Induction of tolerogenic lung CD4+ T cells by local treatment with a pSTAT-3 and pSTAT-5 inhibitor ameliorated experimental allergic asthma

International Immunology

Volumn 23, Issue 1, 2011, Pages 1-15

  Hausding, Michael ^a   Tepe, Marcus ^a   Übel, Caroline ^b   Lehr, Hans A ^c   Röhrig, Bernd ^a   Höhn, Yvonne ^a   Pautz, Andrea ^a   Eigenbrod, Tatjana ^a   Anke, Timm ^d   Kleinert, Hartmut ^a   Erkel, Gerhard ^d   Finotto, Susetta ^b  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

Experimental asthma; FoxP 3; IDO; SOCS 3; STAT 3; STAT 5; STAT 6; Tolerance

Indexed keywords

CD11 ANTIGEN; GALIELLALACTONE; GAMMA INTERFERON; GLYCOPROTEIN P 15095; IBWFA 111 95; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 3 RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 6; OVALBUMIN; PROTEIN INHIBITOR; RNA; SIGNAL TRANSDUCING ADAPTOR PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

AIRWAY; ALLERGIC ASTHMA; ALPHA CHAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DOSE RESPONSE; DOWN REGULATION; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG ISOLATION; EOSINOPHILIA; FEMALE; FERMENTATION; GENE EXPRESSION; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS CELL; MOUSE; MUCUS SECRETION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TH1 CELL; TREATMENT RESPONSE;

EID: 78650341401     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxq451     Document Type: Article

References (61)

