IL-17 eliminates therapeutic effects of oral tolerance in murine airway allergic inflammation

Clinical and Experimental Allergy

Volumn 42, Issue 6, 2012, Pages 946-957

  Kawakami, H ^a   Koya, T ^a   Kagamu, H ^a   Kimura, Y ^a   Sakamoto, H ^a   Yamabayashi, C ^a   Furukawa, T ^a   Sakagami, T ^a   Miyabayashi, T ^a   Hasegawa, T ^b   Suzuki, E ^b   Narita, I ^a  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b NIIGATA UNIVERSITY MEDICAL AND DENTAL HOSPITAL   (Japan)

Author keywords

Bronchial asthma; Il 6; Immunotherapy; Regulatory T cell; Th17

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 6; OVALBUMIN; TRANSCRIPTION FACTOR FOXP3;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL TRANSFER; CHEMOSENSITIZATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; FEEDING; FEMALE; IMMUNOLOGICAL TOLERANCE; INTESTINE; LUNG LAVAGE; MOUSE; NONHUMAN; ORAL TOLERANCE; PEYER PATCH; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RESPIRATORY TRACT INFLAMMATION; TH17 CELL; TH2 CELL;

ADMINISTRATION, ORAL; ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES, MONOCLONAL; ASTHMA; CD4-POSITIVE T-LYMPHOCYTES; DESENSITIZATION, IMMUNOLOGIC; EOSINOPHILIA; FEMALE; IMMUNE TOLERANCE; INTERLEUKIN-17; INTERLEUKIN-6; LUNG; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OVALBUMIN; PEYER'S PATCHES; TH17 CELLS; TH2 CELLS;

EID: 84865160168     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/j.1365-2222.2012.04006.x     Document Type: Article

References (38)

