Mast Cells, FcεRI, and IL-13 Are Required for Development of Airway Hyperresponsiveness after Aerosolized Allergen Exposure in the Absence of Adjuvant

Journal of Immunology

Volumn 172, Issue 10, 2004, Pages 6398-6406

  Taube, Christian ^a   Wei, Xudong ^a   Swasey, Christina H ^a   Joetham, Anthony ^a   Zarini, Simona ^a   Lively, Tricia ^a   Takeda, Katsuyuki ^a   Loader, Joan ^a   Miyahara, Nobuaki ^a   Kodama, Taku ^a   Shultz, Lenny D ^b   Donaldson, Debra D ^c   Hamelmann, Eckard H ^a   Dakhama, Azzeddine ^a   Gelfand, Erwin W ^a  

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

^b JACKSON LABORATORY   (United States)

^c PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; HYBRID PROTEIN; IMMUNOGLOBULIN E RECEPTOR; INTERLEUKIN 13; OVALBUMIN;

AEROSOL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BRONCHUS HYPERREACTIVITY; BRONCHUS MUSCLE; CELL HYPERPLASIA; CONTROLLED STUDY; ELECTROSTIMULATION; FEMALE; GOBLET CELL; HISTOPATHOLOGY; IMMUNOPATHOGENESIS; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; TRACHEA MUSCLE;

EID: 2442487763     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.10.6398     Document Type: Article

References (62)

