IL-10 and regulatory T cells cooperate in allergen-specific immunotherapy to ameliorate allergic asthma

Journal of Immunology

Volumn 194, Issue 3, 2015, Pages 887-897

  Böhm, Livia ^a   Maxeiner, Joachim ^a   Meyer Martin, Helen ^a   Reuter, Sebastian ^a   Finotto, Susetta ^b   Klein, Matthias ^a   Schild, Hansjörg ^a   Schmitt, Edgar ^a   Bopp, Tobias ^a   Taube, Christian ^c  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; GAMMA INTERFERON; IMMUNOGLOBULIN E ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 5; OVALBUMIN; PLACEBO; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR T BET; IMMUNOGLOBULIN E;

AIRWAY REMODELING; ALLERGEN SPECIFIC IMMUNOTHERAPY; ALLERGIC AIRWAY INFLAMMATION; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG MEGADOSE; EOSINOPHIL COUNT; FEMALE; GOBLET CELL METAPLASIA; HISTOPATHOLOGY; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LUNG LAVAGE; METAPLASIA; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY T LYMPHOCYTE; TH1 CELL; TRANSGENIC MOUSE; TREATMENT DURATION; ANIMAL; ASTHMA; BIOSYNTHESIS; DESENSITIZATION; DISEASE MODEL; GENETICS; GOBLET CELL; IMMUNOLOGY; IMMUNOMODULATION; IMMUNOPHENOTYPING; KNOCKOUT MOUSE; LUNG; METABOLISM; PATHOLOGY; RESPIRATORY HYPERSENSITIVITY; T LYMPHOCYTE SUBPOPULATION;

AIRWAY REMODELING; ANIMALS; ASTHMA; CD4-POSITIVE T-LYMPHOCYTES; DESENSITIZATION, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; FEMALE; GOBLET CELLS; IMMUNOGLOBULIN E; IMMUNOMODULATION; IMMUNOPHENOTYPING; INTERLEUKIN-10; LUNG; METAPLASIA; MICE; MICE, KNOCKOUT; OVALBUMIN; RESPIRATORY HYPERSENSITIVITY; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 84921476622     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401612     Document Type: Article

References (53)