1. Wills-Karp M. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu Rev Immunol 1999; 17:255-81.
2. Busse WW, Lemanske RF Jr. Asthma. N Engl J Med 2001; 344:350-62.
3. Umetsu DT, McIntire JJ, Akbari O, Macaubas C, DeKruyff RH. Asthma: an epidemic of dysregulated immunity. Nat Immunol 2002; 3:715-20.
4. Chakir J, Shannon J, Molet S et al. Airway remodeling-associated mediators in moderate to severe asthma: effect of steroids on TGF-beta, IL-11, IL-17, and type I and type III collagen expression. J Allergy Clin Immunol 2003; 111:1293-8.
5. Agache I, Ciobanu C, Agache C, Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med 2010; 104:1131-7
6. Schnyder-Candrian S, Togbe D, Couillin I et al. Interleukin-17 is a negative regulator of established allergic asthma. J Exp Med 2006; 203: 2715-25.
7. Nakae S, Komiyama Y, Nambu A et al. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002; 17:375-87.
8. Holgate ST, Polosa R. Treatment strategies for allergy and asthma. Nat Rev Immunol 2008; 8:218-30.
9. Weiner HL, Friedman A, Miller A et al. Oral tolerance: immunologic mechanisms and treatment of animal and human organ-specific autoimmune diseases by oral administration of autoantigens. Annu Rev Immunol 1994; 12:809-37.
10. Smith KM, Eaton AD, Finlayson LM, Garside P. Oral tolerance. Am J Respir Crit Care Med 2000; 162:S175-8.
11. Faria AM, Weiner HL. Oral tolerance: therapeutic implications for autoimmune diseases. Clin Dev Immunol 2006; 13:143-57.
12. Kraal G, Samsom JN, Mebius RE. The importance of regional lymph nodes for mucosal tolerance. Immunol Rev 2006; 213:119-30
13. Tsuji NM, Kosaka A. Oral tolerance: intestinal homeostasis and antigenspecific regulatory T cells. Trends Immunol 2008; 29:532-40.
14. Weaver CT, Hatton RD. Interplay between the TH17 and TReg cell lineages: a (co-)evolutionary perspective. Nat Rev Immunol 2009; 9:883-9.
15. Fossiez F, Banchereau J, Murray R, Van KC, Garrone P, Lebecque S. Interleukin-17. Int Rev Immunol 1998; 16:541-51.
16. Bettelli E, Carrier Y, Gao W et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441:235-8.
17. Wang GY, Sun B, Kong QF et al. IL-17 eliminates the therapeutic effects of myelin basic protein-induced nasal tolerance in experimental autoimmune encephalomyelitis by activating IL-6. Scand J Immunol 2008; 68:589 -97.
18. Bousquet J, Hejjaoui A, Dhivert H, Clauzel AM, Michel FB. Immunotherapy with a standardized dermatophagoides pteronyssinus extract. Systemic reactions during the rush protocol in patients suffering from asthma. J Allergy Clin Immunol 1989; 83:797-802.
19. US Department of Health and Human Services. National Institutes of Health. National Heart L, and Blood Institute. Expert panel report 3. Guidelines for the diagnosis and management of asthma, 2007. Available at http://www.nhlbi.nih. gov/guidelines/asthma/asthgdln.htm (accessed 1 August 2011).
20. Barczyk A, Pierzchala W, Sozanska E. Interleukin-17 in sputum correlates with airway hyperresponsiveness to methacholine. Respir Med 2003; 97:726-33.
21. Agache I, Ciobanu C, Agache C, Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med 2010; 104:1131-7.
22. Xystrakis E, Kusumakar S, Boswell S et al. Reversing the defective induction of IL-10-secreting regulatory T cells in glucocorticoid-resistant asthma patients. J Clin Invest 2006; 116:146-55.
23. Hartl D, Koller B, Mehlhorn AT et al. Quantitative and functional impairment of pulmonary CD4+CD25hi regulatory T cells in pediatric asthma. J Allergy Clin Immunol 2007; 119: 1258-66.
24. Wakashin H, Hirose K, Maezawa Y et al. IL-23 and Th17 cells enhance Th2-cell-mediated eosinophilic airway inflammation in mice. Am J Respir Crit Care Med 2008; 178:1023-32.
25. Hayashi M, Koya T, Kawakami H et al. A prostacyclin agonist with thromboxane inhibitory activity for airway allergic inflammation in mice. Clin Exp Allergy 2010; 40:317-26.
26. Koya T, Takeda K, Kodama T et al. RANTES (CCL5) regulates airway responsiveness after repeated allergen challenge. Am J Respir Cell Mol Biol 2006; 35:147-54.
27. Koya T, Kodama T, Takeda K et al. Importance of myeloid dendritic cells in persistent airway disease after repeated allergen exposure. Am J Respir Crit Care Med 2006; 173:42-55.
28. Koya T, Matsuda H, Takeda K et al. IL-10-treated dendritic cells decrease airway hyperresponsiveness and airway inflammation in mice. J Allergy Clin Immunol 2007; 119:1241-50.
29. Hauet-Broere F, Unger WW, Garssen J, Hoijer MA, Kraal G, Samsom JN. Functional CD25- and CD25+ mucosal regulatory T cells are induced in gutdraining lymphoid tissue within 48 h after oral antigen application. Eur J Immunol 2003; 33:2801-10.
30. Zinselmeyer BH, Dempster J, Gurney AM et al. In situ characterization of CD4+ T cell behavior in mucosal and systemic lymphoid tissues during the induction of oral priming and tolerance. J Exp Med 2005; 201:1815-23.
31. Doganci A, Eigenbrod T, Krug N et al. The IL-6R alpha chain controls lung CD4+CD25+ Treg development and function during allergic airway inflammation in vivo. J Clin Invest 2005; 115:313-25.
32. Wilson RH, Whitehead GS, Nakano H, Free ME, Kolls JK, Cook DN. Allergic sensitization through the airway primes Th17-dependent neutrophilia and airway hyperresponsiveness. Am J Respir Crit Care Med 2009; 180: 720-30.
33. Peron JP, Yang K, Chen ML et al. Oral tolerance reduces Th17 cells as well as the overall inflammation in the central nervous system of EAE mice. J Neuroimmunol 2010; 227:10-7.
34. Korn T, Mitsdoerffer M, Croxford AL et al. IL-6 controls Th17 immunity in vivo by inhibiting the conversion of conventional T cells into Foxp3+ regulatory T cells. Proc Natl Acad Sci U S A 2008; 105:18460-5.
35. Doganci A, Sauer K, Karwot R, Finotto S. Pathological role of IL-6 in the experimental allergic bronchial asthma in mice. Clin Rev Allergy Immunol 2005; 28:257-70.
36. Russo M, Nahori MA, Lefort J et al. Suppression of asthma-like responses in different mouse strains by oral tolerance. Am J Respir Cell Mol Biol 2001; 24:518-26.
37. Chung YH, Means RE, Choi JK, Lee BS, Jung JU. Kaposi's sarcoma-associated herpesvirus OX2 glycoprotein activates myeloid-lineage cells to induce inflammatory cytokine production. J Virol 2002; 76:4688-98.
38. Razafindratsita A, Saint-Lu N, Mascarell L et al. Improvement of sublingual immunotherapy efficacy with a mucoadhesive allergen formulation. J Allergy Clin Immunol 2007; 120: 278-85.