1. Sporik, R., S. T. Holgate, T. A. Platts-Mills, and J. J. Cogswell. 1990. Exposure to house-dust mite allergen (Der p I) and the development of asthma in childhood: a prospective study. N. Engl. J. Med. 323:502.
2. Peat, J. K., E. Tovey, B. G. Toelle, M. M. Haby, E. J. Gray, A. Mahmic, and A. J. Woolcock. 1996. House dust mite allergens: a major risk factor for childhood asthma in Australia. Am. J. Respir. Crit. Care Med. 153:141.
3. Cartier, A., N. C. Thomson, P. A. Frith, R. Roberts, and F. E. Hargreave. 1982. Allergen-induced increase in bronchial responsiveness to histamine: relationship to the late asthmatic response and change in airway caliber. J. Allergy Clin. Immunol. 70:170.
4. Boulet, L. P., A. Cartier, N. C. Thomson, R. S. Roberts, J. Dolovich, and F. E. Hargreave. 1983. Asthma and increases in nonallergic bronchial responsiveness from seasonal pollen exposure. J. Allergy Clin. Immunol. 71:399.
5. Turner, H., and J. P. Kinet. 1999. Signalling through the high-affinity IgE receptor Fc epsilonRI. Nature 402:B24.
6. Brightling, C. E., P. Bradding, F. A. Symon, S. T. Holgate, A. J. Wardlaw, and I. D. Pavord. 2002. Mast-cell infiltration of airway smooth muscle in asthma. N. Engl. J. Med. 346:1699.
7. Metcalfe, D. D., D. Baram, and Y. A. Mekori. 1997. Mast cells. Physiol. Rev. 77:1033.
8. Garrington, T. P., T. Ishizuka, P. J. Papst, K. Chayama, S. Webb, T. Yujiri, W. Sun, S. Sather, D. M. Russell, S. B. Gibson, et al. 2000. MEKK2 gene disruption causes loss of cytokine production in response to IgE and c-Kit ligand stimulation of ES cell-derived mast cells. EMBO J. 19:5387.
9. Chayama, K., P. J. Pepsi, T. P. Garrington, J. C. Pratt, T. Ishizuka, S. Webb, S. Ganiatsas, L. I. Zon, W. Sun, G. L. Johnson, et al. 2001. Role of MEKK2-MEK5 in the regulation of TNF-α gene expression and MEKK2-MKK7 in the activation of c-Jun N-terminal kinase in mast cells. Proc. Natl. Acad. Sci. USA 98:4599.
10. Kung, T. T., D. Stelts, J. A. Zurcher, H. Jones, S. P. Umland, W. Kreutner, R. W. Egan, and R. W. Chapman. 1995. Mast cells modulate allergic pulmonary eosinophilia in mice. Am J. Respir. Cell Mol. Biol. 12:404.
11. + T cells and supplemental role of mast cells in allergic pulmonary eosinophilia. Int. Arch. Allergy Immunol. 120(Suppl. 1):15.
12. Nogami, M., M. Suko, H. Okudaira, T. Miyamoto, J. Shiga, M. Ito, and S. Kasuya. 1990. Experimental pulmonary eosinophilia in mice by Ascaris suum extract. Am. Rev. Respir. Dis. 141:1289.
13. Brusselle, G. G., J. C. Kips, J. H. Tavernier, J. G. van der Heyden, C. A. Cuvelier, R. A. Pauwels, and H. Bluethmann. 1994. Attenuation of allergic airway inflammation in IL-4 deficient mice. Clin. Exp. Allergy. 24:73.
14. Nagai, H., S. Yamaguchi, Y. Maeda, and H. Tanaka. 1996. Role of mast cells, eosinophils and IL-5 in the development of airway hyperresponsiveness in sensitized mice. Clin. Exp. Allergy 26:642.
15. Takeda, K., E. Hamelmann, A. Joetham, L. D. Shultz, G. L. Larsen, C. G. Irvin, and E. W. Gelfand. 1997. Development of eosinophilic airway inflammation and airway hyperresponsiveness in mast cell-deficient mice. J. Exp. Med. 186:449.
16. Williams, C. M., and S. J. Galli. 2000. Mast cells can amplify airway reactivity and features of chronic inflammation in an asthma model in mice. J. Exp. Med. 192:455.
17. Kobayashi, T., T. Miura, T. Haba, M. Sato, I. Serizawa, H. Nagai, and K. Ishizaka. 2000. An essential role of mast cells in the development of airway hyperresponsiveness in a murine asthma model. J. Immunol. 164:3855.
18. 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.
19. Larsen, 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.
20. Renz, H., G. Lack, J. Saloga, R. Schwinzer, K. Bradley, J. Loader, A. Kupfer, G. L. Larsen, and E. W. Gelfand. 1994. Inhibition of IgE production and normalization of airways responsiveness by sensitized CD8 T cells in a mouse model of allergen-induced sensitization. J. Immunol. 152:351.
21. Hamelmann, E., A. T. Vella, A. Oshiba, J. W. Kappler, P. Marrack, 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.
