IFN-γ attenuates antigen-induced overall immune response in the airway as a Th1-type immune regulatory cytokine

Journal of Immunology

Volumn 183, Issue 1, 2009, Pages 209-220

  Nakagome, Kazuyuki ^a   Okunishi, Katsuhide ^a   Imamura, Mitsuru ^a   Harada, Hiroaki ^a   Matsumoto, Taku ^a   Tanaka, Ryoichi ^a   Miyazaki, Jun Ichi ^b   Yamamoto, Kazuhiko ^a   Dohi, Makoto ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN P 15095; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 5; OVALBUMIN; PLASMID VECTOR; RECOMBINANT GAMMA INTERFERON; TRANSCRIPTION FACTOR FOXP3; ANTIGEN; CYTOKINE; GAMMA INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRONCHUS MUCUS; CD4+ T LYMPHOCYTE; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME LINKED IMMUNOSPOT ASSAY; EOSINOPHILIA; GENE TARGETING; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; MALE; MOUSE; MUCUS SECRETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SENSITIZATION; TH1 CELL; TH17 CELL; ANIMAL; ANTIGEN PRESENTING CELL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DRUG ANTAGONISM; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; PHYSIOLOGY; PLASMID; RESPIRATORY TRACT ALLERGY; TRANSGENIC MOUSE;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS; ANTIGENS, CD11C; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOKINES; INTERFERON-GAMMA; LUNG; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; OVALBUMIN; PLASMIDS; RESPIRATORY HYPERSENSITIVITY; TH1 CELLS;

EID: 68949132856     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0802712     Document Type: Article

References (64)

1. Bochner, B. S., B. J. Undem, and L. M. Lichtenstein. 1994. Immunological aspects of allergic asthma. Annu. Rev. Immunol. 12: 295-335.
2. Randolph, D. A., R. Stephens, C. J. Carruthers, and D. D. Chaplin. 1999. Cooperation between Th1 and Th2 cells in a murine model of eosinophilic airway inflammation. J. Clin. Invest. 104: 1021-1029.
3. Randolph, D. A., C. J. Carruthers, S. J. Szabo, K. M. Murphy, and D. D. Chaplin. 1999. Modulation of airway inflammation by passive transfer of allergen-specific Th1 and Th2 cells in a mouse model of asthma. J. Immunol. 162: 2375-2383.
4. Sugimoto, T., Y. Ishikawa, T. Yoshimoto, N. Hayashi, J. Fujimoto, and K. Nakanishi. 2004. Interleukin 18 acts on memory T helper cells type 1 to induce airway inflammation and hyperresponsiveness in a naive host mouse. J. Exp. Med. 199: 535-545.
5. Stephens, R., D. A. Randolph, G. Huang, M. J. Holtzman, and D. D. Chaplin. 2002. Antigen-nonspecific recruitment of Th2 cells to the lung as a mechanism for viral infection-induced allergic asthma. J. Immunol. 169: 5458-5467. (Pubitemid 35291643)
6. Linden, A. 2001. Role of interleukin-17 and the neutrophil in asthma. Int. Arch. Allergy Immunol. 126: 179-184.
7. Schnyder-Candrian, S., D. Togbe, I. Couillin, I. Mercier, F. Brombacher, V. Quesniaux, F. Fossiez, B. Ryffel, and B. Schnyder. 2006. Interleukin-17 is a negative regulator of established allergic asthma. J. Exp. Med. 203: 2715-2725.
8. Barczyk, A., W. Pierzchala, and E. Sozanska. 2003. Interleukin-17 in sputum correlates with airway hyperresponsiveness to methacholine. Respir. Med. 97: 726-733.
9. Laan, M., Z. H. Cui, H. Hoshino, J. Lotvall, M. Sjostrand, D. C. Gruenert, B. E. Skoogh, and A. Linden. 1999. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J. Immunol. 162: 2347-2352.
10. Holgate, S. T., and R. Polosa. 2006. The mechanisms, diagnosis, and management of severe asthma in adults. Lancet 368: 780-793.
11. 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.
