Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells

Journal of Experimental Medicine

Volumn 199, Issue 11, 2004, Pages 1567-1575

  Akdis, Mübeccel ^a   Verhagen, Johan ^a   Taylor, Alison ^a   Karamloo, Fariba ^a   Karagiannidis, Christian ^a   Crameri, Reto ^a   Thunberg, Sarah ^a,b   Deniz, Günnur ^a,c   Valenta, Rudolf ^d   Fiebig, Helmut ^e   Kegel, Christian ^f   Disch, Rainer ^f   Schmidt Weber, Carsten B ^a   Blaser, Kurt ^a   Akdis, Cezmi A ^a  

^a SWISS INSTITUTE OF ALLERGY AND ASTHMA RESEARCH SIAF   (Switzerland)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c ISTANBUL UNIVERSITY   (Turkey)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e ALLERGOPHARMA JOACHIM GANZER KG   (Germany)

^f Clinic for Dermatology and Allergy   (Switzerland)

Author keywords

Allergens; Immune regulation; Interleukins; Peripheral tolerance; Suppression

Indexed keywords

ALLERGEN; CD4 ANTIGEN; COMPLEMENTARY DNA; CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; ELONGATION FACTOR 1ALPHA; GAMMA INTERFERON; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; POLLEN ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TUBERCULIN;

ALLERGY; ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LYMPHOCYTE CULTURE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL;

ADULT; ALLERGENS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION; HUMANS; HYPERSENSITIVITY; INTERFERON TYPE II; INTERLEUKIN-10; INTERLEUKIN-4; T-LYMPHOCYTES; TH2 CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 2942685507     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20032058     Document Type: Article

References (43)

