, M. C. Fioretti, and P. Puccetti. 2002. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol. 3: 1097-1101.
29. Barchet, W., V. Wimmenauer, M. Schlee, and G. Hartmann. 2008. Accessing the therapeutic potential of immunostimulatory nucleic acids. Curr. Opin. Immunol. 20: 389-395.
30. Fallarino, F., C. Asselin-Paturel, C. Vacca, R. Bianchi, S. Gizzi, M. C. Fioretti, G. Trinchieri, U. Grohmann, and P. Puccetti. 2004. Murine plasmacytoid dendritic cells initiate the immunosuppressive pathway of tryptophan catabolism in response to CD200 receptor engagement. J. Immunol. 173: 3748-3754.
31. Puccetti, P., and U. Grohmann. 2007. IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-kappaB activation. Nat. Rev. Immunol. 7: 817-823.
32. Baban, B., P. R. Chandler, B. A. Johnson, III, L. Huang, M. Li, M. L. Sharpe, L. M. Francisco, A. H. Sharpe, B. R. Blazar, D. H. Munn, and A. L. Mellor. 2011. Physiologic control of IDO competence in splenic dendritic cells. J. Immunol. 187: 2329-2335.
33. Belladonna, M. L., C. Volpi, R. Bianchi, C. Vacca, C. Orabona, M. T. Pallotta, L. Boon, S. Gizzi, M. C. Fioretti, U. Grohmann, and P. Puccetti. 2008. Cutting edge: autocrine TGF-b sustains default tolerogenesis by IDO-competent dendritic cells. J. Immunol. 181: 5194-5198.
34. Yamamoto, M., S. Sato, K. Mori, K. Hoshino, O. Takeuchi, K. Takeda, and S. Akira. 2002. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J. Immunol. 169: 6668-6672.
35. +dendritic cells to acquire potent indoleamine 2,3-dioxygenase- dependent T cell regulatory functions via IFN Type 1 signaling. J. Immunol. 175: 5601-5605.
36. Park, B., M. M. Brinkmann, E. Spooner, C. C. Lee, Y. M. Kim, and H. L. Ploegh. 2008. Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat. Immunol. 9: 1407-1414.
37. Swiecki, M., and M. Colonna. 2010. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol. Rev. 234: 142-162.
38. de Luca, A., S. Bozza, T. Zelante, S. Zagarella, C. D'Angelo, K. Perruccio, C. Vacca, A. Carvalho, C. Cunha, F. Aversa, and L. Romani. 2010. Non-hematopoietic cells contribute to protective tolerance to Aspergillus fumigatus via a TRIF pathway converging on IDO. Cell. Mol. Immunol. 7: 459-470.
39. Bonifazi, P., T. Zelante, C. D'Angelo, A. De Luca, S. Moretti, S. Bozza, K. Perruccio, R. G. Iannitti, G. Giovannini, C. Volpi, et al. 2009. Balancing inflammation and tolerance in vivo through dendritic cells by the commensal Candida albicans. Mucosal Immunol. 2: 362-374.
40. Pallotta, M. T., C. Orabona, C. Volpi, C. Vacca, M. L. Belladonna, R. Bianchi, G. Servillo, C. Brunacci, M. Calvitti, S. Bicciato, et al. 2011. Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat. Immunol. 12: 870-878.
41. Broomfield, S. A., R. G. van der Most, A. C. Prosser, S. Mahendran, M. G. Tovey, M. J. Smyth, B. W. Robinson, and A. J. Currie. 2009. Locally administered TLR7 agonists drive systemic antitumor immune responses that are enhanced by anti-CD40 immunotherapy. J. Immunol. 182: 5217-5224.
42. Vultaggio, A., F. Nencini, S. Pratesi, L. Maggi, A. Guarna, F. Annunziato, S. Romagnani, P. Parronchi, and E. Maggi. 2011. The TLR7 ligand 9-benzyl-2-butoxy-8-hydroxy adenine inhibits IL-17 response by eliciting IL-10 and IL-10-inducing cytokines. J. Immunol. 186: 4707-4715.
43. Yu, C. F., W. M. Peng, J. Oldenburg, J. Hoch, T. Bieber, A. Limmer, G. Hartmann, W. Barchet, A. M. Eis-Hübinger, and N. Novak. 2010. Human plasmacytoid dendritic cells support Th17 cell effector function in response to TLR7 ligation. J. Immunol. 184: 1159-1167.
44. Hemmi, H., T. Kaisho, O. Takeuchi, S. Sato, H. Sanjo, K. Hoshino, T. Horiuchi, H. Tomizawa, K. Takeda, and S. Akira. 2002. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3: 196-200.
45. Kawai, T., and S. Akira. 2006. Innate immune recognition of viral infection. Nat. Immunol. 7: 131-137.