Central role of immunoglobulin (Ig) E in the induction of lung eosinophil infiltration and T helper 2 cell cytokine production: inhibition by a non-anaphylactogenic anti-IgE antibody

doi:10.1084/jem.183.4.1303

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Central role of immunoglobulin (Ig) E in the induction of lung eosinophil infiltration and T helper 2 cell cytokine production: inhibition by a non-anaphylactogenic anti-IgE antibody

AJ Coyle, K Wagner, C Bertrand, S Tsuyuki, J Bews and C Heusser
Ciba-Geigy Ltd., Asthma and Allergy Research Department, Pharmaceutical Division, Basel Switzerland.

Elevated levels of immunoglobulin (Ig) E are associated with bronchial asthma, a disease characterized by eosinophilic inflammation of the airways. Activation of antigen-specific T helper (Th) 2 cells in the lung with the subsequent release of interleukin (IL) 4 and IL-5 is believed to play an important role in the pathogenesis of this disease. In this study, we have used a non-anaphylactogenic anti-mouse-IgE antibody to investigate the relationship between IgE, airway eosinophil infiltration, and the production of Th2 cytokines. Immunization of mice with house dust mite antigen increased serum levels of IgE and IgG. Antigen challenge of immunized but not control mice induced an infiltration of eosinophils in the bronchoalveolar lavage associated with the production of IL-4 and IL-5 from lung purified Thy1.2+ cells activated through the CD3-T cell receptor complex. Administration of the anti-IgE monoclonal antibody (mAb) 6h before antigen challenge neutralized serum IgE but not IgG and inhibited the recruitment of eosinophils into the lungs and the production of IL-4 and IL-5 but not interferon gamma. Studies performed using an anti-CD23 mAb, CD23 deficient and mast cell deficient mice suggest that anti-IgE mAb suppresses eosinophil infiltration and Th2 cytokine production by inhibiting IgE-CD23-facilitated antigen presentation to T cells. Our results demonstrate that IgE-dependent mechanisms are important in the induction of a Th2 immune response and the subsequent infiltration of eosinophils into the airways. Neutralization of IgE, for example, non- anaphylactogenic anti-IgE mAbs may provide a novel therapeutic approach to the treatment of allergic airway disease.
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Skripuletz, T., Schmiedl, A., Schade, J., Bedoui, S., Glaab, T., Pabst, R., von Horsten, S., Stephan, M. (2007). Dose-dependent recruitment of CD25+ and CD26+ T cells in a novel F344 rat model of asthma. Am. J. Physiol. Lung Cell. Mol. Physiol. 292: L1564-L1571 [Abstract] [Full Text]
Pongratz, G., McAlees, J. W., Conrad, D. H., Erbe, R. S., Haas, K. M., Sanders, V. M. (2006). The Level of IgE Produced by a B Cell Is Regulated by Norepinephrine in a p38 MAPK- and CD23-Dependent Manner.. J. Immunol. 177: 2926-2938 [Abstract] [Full Text]
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Yamashita, N., Tashimo, H., Ishida, H., Matsuo, Y., Tamauchi, H., Terashima, M., Yoshiwara, I., Habu, S., Ohta, K. (2006). Involvement of GATA-3-dependent Th2 lymphocyte activation in airway hyperresponsiveness. Am. J. Physiol. Lung Cell. Mol. Physiol. 290: L1045-L1051 [Abstract] [Full Text]
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Byrd, W., Cassels, F. J. (2006). The encapsulation of enterotoxigenic Escherichia coli colonization factor CS3 in biodegradable microspheres enhances the murine antibody response following intranasal administration.. Microbiology 152: 779-786 [Abstract] [Full Text]