22. Dombrowicz, D., V. Flammand, K. K. Brigman, B. H. Keller, and J. P. Kinet. 1993. Abolition of anaphylaxis by targeted disruption of the high affinity immunoglobulin E receptor α chain gene. Cell 75:969.
23. Dombrowicz, D., V. Flamand, I. Miyajima, J. V. Ravetch, S. J. Galli, and J. P. Kinet. 1997. Absence of FcεRI α chain results in upregulation of FcγRIII-dependent mast cell degranulation and anaphylaxis: evidence of competition between FcεRI and FcγRIII for limiting amounts of FcR β and γ chains. J. Clin. Invest. 99:915.
24. MeKenzie, G. J., C. L. Ernson, S. E. Bell, S. Anderson, P. Fallon, G. Zurawski, R. Murray, R. Grencis, and A. N. McKenzie. 1998. Impaired development of Th2 cells in IL-13-deficient mice. Immunity 9:423.
25. + T-cell/dendritic cell interactions in vivo. Cell. Immunol. 214:110.
26. Donaldson, D. D., M. J. Whitters, L. J. Fitz, T. Y. Neben, H. Finnerty, S. L. Henderson, R. M. O'Hara, Jr., D. R. Beier, K. J. Turner, C. R. Wood, et al. 1998. The murine IL-13 receptor α2: molecular cloning, characterization, and comparison with marine IL-13 receptor α1. J. Immunol. 161:2317.
27. Bordier, C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1604.
28. Aida, Y., and M. J. Pabst. 1990. Removal of andotoxin from protein solutions by phase separation using Triton X-114. J. Immunol. Methods 132:191.
29. Ishizuka, T., K. Chayama, K. Takeda, E. Hamelmann, N. Terada, G. M. Keller, G. L. Johnson, and E. W. Gelfand. 1999. Mitogen-activated protein kinase activation through Fcε receptor I and stem cell factor receptor is differentially regulated by phosphatidylinositol 3-kinase and calcineurin in mouse bone marrow-derived mast cells. J. Immunol. 162:2087.
30. Karasuyama, H., and F. Melchers. 1988. Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors. Eur. J. Immunol. 18:97.
31. Tomkinson, A., C. Duez, G. Cieslewicz, J. C. Pratt, A. Joetham, M. C. Shanafelt, R. Gundel, and E. W. Gelfand. 2001. A murine IL-4 receptor antagonist that inhibits IL-4- and IL-13-induced responses prevents antigen-induced airway eosinophilia and airway hyperresponsiveness. J. Immunol. 166:5792.
32. Ranz, 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.
33. Stassen, M., C. Muller, M. Arnold, L. Hultner, S. Klein-Hessling, C. Neudorfl, T. Reineke, E. Serfling, and E. Schmitt. 2001. IL-9 and IL-13 production by activated mast cells is strongly enhanced in the presence of lipopolysaccharide: NF-κB is decisively involved in the expression of IL-9. J. Immunol. 166:4391.
34. Masuda, A., Y. Yoshikai, K. Aiba, and T. Matsuguchi. 2002. Th2 cytokine production from mast cells is directly induced by lipopolysaccharide and distinctly regulated by c-Jun N-terminal kinase and p38 pathways. J. Immunol. 169:3801.
35. Gruning, 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.
36. 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.
37. Walter, D. M., J. J. McIntire, G. Berry, A. N. McKenzie, D. D. Donaldson, R. H. DeKruyff, and D. T. Umetsu. 2001. Critical role for IL-13 in the development of allergen-induced airway hyperractivity. J. Immunol. 167:4668.
38. Taube, C., C. Duez, Z. H. Cui, K. Takeda, Y. H. Rha, J. W. Park, A. Balhorn, D. D. Donaldson, A. Dakhama, and E. W. Gelfand. 2002. The role of IL-13 in established allergic airway disease. J. Immunol. 169:6482.
39. Kinet, J. P. 1999. The high-affinity IgE receptor (FCεRI): from physiology to pathology. Annu. Rev. Immunol. 17:931.
40. Burd, P. R., W. C. Thompson, E. E. Max, and F. C. Mills. 1995. Activated mast cells produce interleukin 13. J. Exp. Med. 181:1373.
41. 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.
42. Hamelmann, E., K. Tadeda, A. Oshiba, and E. W. Gelfand. 1999. Role of IgE in the development of allergic airway inflammation and airway hyperresponsiveness: a murine model. Allergy 54:297.
43. 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 hyperreactivity and eosinophilic inflammation occur in the absence of IgE in a mouse model of asthma. Proc. Natl. Acad. Sci. USA 94:1344.
