The adjuvant effect of TLR agonists on CD4+ effector T cells is under the indirect control of regulatory T cells

European Journal of Immunology

Volumn 41, Issue 8, 2011, Pages 2303-2313

  Olivier, Aurélie ^a,b   Sainz Perez, Alexander ^a,b   Dong, Hui ^a,b   Sparwasser, Tim ^c   Majlessi, Laleh ^a,b   Leclerc, Claude ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

Author keywords

Adjuvant; T cells; TLR; Tregs; Vaccination

Indexed keywords

TOLL LIKE RECEPTOR AGONIST; TRANSCRIPTION FACTOR FOXP3;

ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOMODULATION; IN VIVO STUDY; INHIBITION KINETICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STEADY STATE;

ADJUVANTS, IMMUNOLOGIC; AMINO ACID SEQUENCE; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GREEN FLUORESCENT PROTEINS; IMIDAZOLES; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; OLIGODEOXYRIBONUCLEOTIDES; OVALBUMIN; PEPTIDE FRAGMENTS; POLY I-C; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTORS; ZYMOSAN;

EID: 79960708834     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201041387     Document Type: Article

References (51)

1. Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M. and Toda, M., Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 1995. 155: 1151-1164.
2. Korn, T., Reddy, J., Gao, W., Bettelli, E., Awasthi, A., Petersen, T. R., Backstrom, B. T., et al., Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. 2007. 13: 423-431.
3. + natural regulatory T cells are specific for microbial antigens. J. Exp. Med. 2006. 203: 777-788.
4. Belkaid, Y., Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 2007. 7: 875-888.
5. + T cells: a common basis between tumor immunity and autoimmunity. J. Immunol. 1999. 163: 5211-5218.
6. Kawai, T. and Akira, S., TLR signaling. Semin. Immunol. 2007. 19: 24-32.
7. Steinman, R. M. and Hemmi, H., Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol. 2006. 311: 17-58.
8. + T cells. Immunology 2007. 122: 149-156.
9. Sutmuller, R. P., Morgan, M. E., Netea, M. G., Grauer, O. and Adema, G. J., Toll-like receptors on regulatory T cells: expanding immune regulation. Trends Immunol. 2006. 27: 387-393.
10. + regulatory T cell function. Science 2005. 309: 1380-1384.
11. Sutmuller, R. P., den Brok, M. H., Kramer, M., Bennink, E. J., Toonen, L. W., Kullberg, B. J., Joosten, L. A., et al., Toll-like receptor 2 controls expansion and function of regulatory T cells. J. Clin. Invest. 2006. 116: 485-494.
12. + regulatory T cells. Proc. Natl. Acad. Sci. USA 2006. 103: 7048-7053.
13. Caramalho, I., Lopes-Carvalho, T., Ostler, D., Zelenay, S., Haury, M. and Demengeot, J., Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide. J. Exp. Med. 2003. 197: 403-411.
14. + T regulatory cells. J. Immunol. 2005. 175: 8051-8059.
15. + T cell epitope requires an adjuvant signal. J. Immunol. 2005. 174: 3432-3439.
16. + T-cell help. Blood 2007. 109: 5318-5326.
17. + T regulatory cells. J. Immunol. 2006. 176: 3301-3305.
18. + regulatory T cells induces a scurfy-like disease. J. Exp. Med. 2007. 204: 57-63.
19. Lund, J. M., Hsing, L., Pham, T. T. and Rudensky, A. Y., Coordination of early protective immunity to viral infection by regulatory T cells. Science 2008. 320: 1220-1224.
20. + T cell-mediated suppression by dendritic cells. Science 2003. 299: 1033-1036.
21. Fontenot, J. D., Rasmussen, J. P., Williams, L. M., Dooley, J. L., Farr, A. G. and Rudensky, A. Y., Regulatory T cell lineage specification by the forkhead transcription factor Foxp3. Immunity 2005. 22: 329-341.
22. Wan, Y. Y. and Flavell, R. A., Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc. Natl. Acad. Sci. USA 2005. 102: 5126-5131.
23. + regulatory T cells control the magnitude of T-dependent humoral immune responses to exogenous antigens. Eur. J. Immunol. 2006. 36: 855-863.
24. Oldenhove, G., de Heusch, M., Urbain-Vansanten, G., Urbain, J., Maliszewski, C., Leo, O. and Moser, M., CD4+ CD25+ regulatory T cells control T helper cell type 1 responses to foreign antigens induced by mature dendritic cells in vivo. J. Exp. Med. 2003. 198: 259-266.
25. Hisaeda, H., Maekawa, Y., Iwakawa, D., Okada, H., Himeno, K., Kishihara, K., Tsukumo, S. and Yasutomo, K., Escape of malaria parasites from host immunity requires CD4+ CD25+ regulatory T cells. Nat. Med. 2004. 10: 29-30.