1. Teale, J.M., and N.R. Klinman. 1980. Tolerance as an active process. Nature. 288:385-387.
2. Parijs, L.V., and A.K. Abbas. 1998. Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science. 280:243-247.
3. Mosmann, T.R., H. Cherwinski, M.W. Bond, M.A. Giedlin, and R.L. Coffinan. 1986. Two types of murine helper T cell clones. 1. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 136:2348-2357.
4. Romagnani, S. 1994. Lymphokine production by human T cells in disease states. Annu. Rev. Immunol. 12:227-257.
5. Gershon, R.K., and K. Kondo. 1970. Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology. 18:723-737.
6. + T cells are important for the balance between protective and pathogenic cell-mediated immunity. J. Exp. Med. 179:589-600.
7. Sakaguchi, S., N. Sakaguchi, M. Asano, M. Itoh, and M. Toda. 1995. 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. 155:1151-1164.
8. 2 in bee venom immunotherapy and recovery by IL-2 and IL-15 in vitro. J. Clin. Invest. 98:1676-1683.
9. Davies, J.D., L.Y.W. Leong, A. Mellor, S.P. Cobbold, and H. Waldmann. 1996. T cell suppression in transplantation tolerance through linked recognition. J. Immunol. 168:5558-5565.
10. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 389:737-742.
11. Akdis, C.A., T. Blesken, M. Akdis, B. Wüthrich, and K. Blaser. 1998. Role of IL-10 in specific immunotherapy. J. Clin. Invest. 102:98-106.
12. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188:287-296.
13. Shevach, E.M. 2002. CD4+ CD25+ suppressor T cells: more questions than answers. Nat. Rev. Immunol. 2:389-400.
14. Wood, K.J., and S. Sakaguchi. 2003. Regulatory T cells in transplantation tolerance. Nat. Rev. Immunol. 3:199-210.
15. Qin, S., S.P. Cobbold, H. Pope, J. Elliott, D. Kioussis, J. Davies, and H. Waldmann. 1993. "Infectious" transplantation tolerance. Science. 259:974-977.
16. Chen, Y., V.K. Kuchroo, J. Inobe, D.A. Hafler, and H.L. Weiner. 1994. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science. 265:1237-1240.
17. Cong, Y., C.T. Weaver, A. Lazenby, and C.O. Elson. 2002. Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. J. Immunol. 169:6112-6119.
18. Jutel, M., T. Watanabe, S. Klunker, M. Akdis, O.A.R. Thomet, J. Malolepszy, T. Zak-Nejmarrk, R. Koga, T. Kobayashi, K. Blaser, and A.C. Akdis. 2001. Histamine regulates T-cell and antibody responses by differential expression of H1 and H2 receptors. Nature. 413:420-425.
19. Durham, S.R., S.M. Walker, E.-V. 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.
20. Akdis, C.A., and K. Blaser. 2001. Bypassing IgE and targeting T cells for specific immunotherapy of allergy. Trends Immunol. 22:175-178.
21. Jutel, M., M. Akdis, F. Budak, C. Aebischer-Casaulta, M. Wrzyszcz, K. Blaser, and A.C. Akdis. 2003. IL-10 and TGF-β cooperate in regulatory T cell response to mucosal allergens in normal immunity and specific immunotherapy. Eur. J. Immunol. 33:1205-1214.
22. 2-specific T cell clones from human allergic and non-allergic individuals: cytokine patterns change in response to the antigen concentration. Eur. J. Immunol. 22:1357-1363.
23. Ebner, C., S. Schenk, N. Najafian, U. Siemann, R. Steiner, G.W. Fischer, K. Hoffmann, Z. Szepfalusi, O. Scheiner, and D. Kraft. 1995. Nonallergic individuals recognize the same T cell epitopes of Bet v 1, the major birch pollen allergen, as atopic patients. J. Immunol. 154:1932-1940.
24. + T cells based on cytokine secretion. Eur. J. Immunol. 29:4053-4059.
25. Akdis, C.A., A. Joss, M. Akdis, A. Faith, and K. Blaser. 2000. A molecular basis for T cell suppression by IL-10: CD28-associated IL-10 receptor inhibits CD28 tyrosine phosphorylation and phosphatidylinositol 3-kinase binding. FASEB J. 14:1666-1669.
26. Liu, Y., S.H. Wei, A.S. Ho, R. de Waal Malefyt, and K.W. Moore. 1994. Expression cloning and characterization of a human IL-10 receptor. J. Immunol. 152:1821-1829.
27. Trautmann, A., M. Akdis, D. Kleeman, F. Altznauer, H.-U. Simon, T. Graeve, M. Noll, K. Blaser, and C.A. Akdis. 2000. T cell-mediated Fas-induced keratinocyte apoptosis plays a key pathogenetic role in eczematous dermatitis. J. Clin. Invest. 106:25-35.
28. Kunzmann, S., J.G. Wohfahrt, S. Itoh, H. Asao, M. Komada, C.A. Akdis, K. Blaser, and C.B. Schmidt-Weber. 2003. SARA and Hgs attenuate susceptibility to TGF-beta1-mediated T cell suppression. FASEB J. 17:194-202.
29. Akdis, M., A. Trautmann, S. Klunker, I. Daigle, U.C. Kücü ksezer, W. Deglmann, R. Disch, K. Blaser, and C.A. Akdis. 2003. T helper (Th) 2 predominance in atopic diseases is due to preferential apoptosis of circulating memory/effector Th1 cells. FASEB J. 17:1026-1035.
30. Messi, M., I. Giacchetto, K. Nagata, A. Lanzavecchia, G. Natoli, and F. Sallusto. 2003. Memory and flexibility of cytokine gene expression as separable properties of human T(H)1 and T(H)2 lymphocytes. Nat. Immunol. 4:78-86.
31. Sundrud, M.S., S.M. Grill, D. Ni, K. Nagata, S.S. Alkan, A. Subramaniam, and D. Unutmaz. 2003. Genetic reprogramming of primary human T cells reveals functional plasticity in Th cell differentiation. J. Immunol. 171:3542-3549.
32. + regulatory T cells in vivo. J. Exp. Med. 198:249-258.
33. Read, S., and F. Powrie. 2001. CD4(+) regulatory T cells. Curr. Opin. Immunol. 13:644-649.
34. + T regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J. Exp. Med. 193:1295-1302.
35. Akdis, C.A., and K. Blaser. 1999. IL-10 induced anergy in peripheral T cell and reactivation by microenvironmental cytokines: two key steps in specific immunotherapy. FASEB J. 13:603-609.
36. Bacchetta, R., C. Sartirana, M.K. Levings, C. Bordignon, S. Narula, and M.G. Roncarolo. 2002. Growth and expansion of human T regulatory type 1 cells are independent from TCR activation but require exogenous cytokines. Eur. J. Immunol. 32:2237-2245.
37. Moore, K.W., R. de Waal Malefyt, R.L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19:683-765.
38. Wakkach, A., N. Fournier, V. Brun, J.-P. Breittmayer, F. Cottrez, and H. Groux. 2003. Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity. 18:605-617.
39. Akbari, O., R.H. DeKruyff, and D.T. Umetsu. 2001. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2:725-731.
40. + regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med. 192:303-310.
41. + regulatory cells that control intestinal inflammation. J. Exp. Med. 192:295-302.
42. Nishimura, H., M. Nose, H. Hiai, N. Minato, and T. Honjo. 1999. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity. 11:141-151.
43. Carter, L., L.A. Fouser, J. Jussif, L. Fitz, B. Deng, C.R. Wood, M. Collins, T. Honjo, G.J. Freeman, and B.M. Carreno. 2002. PD-1:PD-L inhibitory pathway affects both CD4(+) and CD8(+) T cells and is overcome by IL-2. Eur. J. Immunol. 32:634-643.