Interleukin 18 Acts on Memory T Helper Cells Type 1 to Induce Airway Inflammation and Hyperresponsiveness in a Naive Host Mouse

Journal of Experimental Medicine

Volumn 199, Issue 4, 2004, Pages 535-545

  Sugimoto, Takaaki ^a   Ishikawa, Yuriko ^a,b   Yoshimoto, Tomohiro ^a,b   Hayashi, Nobuki ^a,b   Fujimoto, Jiro ^a   Nakanishi, Kenji ^a,b  

^a HYOGO COLLEGE OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Bronchial asthma; IL 13; IL 18; IL 9; Th1

Indexed keywords

CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 13; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 9; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ALLERGY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; BRONCHUS HYPERREACTIVITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; FEMALE; HELPER CELL; IMMUNOREGULATION; IMMUNOSTIMULATION; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH2 CELL;

ANIMALS; BRONCHIAL HYPERREACTIVITY; CLONE CELLS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOLOGIC MEMORY; INFLAMMATION; INTERLEUKIN-18; MICE; MICE, INBRED BALB C; OVALBUMIN; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS; TH2 CELLS;

EID: 1242276212     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20031368     Document Type: Article

References (60)

1. Busse, W.W., and R.J. Lemanske. 2001. Asthma. N. Engl. J. Med. 344:350-362.
2. Davies, D.E., J. Wicks, R.M. Powell, S.M. Puddicombe, and S.T. Holgate. 2003. Airway remodeling in a asthma: new insights. J. Allergy Clin. Immunol. 111:215-225.
3. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyper-responsiveness. Annu. Rev. Immunol. 17:255-281.
4. Bochner, B.S., B.J. Undem, and L.M. Lichtenstein. 1994. Immunological aspects of allergic asthma. Annu. Rev. Immunol. 12:295-335.
5. Renauld, J.C. 2001. New insights into the role of cytokines in asthma. J. Clin. Pathol. 54:577-589.
6. Umetsu, D.T., J.J. McIntire, O. Akbari, C. Macaubas, and R.H. DeKruyff. 2002. Asthma: an epidemic of dysregulated immunity. Nat. Immunol. 3:715-720.
7. Elias, J.A., C.G. Lee, T. Zheng, B. Ma, R.J. Homer, and Z. Zhu. 2003. New insights into the pathogenesis of asthma. J. Clin. Invest. 111:291-297.
8. + T cells. Annu. Rev. Immunol. 12:635-673.
9. Hamelmann, E., and E.W. Gelfand. 2001. IL-5-induced airway eosinophilia-the key to asthma? Immunol. Rev. 179:182-191.
10. Mosmann, T.R., M.W. Bond, R.L. Coffman, J. Ohara, and W.E. Paul. 1986. T-cell and mast cell lines respond to B-cell stimulatory factor 1. Proc. Natl. Acad. Sci. USA. 83:5654-5658.
11. Hultner, L., C. Druez, J. Moeller, C. Uyttenhove, E. Schmitt, E. Rude, P. Dormer, and S.J. Van. 1990. Mast cell growth-enhancing activity (MEA) is structurally related and functionally identical to the novel mouse T cell growth factor P40/TCGFIII (interleukin 9). Eur. J. Immunol. 20:1413-1416.
12. Temann, U.A., G.P. Geba, J.A. Rankin, and R.A. Flavell. 1998. Expression of interleukin 9 in the lungs of transgenic mice causes airway inflammation, mast cell hyperplasia, and bronchial hyperresponsiveness. J. Exp. Med. 188:1307-1320.
13. Louahed, J., M. Toda, J. Jen, Q. Hamid, J.C. Renauld, R.C. Levitt, and N.C. Nicolaides. 2000. Interleukin-9 upregulates mucus expression in the airways. Am. J. Respir. Cell. Mol. Biol. 22:649-656.
14. Venneer, P.D., R. Harson, L.A. Einwalter, T. Moninger, and J. Zabner. 2003. Interleukin-9 induces goblet cell hyperplasia during repair of human airway epithelia. Am. J. Respir. Cell. Mol. Biol. 28:286-295.
15. McKenzie, G.J., A. Bancroft, R.K. Grencis, and A.N. McKenzie. 1998. A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr. Biol. 8:339-342.
16. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T.Y. Neben, C.L. Karp, and D.D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science. 282:2258-2261.
17. Grunig, G., M. Warnock, A.E. Wakil, R. Venkayya, F. Brombacher, D.M. Rennick, D. Sheppard, M. Mohrs, D.D. Donaldson, R.M. Locksley, et al. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science. 282:2261-2263.