12. H17 cell-mediated neutrophil recruitment into the airways. J. Allergy Clin. Immunol. 119: 662-670.
13. Ziegler, S. F., and Y. J. Liu. 2006. Thymic stromal lymphopoietin in normal and pathogenic T cell development and function. Nat. Immunol. 7: 709-714.
14. Bradley, L. M., D. K. Dalton, and M. Croft. 1996. A direct role for IFN-γ in regulation of Th1 cell development. J. Immunol. 157: 1350-1358.
15. Fernandez-Botran, R., V. M. Sanders, T. R. Mosmann, and E. S. Vitetta. 1988. Lymphokine-mediated regulation of the proliferative response of clones of T helper 1 and T helper 2 cells. J. Exp. Med. 168: 543-558.
16. Belosevic, M., D. S. Finbloom, P. H. Van Der Meide, M. V. Slayter, and C. A. Nacy. 1989. Administration of monoclonal anti-IFN-γ antibodies in vivo abrogates natural resistance of C3H/HeN mice to infection with Leishmania major. J. Immunol. 143: 266-274. (Pubitemid 19174230)
17. Scott, P. 1991. IFN-γ modulates the early development of Th1 and Th2 responses in a murine model of cutaneous leishmaniasis. J. Immunol. 147: 3149-3155.
18. Chu, C. Q., S. Wittmer, and D. K. Dalton. 2000. Failure to suppress the expansion of the activated CD4 T cell population in interferon γ-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J. Exp. Med. 192: 123-128.
19. Ferber, I. A., S. Brocke, C. Taylor-Edwards, W. Ridgway, C. Dinisco, L. Steinman, D. Dalton, and C. G. Fathman. 1996. Mice with a disrupted IFN-γ gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 156: 5-7.
20. Nakajima, H., H. Takamori, Y. Hiyama, and W. Tsukada. 1990. The effect of treatment with interferon-γ on type II collagen-induced arthritis. Clin. Exp. Immunol. 81: 441-445. (Pubitemid 20273670)
21. Chu, C. Q., D. Swart, D. Alcorn, J. Tocker, and K. B. Elkon. 2007. Interferon-γ regulates susceptibility to collagen-induced arthritis through suppression of interleukin-17. Arthritis Rheum. 56: 1145-1151.
22. Weaver, C. T., R. D. Hatton, P. R. Mangan, and L. E. Harrington. 2007. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25: 821-852.
23. Li, X. M., R. K. Chopra, T. Y. Chou, B. H. Schofield, M. Wills-Karp, and S. K. Huang. 1996. Mucosal IFN-γ gene transfer inhibits pulmonary allergic responses in mice. J. Immunol. 157: 3216-3219.
24. + T cells. J. Exp. Med. 177: 573-576.
25. Stock, P., O. Akbari, G. Berry, G. J. Freeman, R. H. Dekruyff, and D. T. Umetsu. 2004. Induction of T helper type 1-like regulatory cells that express Foxp3 and protect against airway hyper-reactivity. Nat. Immunol. 5: 1149-1156.
26. Nakagome, K., M. Dohi, K. Okunishi, Y. Komagata, K. Nagatani, R. Tanaka, J. Miyazaki, and K. Yamamoto. 2005. In vivo IL-10 gene delivery suppresses airway eosinophilia and hyperreactivity by down-regulating APC functions and migration without impairing the antigen-specific systemic immune response in a mouse model of allergic airway inflammation. J. Immunol. 174: 6955-6966.
27. Nakagome, K., M. Dohi, K. Okunishi, R. Tanaka, T. Kouro, M. R. Kano, K. Miyazono, J. Miyazaki, K. Takatsu, and K. Yamamoto. 2007. IL-5-induced hypereosinophilia suppresses the antigen-induced immune response via a TGF-β-dependent mechanism. J. Immunol. 179: 284-294.
28. Okunishi, K., M. Dohi, K. Nakagome, R. Tanaka, S. Mizuno, K. Matsumoto, J. Miyazaki, T. Nakamura, and K. Yamamoto. 2005. A novel role of hepatocyte growth factor as an immune regulator through suppressing dendritic cell function. J. Immunol. 175: 4745-4753.
