Development of eosinophilic airway inflammation and airway hyperresponsiveness requires interleukin-5 but not immunoglobulin E or B lymphocytes

American Journal of Respiratory Cell and Molecular Biology

Volumn 21, Issue 4, 1999, Pages 480-489

  Hamelmann, Eckard ^a   Takeda, Katsuyuki ^a   Schwarze, Jurgen ^a   Vella, Anthony T ^a   Irvin, Charles G ^a   Gelfand, Erwin W ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; CYTOKINE; IMMUNOGLOBULIN E; INTERLEUKIN 5; OVALBUMIN;

ANIMAL; ARTICLE; ASTHMA; B LYMPHOCYTE; BIOSYNTHESIS; BRONCHUS HYPERREACTIVITY; C57BL MOUSE; DISEASE MODEL; DRUG ANTAGONISM; EOSINOPHILIA; FEMALE; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; MOUSE MUTANT; PATHOLOGY; T LYMPHOCYTE;

ALLERGENS; ANIMALS; ASTHMA; B-LYMPHOCYTES; BRONCHIAL HYPERREACTIVITY; CYTOKINES; DISEASE MODELS, ANIMAL; EOSINOPHILIA; FEMALE; HUMANS; IMMUNOGLOBULIN E; INTERLEUKIN-5; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OVALBUMIN; T-LYMPHOCYTES;

EID: 0033208621     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/ajrcmb.21.4.3659     Document Type: Article

References (36)