1. Robinson, D. S., Q. Hamid, S. Ying, A. Tsicopoulos, J. Barkans, A. M. Bentley, C. Corrigan, S. R. Durham, and A. B. Kay. 1992. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N. Engl. J. Med. 326: 298-304.
2. Eder, W., M. J. Ege, and E. von Mutius. 2006. The asthma epidemic. N. Engl. J. Med. 355: 2226-2235.
3. Taube, C., C. Duez, Z.-H. Cui, K. Takeda, Y.-H. Rha, J.-W. Park, A. Balhorn, D. D. Donaldson, A. Dakhama, and E. W. Gelfand. 2002. The role of IL-13 in established allergic airway disease. J. Immunol. 169: 6482-6489.
4. Galli, S. J., M. Tsai, and A. M. Piliponsky. 2008. The development of allergic inflammation. Nature 454: 445-454.
5. Holgate, S. T. 1999. The epidemic of allergy and asthma. Nature 402: B2-B4.
6. Elias, J. A., Z. Zhu, G. Chupp, and R. J. Homer. 1999. Airway remodeling in asthma. J. Clin. Invest. 104: 1001-1006.
7. Jacobsen, L., B. Niggemann, S. Dreborg, H. A. Ferdousi, S. Halken, A. Høst, A. Koivikko, L. A. Norberg, E. Valovirta, U. Wahn, and C. Möller, The PAT Investigator Group. 2007. Specific immunotherapy has long-term preventive effect of seasonal and perennial asthma: 10-year follow-up on the PAT study. Allergy 62: 943-948.
8. Burks, A. W., M. A. Calderon, T. Casale, L. Cox, P. Demoly, M. Jutel, H. Nelson, and C. A. Akdis. 2013. Update on allergy immunotherapy: American Academy of Allergy, Asthma & Immunology/European Academy of Allergy and Clinical Immunology/PRACTALL consensus report. J. Allergy Clin. Immunol. 131: 1288-1296.
9. Akdis, C. A. 2012. Therapies for allergic inflammation: refining strategies to induce tolerance. Nat. Med. 18: 736-749.
10. Durham, S. R., S. M. Walker, E. M. Varga, M. R. Jacobson, F. O'Brien, W. Noble, S. J. Till, Q. A. Hamid, and K. T. Nouri-Aria. 1999. Long-term clinical efficacy of grass-pollen immunotherapy. N. Engl. J. Med. 341: 468-475.
11. Bonifazi, F., M. Jutel, B. M. Biló, J. Birnbaum, and U. Muller, EAACI Interest Group on Insect Venom Hypersensitivity. 2005. Prevention and treatment of hymenoptera venom allergy: guidelines for clinical practice. Allergy 60: 1459-1470.
12. Abramson, M. J., R. M. Puy, and J. M. Weiner. 2010. Injection allergen immunotherapy for asthma. Cochrane Database Syst. Rev. 8: CD001186.
13. Lichtenstein, L. M., N. A. Holtzman, and L. S. Burnett. 1968. A quantitative in vitro study of the chromatographic distribution and immunoglobulin characteristics of human blocking antibody. J. Immunol. 101: 317-324.
14. Jutel, M., W. J. Pichler, D. Skrbic, A. Urwyler, C. Dahinden, and U. R. Müller. 1995. Bee venom immunotherapy results in decrease of IL-4 and IL-5 and increase of IFN-gamma secretion in specific allergen-stimulated T cell cultures. J. Immunol. 154: 4187-4194.
15. Bellinghausen, I., G. Metz, A. H. Enk, S. Christmann, J. Knop, and J. Saloga. 1997. Insect venom immunotherapy induces interleukin-10 production and a Th2-to-Th1 shift, and changes surface marker expression in venom-allergic subjects. Eur. J. Immunol. 27: 1131-1139.
16. Zheng, Y., and A. Y. Rudensky. 2007. Foxp3 in control of the regulatory T cell lineage. Nat. Immunol. 8: 457-462.
17. Jutel, M., M. Akdis, F. Budak, C. Aebischer-Casaulta, M. Wrzyszcz, K. Blaser, and C. A. Akdis. 2003. IL-10 and TGF-β cooperate in the regulatory T cell response to mucosal allergens in normal immunity and specific immunotherapy. Eur. J. Immunol. 33: 1205-1214.
18. Akdis, C. A., T. Blesken, M. Akdis, B. Wüthrich, and K. Blaser. 1998. Role of interleukin 10 in specific immunotherapy. J. Clin. Invest. 102: 98-106.
19. Francis, J. N., L. K. James, G. Paraskevopoulos, C. Wong, M. A. Calderon, S. R. Durham, and S. J. Till. 2008. Grass pollen immunotherapy: IL-10 induction and suppression of late responses precedes IgG4 inhibitory antibody activity. J. Allergy Clin. Immunol. 121: 1120-1125.
20. Möbs, C., C. Slotosch, H. Löffler, T. Jakob, M. Hertl, and W. Pfützner. 2010. Birch pollen immunotherapy leads to differential induction of regulatory T cells and delayed helper T cell immune deviation. J. Immunol. 184: 2194-2203.