1. Lambrecht, B. N., Pauwels, R. A. and Bullock, G. R. 1996. The dendritic cell: its potent role in the respiratory immune response. Cell Biol. Int. 20:111.
2. Walker, J. G., Ahern, M. J., Coleman, M. et al. 2007. Characterisation of a dendritic cell subset in synovial tissue which strongly expresses Jak/STAT transcription factors from patients with rheumatoid arthritis. Ann. Rheum. Dis. 66:992.
3. Stresemann, E. 1959. The dosage of dexamethasone and triamcinolone in bronchial asthma. Lancet 2:257.
4. Mainali, E. S., Kikuchi, T. and Tew, J. G. 2005. Dexamethasone inhibits maturation and alters function of monocyte-derived dendritic cells from cord blood. Pediatr. Res. 58:125.
5. Ma, W., Gee, K., Lim, W. et al. 2004. Dexamethasone inhibits IL-12p40 production in lipopolysaccharide-stimulated human monocytic cells by down-regulating the activity of c-Jun N-terminal kinase, the activation protein-1, and NF-kappa B transcription factors. J. Immunol. 172:318.
6. Linden, M. and Brattsand, R. 1994. Effects of a corticosteroid, budesonide, on alveolar macrophage and blood monocyte secretion of cytokines: differential sensitivity of GM-CSF, IL-1 beta, and IL-6. Pulm. Pharmacol. 7:43.
7. Maroof, A., Penny, M., Kingston, R. et al. 2006. Interleukin-4 can induce interleukin-4 production in dendritic cells. Immunology 117:271.
8. Suto, A., Nakajima, H., Tokumasa, N. et al. 2005. Murine plasmacytoid dendritic cells produce IFN-gamma upon IL-4 stimulation. J. Immunol. 175:5681.
9. Homma, T., Kato, A., Hashimoto, N. et al. 2004. Corticosteroid and cytokines synergistically enhance toll-like receptor 2 expression in respiratory epithelial cells. Am. J. Respir. Cell Mol. Biol. 31:463.
10. Barton, B. E. 2006. STAT3: a potential therapeutic target in dendritic cells for the induction of transplant tolerance. Expert. Opin. Ther. Targets. 10:459.
11. Akbari, O., DeKruyff, R. H. and Umetsu, D. T. 2001. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2:725.
12. Doganci, A., Eigenbrod, T., Krug, N. et al. 2005. The IL-6R alpha chain controls lung CD4+CD25+ Treg development and function during allergic airway inflammation in vivo. J. Clin. Invest. 115:313.
13. Kopcke, B., Johansson, M., Sterner, O. and Anke, H. 2002. Biologically active secondary metabolites from the ascomycete A111-95. 1. Production, isolation and biological activities. J. Antibiot. (Tokyo) 55:36.
14. Weidler, M., Rether, J., Anke, T. and Erkel, G. 2000. Inhibition of interleukin-6 signaling by galiellalactone. FEBS Lett. 484:1.
15. Seki, Y., Inoue, H., Nagata, N. et al. 2003. SOCS-3 regulates onset and maintenance of T(H)2-mediated allergic responses. Nat. Med. 9:1047.
16. Suzuki, A., Hanada, T., Mitsuyama, K. et al. 2001. CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J. Exp. Med. 193:471.
17. Eljaafari, A., Li, Y. P. and Miossec, P. 2009. IFN-gamma, as secreted during an alloresponse, induces differentiation of monocytes into tolerogenic dendritic cells, resulting in FoxP3+ regulatory T cell promotion. J. Immunol. 183:2932.
18. Takeda, K., Kaisho, T., Yoshida, N., Takeda, J., Kishimoto, T. and Akira, S. 1998. Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: generation and characterization of Tcell-specific Stat3-deficient mice. J. Immunol. 161:4652.
19. Hausding, M., Ho, I. C., Lehr, H. A. et al. 2004. A stage-specific functional role of the leucine zipper transcription factor c-Maf in lung Th2 cell differentiation. Eur. J. Immunol. 34:3401.
20. Maxeiner, J. H., Karwot, R., Hausding, M., Sauer, K. A., Scholtes, P. and Finotto, S. 2007. A method to enable the investigation of murine bronchial immune cells, their cytokines and mediators. Nat. Protoc. 2:105.
21. Finotto, S., Hausding, M., Doganci, A. et al. 2005. Asthmatic changes in mice lacking T-bet are mediated by IL-13. Int. Immunol. 17:993.
22. Finotto, S., Neurath, M. F., Glickman, J. N. et al. 2002. Development of spontaneous airway changes consistent with human asthma in mice lacking T-bet. Science 295:336.
23. Hausding, M., Karwot, R., Scholtes, P. et al. 2007. Lung CD11c+ cells from mice deficient in Epstein-Barr virus-induced gene 3 (EBI-3) prevent airway hyper-responsiveness in experimental asthma. Eur. J. Immunol. 37:1663.
24. Sauer, K. A., Scholtes, P., Karwot, R. and Finotto, S. 2006. Isolation of CD4+ T cells from murine lungs: a method to analyze ongoing immune responses in the lung. Nat. Protoc. 1:2870.
25. Doganci, A., Karwot, R., Maxeiner, J. H. et al. 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.
26. Karwot, R., Maxeiner, J. H., Schmitt, S. et al. 2008. Protective role of nuclear factor of activated T cells 2 in CD8+ long-lived memory T cells in an allergy model. J. Allergy Clin. Immunol. 121:992.
27. Maxeiner, J. H., Karwot, R., Sauer, K. et al. 2009. A key regulatory role of the transcription factor NFATc2 in bronchial adenocarcinoma via CD8+ T lymphocytes. Cancer Res. 69:3069.
28. Cohen, J. 1994. The earth is round (p < 0.5). Am Psychol. 49:997.
29. Mellor, A. L., Chandler, P., Baban, B. et al. 2004. Specific subsets of murine dendritic cells acquire potent T cell regulatory functions following CTLA4-mediated induction of indoleamine 2,3 dioxygenase. Int. Immunol. 16:1391.
30. Burchell, J. T., Wikstrom, M. E., Stumbles, P. A., Sly, P. D. and Turner, D. J. 2009. Attenuation of allergen-induced airway hyperresponsiveness is mediated by airway regulatory T cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 296:L307.
31. Presser, K., Schwinge, D., Wegmann, M. et al. 2008. Coexpression of TGF-beta1 and IL-10 enables regulatory T cells to completely suppress airway hyperreactivity. J. Immunol. 181:7751.