Fischer, R., McGhee, J. R., Vu, H. L., Atkinson, T. P., Jackson, R. J., Tome, D., Boyaka, P. N. (2005). Oral and Nasal Sensitization Promote Distinct Immune Responses and Lung Reactivity in a Mouse Model of Peanut Allergy. Am. J. Pathol. 167: 1621-1630 [Abstract] [Full Text]
Djukanovic, R., Wilson, S. J., Kraft, M., Jarjour, N. N., Steel, M., Chung, K. F., Bao, W., Fowler-Taylor, A., Matthews, J., Busse, W. W., Holgate, S. T., Fahy, J. V. (2004). Effects of Treatment with Anti-immunoglobulin E Antibody Omalizumab on Airway Inflammation in Allergic Asthma. Am. J. Respir. Crit. Care Med. 170: 583-593 [Abstract] [Full Text]
Wittke, A., Weaver, V., Mahon, B. D., August, A., Cantorna, M. T. (2004). Vitamin D Receptor-Deficient Mice Fail to Develop Experimental Allergic Asthma. J. Immunol. 173: 3432-3436 [Abstract] [Full Text]
Odom, S., Gomez, G., Kovarova, M., Furumoto, Y., Ryan, J. J., Wright, H. V., Gonzalez-Espinosa, C., Hibbs, M. L., Harder, K. W., Rivera, J. (2004). Negative Regulation of Immunoglobulin E-dependent Allergic Responses by Lyn Kinase. J. Exp. Med. 199: 1491-1502 [Abstract] [Full Text]
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Kang, H.-S., Blink, S. E., Chin, R. K., Lee, Y., Kim, O., Weinstock, J., Waldschmidt, T., Conrad, D., Chen, B., Solway, J., Sperling, A. I., Fu, Y.-X. (2003). Lymphotoxin Is Required for Maintaining Physiological Levels of Serum IgE That Minimizes Th1-mediated Airway Inflammation. J. Exp. Med. 198: 1643-1652 [Abstract] [Full Text]
Buhl, R., Hanf, G., Soler, M., Bensch, G., Wolfe, J., Everhard, F., Champain, K., Fox, H., Thirlwell, J. (2002). The anti-IgE antibody omalizumab improves asthma-related quality of life in patients with allergic asthma. Eur Respir J 20: 1088-1094 [Abstract] [Full Text]
Lemanske, R. F. Jr, Nayak, A., McAlary, M., Everhard, F., Fowler-Taylor, A., Gupta, N. (2002). Omalizumab Improves Asthma-Related Quality of Life in Children With Allergic Asthma. Pediatrics 110: e55-55 [Abstract] [Full Text]
SCHULMAN, E. S. (2001). Development of a Monoclonal Anti-Immunoglobulin E Antibody (Omalizumab) for the Treatment of Allergic Respiratory Disorders. Am. J. Respir. Crit. Care Med. 164: S6-11 [Abstract] [Full Text]
Papouchado, B. G., Chapoval, S. P., Marietta, E. V., Weiler, C. R., David, C. S. (2001). Cockroach Allergen-Induced Eosinophilic Airway Inflammation in HLA-DQ/Human CD4+ Transgenic Mice. J. Immunol. 167: 4627-4634 [Abstract] [Full Text]
Wu, C. A., Puddington, L., Whiteley, H. E., Yiamouyiannis, C. A., Schramm, C. M., Mohammadu, F., Thrall, R. S. (2001). Murine Cytomegalovirus Infection Alters Th1/Th2 Cytokine Expression, Decreases Airway Eosinophilia, and Enhances Mucus Production in Allergic Airway Disease. J. Immunol. 167: 2798-2807 [Abstract] [Full Text]
Chanez, P. (2001). Immunological intervention with anti-immunoglobulin-E antibody to prevent asthma exacerbations. Eur Respir J 18: 249-250 [Full Text]
Soler, M., Matz, J., Townley, R., Buhl, R., O'Brien, J., Fox, H., Thirlwell, J., Gupta, N., Della Cioppa, G. (2001). The anti-IgE antibody omalizumab reduces exacerbations and steroid requirement in allergic asthmatics. Eur Respir J 18: 254-261 [Abstract] [Full Text]
Kips, J.C. (2001). Cytokines in asthma. Eur Respir J 18: 24S-33s [Abstract] [Full Text]
Lloyd, C. M., Gonzalo, J.-A., Nguyen, T., Delaney, T., Tian, J., Oettgen, H., Coyle, A. J., Gutierrez-Ramos, J.-C. (2001). Resolution of Bronchial Hyperresponsiveness and Pulmonary Inflammation Is Associated with IL-3 and Tissue Leukocyte Apoptosis. J. Immunol. 166: 2033-2040 [Abstract] [Full Text]