44. Hamelmann, E., G. Cieslewicz, J. Schwarze, T. Ishizuka, A. Joetham, C. Heusser, and E. W. Gelfand. 1999. Anti-interleukin 5 but not anti-IgE prevents airway inflammation and airway hyperresponsiveness. Am. J. Respir. Crit. Care Med. 160:934.
45. Mayr, S. I., R. I. Zuberi, M. Zhang, J. de Sousa-Hitzler, K. Ngo, Y. Kuwabara, L. Yu, W. P. Fung-Leung, and F. T. Liu. 2002. IgE-dependent mast cell activation potentiates airway responses in murine asthma models. J. Immunol. 169:2061.
46. Haczku, A., K. Takeda, E. Hamelmann, J. Loader, A. Joetham, I. Redai, C. G. Irvin, J. J. Lee, H. Kikutani, D. Conrad, et al. 2000. CD23 exhibits negative regulatory effects on allergic sensitization and airway hyperresponsiveness. Am. J. Respir. Crit. Care Med. 161:952.
47. Nakano, T., T. Sonoda, C. Hayashi, A. Yamatodani, Y. Kanayama, T. Yamamura, H. Asai, T. Yonezawa, Y. Kitamura, and S. J. Galli. 1985. Fate of bone marrow-derived cultured mast cells after intracutaneous, intraperitoneal, and intravenous transfer into genetically mast cell-deficient W/Wv mice: evidence that cultured mast cells can give rise to both connective tissue type and mucosal mast cells. J. Exp. Med. 162:1025.
48. Otsu, K., T. Nakano, Y. Kanakura, H. Asai, H. R. Katz, K. F. Austen, R. L. Stevens, S. J. Gaili, and Y. Kitamura 1987. Phenotypic changes of bone marrow-derived mast cells after intraperitoneal transfer into W/Wv mice that are genetically deficient in mast cells. J. Exp. Med. 165:615.
49. Kraneveld, A. D., H. P. van der Kleij, M. Kool, A. H. van Houwelingen, A. C. Waitenberg, F. A. Redegeld, and F. P. Nijkamp. 2002. Key role for mast cells in nonatopic asthma. J. Immunol. 169:2044.
50. 125I-fibrin deposition in IgE-dependent immediate hypersensitivity reactions in mouse skin: demonstration of the role of mast cells using genetically mast cell-deficient mice locally reconstituted with cultured mast cells. J. Immunol. 139:2605.
51. Qureshi, R., and B. A. Jakschik. 1988. The role of mast cells in thioglycollate-induced inflammation. J. Immunol. 141:2090.
52. + cells developing in IL-3-dependent murine bone marrow-derived cell cultures. J. Immunol. 151:4950.
53. Dvorak, A. M., R. A. Seder, W. E. Paul, E. S. Morgan, and S. J. Galli. 1994. Effects of interleukin-3 with or without the c-kit ligand, stem cell factor, on the survival and cytoplasmic granule formation of mouse basophils and mast cells in vitro. Am. J. Pathol. 144:160.
54. Zhu, Z., R. J. Homer, Z. Wang, Q. Chen, G. P. Geba, J. Wang, Y. Zhang, and J. A. Elias. 1999. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103:779.
55. 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.
56. Zurawski, G., and J. E. de Vries. 1994. Interleukin 13, an interleukin 4-like cytokine that acts on monocytes and B cells, but not on T cells, Immunol. Today 15:19.
57. Bochner, B. S., D. A. Klunk, S. A. Sterbinsky, R. L. Coffman, and R. P. Schleimer. 1995. IL-13 selectively induces vascular cell adhesion molecule-1 expression in human endothelial cells. J. Immunol. 154:799.
58. Zuhdi Alimam, M., F. M. Piazza, D. M. Selby, N. Letwin, L. Huang, and M. C. Rose. 2000. Muc-5/5ac mucin messenger RNA and protein expression is a marker of goblet cell metaplasia in murine airways. Am. J. Respir. Cell Mol. Biol. 22:253.
59. Marietta, E. V., Y. Chen, and J. H. Weis. 1996. Modulation of expression of the anti-inflammatory cytokines interleukin-13 and interleukin-10 by interleukin-3. Eur. J. Immunol. 26:49.
60. Grunstein, M. M., H. Hakonarson, J. Leiter, M. Chen, R. Whelan, J. S. Grunstein, and S. Chuang. 2002. IL-13-dependent autocrine signaling mediates altered responsiveness of IgE-sensitized airway smooth muscle. Am. J. Physiol. 282:L520.
61. Hoshino, T., R. T. Winkler-Pickett, A. T. Mason, J. R. Ortaldo, and H. A. Young. 1999. IL-13 production by NK cells: IL-13-producing NK and T cells are present in vivo in the absence of IFN-γ. J. Immunol. 162:51.
62. Akbari, O., P. Stock, E. Meyer, M. Kronenberg, S. Sidobre, T. Nakayama, M. Taniguchi, M. J. Grusby, R. H. DeKruyff, and D. T. Umetsu. 2003. Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat. Med. 9:582.