29. Nakagome, K., M. Dohi, K. Okunishi, R. Tanaka, J. Miyazaki, and K. Yamamoto. 2006. In vivo IL-10 gene delivery attenuates bleomycin induced pulmonary fibrosis by inhibiting the production and activation of TGF-β in the lung. Thorax 61: 886-894.
30. Jiang, J., E. Yamato, and J. Miyazaki. 2001. Intravenous delivery of naked plasmid DNA for in vivo cytokine expression. Biochem. Biophys. Res. Commun. 289: 1088-1092.
31. Dalton, D. K., L. Haynes, C. Q. Chu, S. L. Swain, and S. Wittmer. 2000. Interferon γ eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J. Exp. Med. 192: 117-122.
32. + T cells during mycobacterial infection to promote apoptosis by inducing components of the intracellular apoptosis machinery and by inducing extracellular proapoptotic signals. J. Immunol. 179: 939-949.
33. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299: 1057-1061.
34. Zou, W. 2006. Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 6: 295-307.
35. Refaeli, Y., L. Van Parijs, S. I. Alexander, and A. K. Abbas. 2002. Interferon γ is required for activation-induced death of T lymphocytes. J. Exp. Med. 196: 999-1005.
36. Shimozato, O., J. R. Ortaldo, K. L. Komschlies, and H. A. Young. 2002. Impaired NK cell development in an IFN-γ transgenic mouse: aberrantly expressed IFN-γ enhances hematopoietic stem cell apoptosis and affects NK cell differentiation. J. Immunol. 168: 1746-1752. (Pubitemid 34135773)
37. Qin, H. Y., P. Chaturvedi, and B. Singh. 2004. In vivo apoptosis of diabetogenic T cells in NOD mice by IFN-γ/TNF-α. Int. Immunol. 16: 1723-1732.
38. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
39. Lambrecht, B. N., and H. Hammad. 2003. Taking our breath away: dendritic cells in the pathogenesis of asthma. Nat. Rev. Immunol. 3: 994-1003.
40. + dendritic cells during allergen challenge abrogates the characteristic features of asthma. J. Exp. Med. 201: 981-991.
41. Kool, M., T. Soullié, M. van Nimwegen, M. A. Willart, F. Muskens, S. Jung, H. C. Hoogsteden, H. Hammad, and B. N. Lambrecht. 2008. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J. Exp. Med. 205: 869-882.
42. Adikari, S. B., H. Lian, H. Link, Y. M. Huang, and B. G. Xiao. 2004. Interferon-γ-modified dendritic cells suppress B cell function and ameliorate the development of experimental autoimmune myasthenia gravis. Clin. Exp. Immunol. 138: 230-236.
43. Shinomiya, M., S. M. Fazle-Akbar, H. Shinomiya, and M. Onji. 1999. Transfer of dendritic cells (DC) ex vivo stimulated with interferon-γ (IFN-γ) down-modulates autoimmune diabetes in non-obese diabetic (NOD) mice. Clin. Exp. Immunol. 117: 38-43.
44. Xiao, B. G., X. C. Wu, J. S. Yang, L. Y. Xu, X. Liu, Y. M. Huang, B. Bjelke, and H. Link. 2004. Therapeutic potential of IFN-γ-modified dendritic cells in acute and chronic experimental allergic encephalomyelitis. Int. Immunol. 16: 13-22.
45. Hofstra, C. L., I. Van Ark, G. Hofman, F. P. Nijkamp, P. M. Jardieu, and A. J. Van Oosterhout. 1998. Differential effects of endogenous and exogenous interferon-γ on immunoglobulin E, cellular infiltration, and airway responsiveness in a murine model of allergic asthma. Am. J. Respir. Cell Mol. Biol. 19: 826-835.
46. + Tregs. J. Clin. Invest. 116: 2434-2441.
47. Foulds, K. E., M. J. Rotte, M. A. Paley, B. Singh, D. C. Douek, B. J. Hill, J. J. O'Shea, W. T. Watford, R. A. Seder, and C. Y. Wu. 2008. IFN-γ mediates the death of Th1 cells in a paracrine manner. J. Immunol. 180: 842-849.
48. Feuerer, M., K. Eulenburg, C. Loddenkemper, A. Hamann, and J. Huehn. 2006. Self-limitation of Th1-mediated inflammation by IFN-γ. J. Immunol. 176: 2857-2863.