COYLE, A. J., LLOYD, C. M., GUTIERREZ-RAMOS, J.-C. (2000). Biotherapeutic Targets for the Treatment of Allergic Airway Disease. Am. J. Respir. Crit. Care Med. 162: S179-184 [Abstract] [Full Text]
Hamelmann, E., Takeda, K., Haczku, A., Cieslewicz, G., Shultz, L., Hamid, Q., Xing, Z., Gauldie, J., Gelfand, E. W. (2000). Interleukin (IL)-5 but Not Immunoglobulin E Reconstitutes Airway Inflammation and Airway Hyperresponsiveness in IL-4-Deficient Mice. Am. J. Respir. Cell Mol. Bio. 23: 327-334 [Abstract] [Full Text]
KIPS, J. C., TOURNOY, K. G., PAUWELS, R. A. (2000). Gene Knockout Models of Asthma. Am. J. Respir. Crit. Care Med. 162: S66-70 [Full Text]
Gonzalo, J.-A., Lloyd, C. M., Peled, A., Delaney, T., Coyle, A. J., Gutierrez-Ramos, J.-C. (2000). Critical Involvement of the Chemotactic Axis CXCR4/Stromal Cell-Derived Factor-1{alpha} in the Inflammatory Component of Allergic Airway Disease. J. Immunol. 165: 499-508 [Abstract] [Full Text]
Zuberi, R. I., Apgar, J. R., Chen, S.-S., Liu, F.-T. (2000). Role for IgE in Airway Secretions: IgE Immune Complexes Are More Potent Inducers Than Antigen Alone of Airway Inflammation in a Murine Model. J. Immunol. 164: 2667-2673 [Abstract] [Full Text]
Barnes, P. J. (1999). Anti-IgE Antibody Therapy for Asthma. NEJM 341: 2006-2008 [Full Text]
Johnson, T. R., Graham, B. S. (1999). Secreted Respiratory Syncytial Virus G Glycoprotein Induces Interleukin-5 (IL-5), IL-13, and Eosinophilia by an IL-4-Independent Mechanism. J. Virol. 73: 8485-8495 [Abstract] [Full Text]
Hamelmann, E., Takeda, K., Schwarze, J., Vella, A. T., Irvin, C. G., Gelfand, E. W. (1999). Development of Eosinophilic Airway Inflammation and Airway Hyperresponsiveness Requires Interleukin-5 but Not Immunoglobulin E or B Lymphocytes. Am. J. Respir. Cell Mol. Bio. 21: 480-489 [Abstract] [Full Text]
TOMKINSON, A., KANEHIRO, A., RABINOVITCH, N., JOETHAM, A., CIESLEWICZ, G., GELFAND, E. W. (1999). The Failure of STAT6-deficient Mice to Develop Airway Eosinophilia and Airway Hyperresponsiveness Is Overcome by Interleukin-5. Am. J. Respir. Crit. Care Med. 160: 1283-1291 [Abstract] [Full Text]
HAMELMANN, E., CIESLEWICZ, G., SCHWARZE, J., ISHIZUKA, T., JOETHAM, A., HEUSSER, C., GELFAND, E. W. (1999). Anti-interleukin 5 But Not Anti-IgE Prevents Airway Inflammation and Airway Hyperresponsiveness. Am. J. Respir. Crit. Care Med. 160: 934-941 [Abstract] [Full Text]
van Neerven, R. J. J., Wikborg, T., Lund, G., Jacobsen, B., Brinch-Nielsen, A., Arnved, J., Ipsen, H. (1999). Blocking Antibodies Induced by Specific Allergy Vaccination Prevent the Activation of CD4+ T Cells by Inhibiting Serum-IgE-Facilitated Allergen Presentation. J. Immunol. 163: 2944-2952 [Abstract] [Full Text]
Kato, Y., Manabe, T., Tanaka, Y., Mochizuki, H. (1999). Effect of an Orally Active Th1/Th2 Balance Modulator, M50367, on IgE Production, Eosinophilia, and Airway Hyperresponsiveness in Mice. J. Immunol. 162: 7470-7479 [Abstract] [Full Text]
Yiamouyiannis, C. A., Schramm, C. M., Puddington, L., Stengel, P., Baradaran-Hosseini, E., Wolyniec, W. W., Whiteley, H. E., Thrall, R. S. (1999). Shifts in Lung Lymphocyte Profiles Correlate with the Sequential Development of Acute Allergic and Chronic Tolerant Stages in a Murine Asthma Model. Am. J. Pathol. 154: 1911-1921 [Abstract] [Full Text]
Sur, S., Wild, J. S., Choudhury, B. K., Sur, N., Alam, R., Klinman, D. M. (1999). Long Term Prevention of Allergic Lung Inflammation in a Mouse Model of Asthma by CpG Oligodeoxynucleotides. J. Immunol. 162: 6284-6293 [Abstract] [Full Text]