26. Taylor, M. D., LeGoff, L., Harris, A., Malone, E., Allen, J. E. and Maizels, R. M., Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 2005. 174: 4924-4933.
27. Fecci, P. E., Sweeney, A. E., Grossi, P. M., Nair, S. K., Learn, C. A., Mitchell, D. A., Cui, et al., Systemic anti-CD25 monoclonal antibody administration safely enhances immunity in murine glioma without eliminating regulatory T cells. Clin. Cancer Res. 2006. 12: 4294-4305.
28. Conroy, H., Marshall, N. A. and Mills, K. H., TLR ligand suppression or enhancement of Treg cells? A double-edged sword in immunity to tumours. Oncogene 2008. 27: 168-180.
29. Dai, J., Liu, B. and Li, Z., Regulatory T cells and Toll-like receptors: what is the missing link? Int. Immunopharmacol. 2009. 9: 528-533.
30. Kabelitz, D., Expression and function of Toll-like receptors in T lymphocytes. Curr. Opin. Immunol. 2007. 19: 39-45.
31. Berraondo, P., Nouze, C., Preville, X., Ladant, D. and Leclerc, C., Eradication of large tumors in mice by a tritherapy targeting the innate, adaptive, and regulatory components of the immune system. Cancer Res. 2007. 67: 8847-8855.
32. Chen, Q., Davidson, T. S., Huter, E. N. and Shevach, E. M., Engagement of TLR2 does not reverse the suppressor function of mouse regulatory T cells, but promotes their survival. J. Immunol. 2009. 183: 4458-4466.
33. Gelman, A. E., LaRosa, D. F., Zhang, J., Walsh, P. T., Choi, Y., Sunyer, J. O. and Turka, L. A., The adaptor molecule MyD88 activates PI-3 kinase signaling in CD4+ T cells and enables CpG oligodeoxynucleotide-mediated costimulation. Immunity 2006. 25: 783-793.
34. + T cells. Immunol. Lett. 2007. 108: 183-188.
35. Tadokoro, C. E., Shakhar, G., Shen, S., Ding, Y., Lino, A. C., Maraver, A., Lafaille, J. J. and Dustin, M. L., Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. J. Exp. Med. 2006. 203: 505-511.
36. + regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur. J. Immunol. 2000. 30: 1538-1543.
37. high regulatory T cells modulate myeloid but not plasmacytoid dendritic cells activation. J. Immunol. 2006. 176: 5293-5298.
38. + T cells. J. Immunol. 2006. 176: 6202-6210.
39. + T cells induce perforin-dependent dendritic cell death in tumor-draining lymph nodes. Immunity 2010. 32: 266-278.
40. van Maren, W. W., Jacobs, J. F., de Vries, I. J., Nierkens, S. and Adema, G. J., Toll-like receptor signalling on Tregs: to suppress or not to suppress? Immunology 2008. 124: 445-452.
41. Netea, M. G., Sutmuller, R., Hermann, C., Van der Graaf, C. A., Van der Meer, J. W., van Krieken, J. H., Hartung, T., et al., Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J. Immunol. 2004. 172: 3712-3718.
42. Wesch, D., Beetz, S., Oberg, H. H., Marget, M., Krengel, K. and Kabelitz, D., Direct costimulatory effect of TLR3 ligand poly(I:C) on human gamma delta T lymphocytes. J. Immunol. 2006. 176: 1348-1354.
43. Krieg, A. M., Therapeutic potential of Toll-like receptor 9 activation. Nat. Rev. Drug Discov. 2006. 5: 471-484.
44. Wang, R. F., Regulatory T cells and toll-like receptors in cancer therapy. Cancer Res. 2006. 66: 4987-4990.
45. El Andaloussi, A., Han, Y. and Lesniak, M. S., Prolongation of survival following depletion of CD4+CD25+ regulatory T cells in mice with experimental brain tumors. J. Neurosurg. 2006. 105: 430-437.
46. Dannull, J., Su, Z., Rizzieri, D., Yang, B. K., Coleman, D., Yancey, D., Zhang, A., et al., Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J. Clin. Invest. 2005. 115: 3623-3633.
47. Morse, M. A., Hobeika, A. C., Osada, T., Serra, D., Niedzwiecki, D., Lyerly, H. K. and Clay, T. M., Depletion of human regulatory T cells specifically enhances antigen specific immune responses to cancer vaccines. Blood 2008. 112: 610-618.
48. Jarnicki, A. G., Conroy, H., Brereton, C., Donnelly, G., Toomey, D., Walsh, K., Sweeney, C., et al., Attenuating regulatory T cell induction by TLR agonists through inhibition of p38 MAPK signaling in dendritic cells enhances their efficacy as vaccine adjuvants and cancer immunotherapeutics. J. Immunol. 2008. 180: 3797-3806.
49. Muller, U., Steinhoff, U., Reis, L. F., Hemmi, S., Pavlovic, J., Zinkernagel, R. M. and Aguet, M., Functional role of type I and type II interferons in antiviral defense. Science 1994. 264: 1918-1921.
50. + regulatory T cells. J. Immunol. 2008. 180: 1565-1575.
51. + T-cell responses in vivo after viral stimulation. Blood 2004. 104: 1808-1815.