49. Pan, J., M. Zhang, J. Wang, Q. Wang, D. Xia, W. Sun, L. Zhang, H. Yu, Y. Liu, and X. Cao. 2004. Interferon-γ is an autocrine mediator for dendritic cell maturation. Immunol. Lett. 94: 141-151.
50. Akbar, S. M., K. Kajino, K. Tanimoto, K. Yamamura, M. Onji, and O. Hino. 1999. Unique features of dendritic cells in IFN-γ transgenic mice: relevance to cancer development and therapeutic implications. Biochem. Biophys. Res. Commun. 259: 294-299.
51. Sun, K., and D. W. Metzger. 2008. Inhibition of pulmonary antibacterial defense by interferon-γ during recovery from influenza infection. Nat. Med. 14: 558-564.
52. Arredouani, M. S., F. Franco, A. Imrich, A. Fedulov, X. Lu, D. Perkins, R. Soininen, K. Tryggvason, S. D. Shapiro, and L. Kobzik. 2007. Scavenger receptors SR-AI/II and MARCO limit pulmonary dendritic cell migration and allergic airway inflammation. J. Immunol. 178: 5912-5920.
53. Finkelman, F. D., J. Holmes, I. M. Katona, J. F. Urban, Jr., M. P. Beckmann, L. S. Park, K. A. Schooley, R. L. Coffman, T. R. Mosmann, and W. E. Paul. 1990. Lymphokine control of in vivo immunoglobulin isotype selection. Annu. Rev. Immunol. 8: 303-333.
54. Snapper, C. M., C. Peschel, and W. E. Paul. 1988. IFN-γ stimulates IgG2a secretion by murine B cells stimulated with bacterial lipopolysaccharide. J. Immunol. 140: 2121-2127.
55. Klinman, D. M. 1990. IgG1 and IgG2a production by autoimmune B cells treated in vitro with IL-4 and IFN-γ. J. Immunol. 144: 2529-2534.
56. Finkelman, F. D., I. M. Katona, T. R. Mosmann, and R. L. Coffman. 1988. IFN-γ regulates the isotypes of Ig secreted during in vivo humoral immune responses. J. Immunol. 140: 1022-1027.
57. Jaffe, H. A., R. Buhl, A. Mastrangeli, K. J. Holroyd, C. Saltini, D. Czerski, H. S. Jaffe, S. Kramer, S. Sherwin, and R. G. Crystal. 1991. Organ specific cytokine therapy: local activation of mononuclear phagocytes by delivery of an aerosol of recombinant interferon-γ to the human lung. J. Clin. Invest. 88: 297-302.
58. 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.
59. Hawrylowicz, C. M., and A. O'Garra. 2005. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat. Rev. Immunol. 5: 271-283.
60. Wark, P. A., S. L. Johnston, F. Bucchieri, R. Powell, S. Puddicombe, V. Laza-Stanca, S. T. Holgate, and D. E. Davies. 2005. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J. Exp. Med. 201: 937-947.
61. Contoli, M., S. D. Message, V. Laza-Stanca, M. R. Edwards, P. A. Wark, N. W. Bartlett, T. Kebadze, P. Mallia, L. A. Stanciu, H. L. Parker, et al. 2006. Role of deficient type III interferon-λ production in asthma exacerbations. Nat. Med. 12: 1023-1026.
62. Papadopoulos, N. G., L. A. Stanciu, A. Papi, S. T. Holgate, and S. L. Johnston. 2002. A defective type 1 response to rhinovirus in atopic asthma. Thorax 57: 328-332.
63. Brooks, G. D., K. A. Buchta, C. A. Swenson, J. E. Gern, and W. W. Busse. 2003. Rhinovirus-induced interferon-γ and airway responsiveness in asthma. Am. J. Respir. Crit. Care Med. 168: 1091-1094.
64. Gern, J. E., R. Vrtis, K. A. Grindle, C. Swenson, and W. W. Busse. 2000. Relationship of upper and lower airway cytokines to outcome of experimental rhinovirus infection. Am. J. Respir. Crit. Care Med. 162: 2226-2231.