32. Kimura, A., Naka, T. and Kishimoto, T. 2007. IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc. Natl Acad. Sci. U S A 104:12099.
33. Bettelli, E., Carrier, Y., Gao, W. et al. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441:235.
34. Eljaafari, A., Van Snick, J., Voisin, A. et al. 2006. Alloreaction increases or restores CD40, CD54, and/or HLA molecule expression in acute myelogenous leukemia blasts, through secretion of inflammatory cytokines: dominant role for TNFbeta, in concert with IFNgamma. Leukemia 20:1992.
35. Takatori, H., Nakajima, H., Kagami, S. et al. 2005. Stat5a inhibits IL-12-induced Th1 cell differentiation through the induction of suppressor of cytokine signaling 3 expression. J. Immunol. 174:4105.
36. Chen, Z., Laurence, A., Kanno, Y. et al. 2006. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc. Natl Acad. Sci. U S A 103:8137.
37. Yanagawa, Y., Iwabuchi, K. and Onoe, K. 2009. Co-operative action of interleukin-10 and interferon-gamma to regulate dendritic cell functions. Immunology 127:345.
38. Kuikka, L., Reijonen, T., Remes, K. and Korppi, M. 1994. Bronchial asthma after early childhood wheezing: a follow-up until 4.5-6 years of age. Acta Paediatr. 83:744.
39. Pinkerton, H. H. Jr. and Van Metre, T. E. Jr. 1958. Immediate therapy for the acute attack of asthma; a comparison of epinephrine and orally and intravenously administered prednisolone. N. Engl. J. Med. 258:363.
40. Eggleston, P. A. 1997. Allergen-specific immunotherapy in childhood asthma. Curr. Opin. Pediatr. 9:582.
41. Adcock, I. M., Shirasaki, H., Gelder, C. M., Peters, M. J., Brown, C. R. and Barnes, P. J. 1994. The effects of glucocorticoids on phorbol ester and cytokine stimulated transcription factor activation in human lung. Life Sci. 55:1147.
42. Komlosi, Z. I., Pozsonyi, E., Tabi, T. et al. 2006. Lipopolysaccharide exposure makes allergic airway inflammation and hyperresponsiveness less responsive to dexamethasone and inhibition of iNOS. Clin. Exp. Allergy. 36:951.
43. Stock, P., Akbari, O., DeKruyff, R. H. and Umetsu, D. T. 2005. Respiratory tolerance is inhibited by the administration of corticosteroids. J. Immunol. 175:7380.
44. Seidel, H. M., Milocco, L. H., Lamb, P., Darnell, J. E. Jr., Stein, R. B. and Rosen, J. 1995. Spacing of palindromic half sites as a determinant of selective STAT (signal transducers and activators of transcription) DNA binding and transcriptional activity. Proc. Natl Acad. Sci. U S A 92:3041.
45. Shu, S. A., Lian, Z. X., Chuang, Y. H. et al. 2007. The role of CD11c(+) hepatic dendritic cells in the induction of innate immune responses. Clin. Exp. Immunol. 149:335.
46. Ettmayer, P., Mayer, P., Kalthoff, F. et al. 2006. A novel low molecular weight inhibitor of dendritic cells and B cells blocks allergic inflammation. Am. J. Respir. Crit. Care Med. 173:599.
47. Finotto, S., Eigenbrod, T., Karwot, R. et al. 2007. Local blockade of IL-6R signaling induces lung CD4+ T cell apoptosis in a murine model of asthma via regulatory T cells. Int. Immunol. 19:685.
48. Schnyder-Candrian, S., Togbe, D., Couillin, I. et al. 2006. Interleukin-17 is a negative regulator of established allergic asthma. J. Exp. Med. 203:2715.
49. Pichavant, M., Goya, S., Meyer, E. H. et al. 2008. Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17. J. Exp. Med. 205:385.
50. Nakae, S., Lunderius, C., Ho, L. H., Schafer, B., Tsai, M. and Galli, S. J. 2007. TNF can contribute to multiple features of ovalbumin-induced allergic inflammation of the airways in mice. J. Allergy Clin. Immunol. 119:680.
51. Wong, C. K., Ho, C. Y., Ko, F. W. et al. 2001. Proinflammatory cytokines (IL-17, IL-6, IL-18 and IL-12) and Th cytokines (IFNgamma, IL-4, IL-10 and IL-13) in patients with allergic asthma. Clin. Exp. Immunol. 125:177.
52. Nakae, S., Komiyama, Y., Nambu, A. et al. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17:375.
53. Teunissen, M. B., Koomen, C. W., de Waal Malefyt, R., Wierenga, E. A. and Bos, J. D. 1998. Interleukin-17 and interferon-gamma synergize in the enhancement of proinflammatory cytokine production by human keratinocytes. J. Invest. Dermatol. 111:645.
54. Umemura, M., Yahagi, A., Hamada, S. et al. 2007. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 178:3786.
55. Maitra, U., Davis, S., Reilly, C. M. and Li, L. 2009. Differential regulation of Foxp3 and IL-17 expression in CD4 T helper cells by IRAK-1. J. Immunol. 182:5763.
56. Gao, H. and Ward, P. A. 2007. STAT3 and suppressor of cytokine signaling 3: potential targets in lung inflammatory responses. Expert Opin. Ther Targets 11:869.
57. Pillemer, B. B., Xu, H., Oriss, T. B., Qi, Z. and Ray, A. 2007. Deficient SOCS3 expression in CD4+CD25+FoxP3+ regulatory T cells and SOCS3-mediated suppression of Treg function. Eur. J. Immunol. 37:2082.
58. Radojcic, V., Pletneva, M. A., Yen, H. R. et al. 2007. STAT3 signaling in CD4+ T cells is critical for the pathogenesis of chronic sclerodermatous graft-versus-host disease in a murine model. J. Immunol. 184:764.
59. Pallandre, J. R., Brillard, E., Crehange, G. et al. 2007. Role of STAT3 in CD4+CD25+FOXP3+ regulatory lymphocyte generation: implications in graft-versus-host disease and antitumor immunity. J. Immunol. 179:7593.
60. Kortylewski, M., Xin, H., Kujawski, M. et al. 2009. Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment. Cancer Cell 15:114.
61. Stewart, C. A. and Trinchieri, G. 2009. Reinforcing suppression using regulators: a new link between STAT3, IL-23, and Tregs in tumor immunosuppression. Cancer Cell 15:81