18. Kuperman, D.A., X. Huang, L.L. Koth, G.H. Chang, G.M. Dolganov, Z. Zhu, J.A. Elias, D. Sheppard, and D.J. Erle. 2002. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat. Med. 8:885-889.
19. Wills-Karp, M., and M. Chiaramonte. 2003. Interleukin-13 in asthma. Curr. Opin. Pulm. Med. 9:21-27.
20. Ritz, S.A., M.R. Stampfli, D.E. Davies, S.T. Holgate, and M. Jordana. 2002. On the generation of allergic airway diseases: from GM-CSF to Kyoto. Trends Immunol. 23:396-402.
21. Del Prete, A. 1998. The concept of type-1 and type-2 helper T cells and their cytokines in humans. Int. Rev. Immunol. 16:427-455.
22. Barnes, P.J. 1999. Therapeutic strategies for allergic diseases. Nature. 402:B31-B38.
23. 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-γ. J. Immunol. 166:207-217.
24. Hansen, G., G. Berry, R.H. DeKruyff, and D.T. Umetsu. 1999. Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation. J. Clin. Invest. 103:175-183.
25. Randolph, D.A., C.J. Carruthers, SJ. 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.
26. Randolph, D.A., R. Stephens, CJ. 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.
27. Li, L., Y. Xia, A. Nguyen, L. Feng, and D. Lo. 1998. Th2-induced eotaxin expression and eosinophilia coexist with Th1 responses at the effector stage of lung inflammation. J. Immunol. 161:3128-3135.
28. Ford, J.G., D. Rennick, D.D. Donaldson, R. Venkayya, C. McArthur, E. Hansell, V.P. Kurup, M. Warnock, and G. Grunig. 2001. IL-13 and IFN-γ: interactions in lung inflammation. J. Immunol. 167:1769-1777.
29. Takaoka, A., Y. Tanaka, T. Tsuji, T. Jinushi, A. Hoshino, Y. Asakura, Y. Mita, K. Watanabe, S. Nakaike, Y. Togashi, et al. 2001. A critical role for mouse CXC chemokine(s) in pulmonary neutrophilia during Th type 1-dependent airway inflammation. J. Immunol. 167:2349-2353.
30. Okamura, H., H. Tsutsi, T. Komatsu, M. Yutsudo, A. Hakura, T. Tanimoto, K. Torigoe, T. Okura, Y. Nukada, K. Hattori, et al. 1995. Cloning of a new cytokine that induces IFN-γ production by T cells. Nature. 378:88-91.
31. Kohno, K., J. Kataoka, T. Ohtsuki, Y. Suemoto, I. Okamoto, M. Usui, M. Ikeda, and M. Kurimoto. 1997. IFN-gamma-inducing factor (IGIF) is a costimulatory factor on the activation of Th1 but not Th2 cells and exerts its effect independently of IL-12. J. Immunol. 158:1541-1550.
32. Okamura, H., H. Tsutsui, S. Kashiwamura, T. Yoshimoto, and K. Nakanishi. 1998. Interleukin-18: a novel cytokine that augments both innate and acquired immunity. Adv. Immunol. 70:281-312.
33. Yoshimoto, T., H. Tsutsui, K. Tominaga, K. Hoshino, H. Okamura, S. Akira, W.E. Paul, and K. Nakanishi. 1999. IL-18, although antiallergic when administered with IL-12, stimulates IL-4 and histamine release by basophils. Proc. Natl. Acad. Sci. USA. 96:13962-13966.
34. + T cells, IL-4 and STAT6. Nat. Immunol. 1:132-137.
35. + T cells in the induction of immunoglobulin E antibodies in response to interleukin 18 treatment of mice. J. Exp. Med. 197:997-1005.
36. Hoshino, T., R.-H. Wiltrout, and H.A. Young. 1999. IL-18 is a potent coinducer of IL-13 in NK and T cells: a new potential role for IL-18 in modulating the immune response. J. Immunol. 162:5070-5077.
37. Wild, J.S., A. Sigounas, N, Sur, M.S. Siddiqui, R. Alam, M. Kurimoto, and S. Sur. 2000. IFN-γ-inducing factor (IL-18) increases allergic sensitization, serum IgE, Th2 cytokines, and airway eosinophilia in a mouse model of allergic asthma. J. Immunol. 164:2701-2710.
38. Nakanishi, K., T. Yoshimoto, H. Tsutsui, and H. Okamura. 2001. Interleukin-18 regulates both Th1 and Th2 responses. Annu. Rev. Immunol. 19:423-474.
39. Takeuchi, M., Y. Nishizaki, O. Sano, T. Ohta, M. Ikeda, and M. Kurimoto. 1997. Immunohistochemical and immuno-electron-microscopic detection of interferon-γ-inducing factor ("interleukin-18") in mouse intestinal epithelial cells. Cell Tissue Res. 289:499-503.
40. Pizarro, T.T., M.H. Michie, M. Bentz, J. Woraratanadharm, M.J. Smith, E. Foley, C.A. Moskaluk, SJ. Bickston, and F. Cominelli. 1999. IL-18, a novel immunoregulatory cytokine, is up-regulated in Crohn's disease: expression and localization in intestinal mucosal cells. J. Immunol. 162:6829-6835.