21. Radulovic, S., M. R. Jacobson, S. R. Durham, and K. T. Nouri-Aria. 2008. Grass pollen immunotherapy induces Foxp3-expressing CD4+ CD25+ cells in the nasal mucosa. J. Allergy Clin. Immunol. 121: 1467-1472.
22. Kerstan, A., C. Albert, D. Klein, E.-B. Bröcker, and A. Trautmann. 2011. Wasp venom immunotherapy induces activation and homing of CD4(+)CD25(+) forkhead box protein 3-positive regulatory T cells controlling T(H)1 responses. J. Allergy Clin. Immunol. 127: 495-501.
23. Lou, W., C. Wang, Y. Wang, D. Han, and L. Zhang. 2012. Responses of CD4(+) CD25(+) Foxp3(+) and IL-10-secreting type I T regulatory cells to clusterspecific immunotherapy for allergic rhinitis in children. Pediatr. Allergy Immunol. 23: 140-149.
24. Van Oosterhout, A. J., B. Van Esch, G. Hofman, C. L. Hofstra, I. Van Ark, F. P. Nijkamp, M. L. Kapsenberg, H. F. Savelkoul, and F. R. Weller. 1998. Allergen immunotherapy inhibits airway eosinophilia and hyperresponsiveness associated with decreased IL-4 production by lymphocytes in a murine model of allergic asthma. Am. J. Respir. Cell Mol. Biol. 19: 622-628.
25. Janssen, E. M., A. J. van Oosterhout, F. P. Nijkamp, W. van Eden, and M. H. Wauben. 2000. The efficacy of immunotherapy in an experimental murine model of allergic asthma is related to the strength and site of T cell activation during immunotherapy. J. Immunol. 165: 7207-7214.
26. Taher, Y. A., B. C. A. M. van Esch, G. A. Hofman, P. A. J. Henricks, and A. J. M. van Oosterhout. 2008. 1alpha,25-dihydroxyvitamin D3 potentiates the beneficial effects of allergen immunotherapy in a mouse model of allergic asthma: role for IL-10 and TGF-beta. J. Immunol. 180: 5211-5221.
27. Maazi, H., S. Shirinbak, M. Willart, H. M. Hammad, M. Cabanski, L. Boon, V. Ganesh, A. M. Baru, G. Hansen, B. N. Lambrecht, et al. 2012. Contribution of regulatory T cells to alleviation of experimental allergic asthma after specific immunotherapy. Clin. Exp. Allergy 42: 1519-1528.
28. Al-Muhsen, S., J. R. Johnson, and Q. Hamid. 2011. Remodeling in asthma. J. Allergy Clin. Immunol. 128: 451-462, quiz 463-464.
29. 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.
30. Taube, C., C. Tertilt, G. Gyülveszi, N. Dehzad, K. Kreymborg, K. Schneeweiss, E. Michel, S. Reuter, J.-C. Renauld, D. Arnold-Schild, et al. 2011. IL-22 is produced by innate lymphoid cells and limits inflammation in allergic airway disease. PLoS One 6: e21799.
31. Reuter, S., A. Heinz, M. Sieren, R. Wiewrodt, E. W. Gelfand, M. Stassen, R. Buhl, and C. Taube. 2008. Mast cell-derived tumour necrosis factor is essential for allergic airway disease. Eur. Respir. J. 31: 773-782.
32. Doganci, A., R. Karwot, J. H. Maxeiner, P. Scholtes, E. Schmitt, M. F. Neurath, H. A. Lehr, I.-C. Ho, and S. Finotto. 2008. IL-2 receptor beta-chain signaling controls immunosuppressive CD4+ T cells in the draining lymph nodes and lung during allergic airway inflammation in vivo. J. Immunol. 181: 1917-1926.
33. Bopp, T., N. Dehzad, S. Reuter, M. Klein, N. Ullrich, M. Stassen, H. Schild, R. Buhl, E. Schmitt, and C. Taube. 2009. Inhibition of cAMP degradation improves regulatory T cell-mediated suppression. J. Immunol. 182: 4017-4024.
34. Martin, H., S. Reuter, N. Dehzad, A. Heinz, I. Bellinghausen, J. Saloga, I. Haasler, S. Korn, H. Jonuleit, R. Buhl, et al. 2012. CD4-mediated regulatory T-cell activation inhibits the development of disease in a humanized mouse model of allergic airway disease. J. Allergy Clin. Immunol. 129: 521-528.
35. Müller, U., A. Helbling, and M. Bischof. 1989. Predictive value of venomspecific IgE, IgG and IgG subclass antibodies in patients on immunotherapy with honey bee venom. Allergy 44: 412-418.
36. Randolph, C. C., and R. E. Reisman. 1986. Evaluation of decline in serum venom-specific IgE as a criterion for stopping venom immunotherapy. J. Allergy Clin. Immunol. 77: 823-827.
37. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
38. Finotto, S., M. F. Neurath, J. N. Glickman, S. Qin, H. A. Lehr, F. H. Green, K. Ackerman, K. Haley, P. R. Galle, S. J. Szabo, et al. 2002. Development of spontaneous airway changes consistent with human asthma in mice lacking T-bet. Science 295: 336-338.
39. Huang, T. J., P. A. MacAry, P. Eynott, A. Moussavi, K. C. Daniel, P. W. Askenase, D. M. Kemeny, and K. F. Chung. 2001. Allergen-specific Th1 cells counteract efferent Th2 cell-dependent bronchial hyperresponsiveness and eosinophilic inflammation partly via IFN-gamma. J. Immunol. 166: 207-217.
40. Wilder, J. A., D. D. Collie, D. E. Bice, Y. Tesfaigzi, C. R. Lyons, and M. F. Lipscomb. 2001. Ovalbumin aerosols induce airway hyperreactivity in naive DO11.10 T cell receptor transgenic mice without pulmonary eosinophilia or OVA-specific antibody. J. Leukoc. Biol. 69: 538-547.
41. Itoh, M., T. Takahashi, N. Sakaguchi, Y. Kuniyasu, J. Shimizu, F. Otsuka, and S. Sakaguchi. 1999. Thymus and autoimmunity: production of CD25+CD4+ naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J. Immunol. 162: 5317-5326.
42. Secrist, H., C. J. Chelen, Y. Wen, J. D. Marshall, and D. T. Umetsu. 1993. Allergen immunotherapy decreases interleukin 4 production in CD4+ T cells from allergic individuals. J. Exp. Med. 178: 2123-2130.
43. Cantani, A., and M. Micera. 2005. Significant decrease of IgE antibodies after a three-year controlled study of specific immunotherapy to pollen allergens in children with allergic asthma. Eur. Rev. Med. Pharmacol. Sci. 9: 103-111.
44. McMillan, S. J., G. Xanthou, and C. M. Lloyd. 2005. Therapeutic administration of Budesonide ameliorates allergen-induced airway remodelling. Clin. Exp. Allergy 35: 388-396.
45. Kearley, J., D. S. Robinson, and C. M. Lloyd. 2008. CD4+CD25+ regulatory T cells reverse established allergic airway inflammation and prevent airway remodeling. J. Allergy Clin. Immunol. 122: 617-624.
46. Shirinbak, S., Y. A. Taher, H. Maazi, R. Gras, B. C. van Esch, P. A. Henricks, J. N. Samsom, J. S. Verbeek, B. N. Lambrecht, A. J. van Oosterhout, and M. C. Nawijn. 2010. Suppression of Th2-driven airway inflammation by allergen immunotherapy is independent of B cell and Ig responses in mice. J. Immunol. 185: 3857-3865.
47. Finotto, S., M. Hausding, A. Doganci, J. H. Maxeiner, H. A. Lehr, C. Luft, P. R. Galle, and L. H. Glimcher. 2005. Asthmatic changes in mice lacking T-bet are mediated by IL-13. Int. Immunol. 17: 993-1007.
48. Fujiwara, M., K. Hirose, S. Kagami, H. Takatori, H. Wakashin, T. Tamachi, N. Watanabe, Y. Saito, I. Iwamoto, and H. Nakajima. 2007. T-bet inhibits both TH2 cell-mediated eosinophil recruitment and TH17 cell-mediated neutrophil recruitment into the airways. J. Allergy Clin. Immunol. 119: 662-670.
49. Dehzad, N., T. Bopp, S. Reuter, M. Klein, H. Martin, A. Ulges, M. Stassen, H. Schild, R. Buhl, E. Schmitt, and C. Taube. 2011. Regulatory T cells more effectively suppress Th1-induced airway inflammation compared with Th2. J. Immunol. 186: 2238-2244.
50. Meiler, F., J. Zumkehr, S. Klunker, B. Rückert, C. A. Akdis, and M. Akdis. 2008. In vivo switch to IL-10-secreting T regulatory cells in high dose allergen exposure. J. Exp. Med. 205: 2887-2898.
51. Häringer, B., L. Lozza, B. Steckel, and J. Geginat. 2009. Identification and characterization of IL-10/IFN-gamma-producing effector-like T cells with regulatory function in human blood. J. Exp. Med. 206: 1009-1017.
52. Vissers, J. L. M., B. C. A. M. van Esch, G. A. Hofman, M. L. Kapsenberg, F. R. Weller, and A. J. M. van Oosterhout. 2004. Allergen immunotherapy induces a suppressive memory response mediated by IL-10 in a mouse asthma model. J. Allergy Clin. Immunol. 113: 1204-1210.
53. Kearley, J., J. E. Barker, D. S. Robinson, and C. M. Lloyd. 2005. Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4+ CD25+ regulatory T cells is interleukin 10 dependent. J. Exp. Med. 202: 1539-1547.