1. Arm, J. P., and T. H. Lee. 1992. The pathobiology of bronchial asthma. Adv. Immunol. 51:323-382.
2. Burrows, B., F. D. Martinez, M. Halonen, R. A. Barbee, and M. G. Cline. 1989. Association of asthma with serum IgE levels and skin-test reactivity to allergens. N. Engl. J. Med. 320:271-277.
3. Sears, M. R., B. Burrows, E. M. Flannery, G. P. Herbison, C. J. Hewitt, and M. D. Holdaway. 1991. Relation between airway responsiveness and serum IgE in children with asthma and in apparently normal children. N. Engl. J. Med. 325:1067-1071.
4. Coyle, A. J., K. Wagner, C. Bertrand, S. Tsuyuki, J. Bews, and C. H. Heusser. 1996. Central role of IgE in the induction of lung eosinophil infiltration and T helper 2 cell cytokine production: inhibition by a non-anaphylactogenic anti-IgE antibody. J. Exp. Med. 183:1303-1310.
5. Eum, S. Y., S. Haile, J. Lefort, M. Huerre, and B. B. Vargaflig. 1995. Eosinophil recruitment into the respiratory epithelium following antigenic challenge in hyper-IgE mice is accompanied by interleukin 5-dependent bronchial hyperresponsiveness. Proc. Natl. Acad. Sci. USA 92:12290-12294.
6. Corry, D. B., H. G. Folkesson, M. L Warnock, D. J. Erle, M. A. Matthay, J. P. Wiener-Kronish, and R. M. Locksley. 1996. Interleukin-4, but not interleukin-5 or eosinophils, is required in a murine model of acute airway hyper-reactivity. J. Exp. Med. 183:109-117.
7. Brusselle, G., J. Kips, G. Joos, H. Blucthmann, and R. Pauwels. 1995. Allergen-induced airway inflammation and bronchial responsiveness in wild-type and interleukin-4-deficient mice. Am. J. Respir. Cell Mol. Biol. 12: 254-259.
8. Coyle, A. J., G. Le Gros, C. Bertrand, S. Tsuyuki, C. H. Heusser, M. Kopf, and G. P. Anderson. 1995. Interleukin-4 is required for the induction of lung Th2 mucosal immunity. Am. J. Respir. Cell Mol. Biol. 13:54-59.
9. Bousquet, J., P. Chanez, J. Y. Lacoste, G. Barneon, N. Ghavanian, I. Enander, P. Venge, S. Ahlstedt, J. Simony-Lafontaine, P. Godard, and F. B. Michel. 1990. Eosinophilic inflammation in asthma. N. Engl. J. Med. 323:1033-1039.
10. Holgate, S. T., W. R. Roche, and M. K. Church. 1991. The role of the eosinophil in asthma. Am. Rev. Respir. Dis. 143:S66-S70.
11. Kay, A.B. 1991. Eosinophils and asthma. N. Engl. J. Med. 324:1514-1515.
12. Corrigan, C. J., and A. B. Kay. 1992. T cells and eosinophils in the pathogenesis of asthma. Immunol. Today 13:501-507.
13. Hamelmann, E., A. Oshiba, J. Loader, G. L. Larsen, G. J. Gleich, J. J. Lee, and E. W. Gelfand. 1997. Anti-interleukin-5 antibody prevents airway hyperresponsiveness in a murine model of airway sensitization. Am. J. Respir. Crit. Care Med. 155:819-825.
14. Foster, P. S., S. P. Hogan, A. J. Ramsay, K. I. Matthaci, and I. G. Young. 1996. Interleukin 5 deficiency abolishes eosinophilia, airway hyperreactivity, and lung damage in a mouse asthma model. J. Exp. Med. 183:195-201.
15. Kitamura, D., J. Roes, R. Kuhn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350:423-426.
16. Epstein, M. M., F. Di Rosa, D. Jankovic, A. Sher, and P. Matzinger. 1995. Successful T-cell priming in B-cell-deficient mice. J. Exp. Med. 182:915-922.
17. Phillips, J. A., C. G. Romball, M. V. Hobbs, D. N. Ernst, L. Shultz, and D. O. Weigle. 1996. CD4+ T-cell activation and tolerance induction in B-cell knockout mice. J. Exp. Med. 183:1339-1344.
18. Di Rosa, F., and P. Matzinger. 1996. Long-lasting CD8 T-cell memory in the absence of CD4 T cells and B cells. J. Exp. Med. 183:2153-2163.
19. Hamelmann, E., A. T. Vella, A. Oshiba, P. Marrack, J. W. Kappler, and E. W. Gelfand. 1997. Allergic airway sensitization induces T-cell activation but not airway hyperresponsiveness in B-cell deficient mice. Proc. Natl. Acad. Sci. USA 94:1350-1355.
20. Oshiba, A., E. Hamelmann, K. Takeda, K. L. Bradley, J. E. Loader, G. L. Larsen, and E. W. Gelfand. 1996. Passive transfer of immediate hypersensitivity and airway hyperresponsiveness by allergen-specific IgE and IgG1 in mice. J. Clin. Invest. 97:1398-1408.
21. Larsen, G. L., H. Renz, J. E. Loader, K. L. Bradley, and E. W. Gelfand. 1992. Airway response to electrical field stimulation in sensitized inbred mice. Passive transfer of increased responsiveness with peribronchial lymph nodes. J. Clin. Invest. 89:747-752.
22. Takeda, K., E. Hamelmann, A. Joetham, C. G. Irvin, L. Shultz, and E. W. Gelfand. 1997. Development of eosinophilic airway inflammation and airway hyperresponsiveness in allergen sensitised mast cell-deficient mice. J. Exp. Med. 186:449-454.
23. Renz, H., H. R. Smith, J. E. Henson, B. S. Ray, C. G. Irvin, and E. W. Gelfand. 1992. Aerosolized antigen exposure without adjuvant causes increased IgE production and increased airway responsiveness in the mouse. J. Allergy Clin. Immunol. 89:1127-1138.
24. Hamelmann, E., J. Schwarze, K. Takeda, A. Oshiba, and E. W. Gelfand. 1997. Noninvasive measurement of airway responsiveness in allergen sensitized mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 156:766-775.
25. Larson, G. L., T. M. Fame, H. Renz, J. E. Loader, J. Graves, M. Hill, and E. W. Gelfand. 1994. Increased acetylcholine release in tracheas from allergen-exposed IgE-immune mice. Am. J. Physiol. 266:L263-L270.
26. Vella, A. T., M. T. Scherer, L. Schultz, J. W. Kappler, and P. Marrack. 1996. B cells are not essential for peripheral T-cell tolerance. Proc. Natl. Acad. Sci. USA 93:951-955.
27. Robinson, D. S., Q. Hamid, S. Ying, A. Tsicopoulos, J. Barkans, A. M. Bentley, C. Corrigan, S. K. Durham, and A. B. Kay. 1992. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N. Engl. J. Med. 326:298-304.
28. Swain, S. L., A. D. Weinberg, M. English, and G. Huston. 1990. IL-4 directs the development of TH2-like helper/effectors. J. Immunol. 145:3796-3806.
29. Pene, J., F. Rousset, F. Briere, I. Chretien, J. Y. Bonnefoy, H. Spits, T. Yokota, N. Arai, K. Arai, J. Banchereau, and J. de Vries. 1988. IgE production by normal human lymphocytes is induced by interleukin-4 and suppressed by interferons gamma and alpha and prostaglandin E2. Proc. Natl. Acad. Sci. USA 85:6880-6884.
30. Renz, H., K. Enssle, L. Lauffer, R. Kurrle, and E. W. Gelfand. 1995. Inhibition of allergen-induced IgE and IgG1 production by soluble IL-4 receptor. Int. Arch. Allergy Immunol. 106:46-54.
31. Oettgen, H. C., T. R. Martin, B. A. Wynshaw, C. Deng, J. M. Drazen, and P. Leder. 1994. Active anaphylaxis in IgE-deficient mice. Nature 370:367-370.
32. Mehlhop, P. D., M. van de Rijn, A. B. Goldberg, J. P. Brewer, V. P. Kurup, T. R. Martin, and H. C. Oettgen. 1997. Allergen-induced bronchial hyper-reactivity and eosinophilic inflammation occur in the absence of IgE in a mouse model of asthma. Proc. Natl. Acad. Sci. USA 94:1344-1349.
33. Kaneko, M., M. C. Swanson, G. J. Gleich, and H. Kita. 1995. Allergen-specific IgG1 and IgG3 through Fc gamma RII induce eosinophil degranulation. J. Clin. Invest. 95:2813-2821.
34. Haezku, A., K. Takeda, E. Hamelmann, A. Oshiba, J. Loader, A. Joetham, C. Irvin, H. Kikutani, and E. W. Gelfand. 1997. CD23-deficient mice develop allergic airway hyperresponsiveness following sensitization with ovalbumin. Am. J. Respir. Crit. Care Med. 156:1945-1955.
35. Nigai, H., S. Yamaguchi, N. Inagaki, N. Tsuruoka, Y. Hitoshi, and K. Takatsu. 1993. Effect of anti-IL-5 monoclonal antibody on allergic bronchial eosinophilia and airway hyperresponsiveness in mice. Life Sci. 53: PL243-PL247.
36. Hamelmann, E., A. Oshiba, J. Schwarze, K. L. Bradley, J. E. Loader, G. L. Larsen, and E. W. Gelfand. 1997. Allergen-specific IgE and IL-5 are essential for the development of airway hyperresponsiveness. Am. J. Respir. Cell Mol. Biol. 16:674-682.