41. Cameron, L.A., R.A. Taha, A. Tsicopoulos, M. Kurimoto, R. Olivenstein, B. Wallaert, E.M. Minshall, and Q.A. Hamid. 1999. Airway epithelium expresses interleukin-18. Eur. Respir. J. 14:553-559.
42. Sugawara, S., A. Uehara, T. Nochi, T. Yamaguchi, H. Ueda, A. Sugiyama, K. Hanzawa, K. Kumagai, H. Okamura, and H. Takada. 2001. Neutrophil proteinase 3-mediated induction of bioactive IL-18 secretion by human oral epithelial cells. J. Immunol. 167:6568-6575.
43. Abbas, A.K., K.M. Murphy, and A. Sher. 1996. Functional diversity of helper T lymphocytes. Nature. 383:787-793.
44. Yoshimoto, T., K. Takeda, T. Tanaka, K. Ohkusu, S. Kashiwamura, H. Okamura, S. Akira, and K. Nakanishi. 1998. IL-12 up-regulates IL-18 receptor expression on T cells, Th1 cells, and B cells: synergism with IL-18 for IFN-γ production. J. Immunol. 161:3400-3407.
45. Tominaga, K., T. Yoshimoto, K. Torigoe, M. Kurimoto, K. Matsui, T. Hada, H. Okamura, and K. Nakanishi. 2000. IL-12 synergizes with IL-18 or IL-1β for IFN-γ production from human T cells. Int. Immunol. 12:151-160.
46. lo thymocytes in vivo. Science. 250:1720-1723.
47. Hyodo, Y., K. Matsui, N. Hayashi, H. Tsutsui, S. Kashiwamura, H. Yamauchi, K. Hiroishi, K. Takeda, Y. Tagawa, Y. Iwakura, et al. 1999. IL-18 up-regulates perforin-mediated NK activity without increasing perforin messenger RNA expression by binding to constitutively expressed IL-18 receptor. J. Immunol. 162:1662-1668.
48. - T cells modify the MHC-restricted function of heterogeneous and cloned T suppressor cells. J. Exp. Med. 162:413-426.
49. Tamura, T., and H. Nariuchi. 1992. T cell activation through TCR/-CD3 complex. IL-2 production of T cell clones stimulated with anti-CD3 without cross-linkage. J. Immunol. 148:2370-2377.
50. Kaye, J., S. Porcelli, J. Tite, B. Jones, and C.J. Janeway. 1983. Both a monoclonal antibody and antisera specific for determinants unique to individual cloned helper T cell lines can substitute for antigen and antigen-presenting cells in the activation of T cells. J. Exp. Med. 158:836-856.
51. Hayashi, N., D. Liu, B. Min, S.S. Ben, and W.E. Paul. 2002. Antigen challenge leads to in vivo activation and elimination of highly polarized TH1 memory T cells. Proc. Natl. Acad. Sci. USA. 99:6187-6191.
52. Hamelmann, E., J. Schwarze, K. Takeda, A. Oshiba, G.L. Larsen, C.G. Irvin, and E.W. Gelfand. 1997. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care. Med. 156:766-775.
53. Luster, A.D. 1998. Chemokines-chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 12:436-445.
54. Urban, J.J., T.N. Noben, D.D. Donaldson, K.B. Madden, S.C. Morris, M. Collins, and F.D. Finkelman. 1998. IL-13, IL-4Rα, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity. 8:255-264.
55. Ray, A., and L. Cohn. 1999. Th2 cells and GATA-3 in asthma: new insights into the regulation of airway inflammation. J. Clin. Invest. 104:985-993.
56. Zhang, D.H., L. Yang, L. Cohn, L. Parkyn, R. Homer, P. Ray, and A. Ray. 1999. Inhibition of allergic inflammation in a murine model of asthma by expression of a dominant-negative mutant of GATA-3. Immunity. 11:473-482.
57. Finotto, S., S.G. De, H.A. Lehr, U. Herz, M. Buerke, M. Schipp, B. Bartsch, R. Atreya, E. Schmitt, P.R. Galle, et al. 2001. Treatment of allergic airway inflammation and hyperresponsiveness by antisense-induced local blockade of GATA-3 expression. J. Exp. Med. 193:1247-1260.
58. Gleich, G.J. 1990. The eosinophil and bronchial asthma: current understanding. J. Allergy. Clin. Immunol. 85:422-436.
59. Leckie, M.J., A. ten Brinke, J. Khan, Z. Diamant, B.J. O'Connor, C.M. Walls, A.K. Mathur, H.C. Cowley, K.F. Chung, R. Djukanovic, et al. 2000. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsiveness, and the late asthmatic response. Lancet. 356:2144-2148.
60. Kawakami, T., and S.J. Galli. 2002. Regulation of mast-cell and basophil function and survival by IgE. Nat. Rev. Immunol. 2:773-786.