Haile, S., Lefort, J., Joseph, D., Gounon, P., Huerre, M., Boris Vargaftig, B. (1999). Mucous-Cell Metaplasia and Inflammatory-Cell Recruitment Are Dissociated in Allergic Mice after Antibody- and Drug-Dependent Cell Depletion in a Murine Model of Asthma. Am. J. Respir. Cell Mol. Bio. 20: 891-902 [Abstract] [Full Text]
Wise, J. T., Baginski, T. J., Mobley, J. L. (1999). An Adoptive Transfer Model of Allergic Lung Inflammation in Mice Is Mediated by CD4+CD62LlowCD25+ T Cells. J. Immunol. 162: 5592-5600 [Abstract] [Full Text]
Cernadas, M., De Sanctis, G. T., Krinzman, S. J., Mark, D. A., Donovan, C. E., Listman, J. A., Kobzik, L., Kikutani, H., Christiani, D. C., Perkins, D. L., Finn, P. W. (1999). CD23 and Allergic Pulmonary Inflammation: Potential Role as an Inhibitor. Am. J. Respir. Cell Mol. Bio. 20: 1-8 [Abstract] [Full Text]
RABE, K.�F. (1998). Mechanisms of Immune Sensitization of Human Bronchus. Am. J. Respir. Crit. Care Med. 158: S161-S170 [Abstract] [Full Text]
Li, L., Xia, Y., Nguyen, A., Feng, L., Lo, D. (1998). Th2-Induced Eotaxin Expression and Eosinophilia Coexist with Th1 Responses at the Effector Stage of Lung Inflammation. J. Immunol. 161: 3128-3135 [Abstract] [Full Text]
Hogan, S. P., Matthaei, K. I., Young, J. M., Koskinen, A., Young, I. G., Foster, P. S. (1998). A Novel T Cell-Regulated Mechanism Modulating Allergen-Induced Airways Hyperreactivity in BALB/c Mice Independently of IL-4 and IL-5. J. Immunol. 161: 1501-1509 [Abstract] [Full Text]
Ghaffar, O., Durham, S. R., Al-Ghamdi, K., Wright, E., Small, P., Frenkiel, S., Gould, H. J., Hamid, Q. (1998). Expression of IgE Heavy Chain Transcripts in the Sinus Mucosa of Atopic and Nonatopic Patients with Chronic Sinusitis. Am. J. Respir. Cell Mol. Bio. 18: 706-711 [Abstract] [Full Text]
Hakonarson, H., Grunstein, M. M. (1998). Autologously up-regulated Fc receptor expression and action in airway smooth muscle mediates its altered responsiveness in the atopic asthmatic sensitized state. Proc. Natl. Acad. Sci. USA 95: 5257-5262 [Abstract] [Full Text]
Rudolf, M. P., Vogel, M., Kricek, F., Ruf, C., Zurcher, A. W., Reuschel, R., Auer, M., Miescher, S., Stadler, B. M. (1998). Epitope-Specific Antibody Response to IgE by Mimotope Immunization. J. Immunol. 160: 3315-3321 [Abstract] [Full Text]
Galli, S. J. (1997). Complexity and Redundancy in the Pathogenesis of Asthma: Reassessing the Roles of Mast Cells and T Cells. J. Exp. Med. 186: 343-347 [Full Text]
RABE, K.�F., WATSON, N., DENT, G., MORTON, B.�E., WAGNER, K., MAGNUSSEN, H., HEUSSER, C.�H. (1997). Inhibition of Human Airway Sensitization by a Novel Monoclonal Anti-IgE Antibody, 17-9�. Am. J. Respir. Crit. Care Med. 157: 1429-1435 [Abstract] [Full Text]
Gleich, G. J., Kita, H. (1997). Bronchial asthma: Lessons from�murine�models. Proc. Natl. Acad. Sci. USA 94: 2101-2102 [Full Text]
Korsgren, M., alt, J. S.�E., Korsgren, O., Sundler, F., Persson, C. G.A. (1997). Allergic Eosinophil-rich Inflammation Develops in Lungs and Airways of B Cell-deficient Mice. J. Exp. Med. 185: 885-892 [Abstract] [Full Text]
Mehlhop, P.�D., van�de�Rijn, M., Goldberg, A.�B., Brewer, J.�P., Kurup, V.�P., Martin, T.�R., Oettgen, H.�C. (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: 1344-1349 [Abstract] [Full Text]
Hamelmann, E., Vella, A.�T., Oshiba, A., Kappler, J.�W., Marrack, P., Gelfand, E.�W. (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 [Abstract] [Full Text]
HOGAN, S.�P., KOSKINEN, A., MATTHAEI, K.�I., YOUNG, I.�G., FOSTER, P.�S. (1997). Interleukin-5-producing CD4+ T Cells Play a Pivotal Role in Aeroallergen-induced Eosinophilia, Bronchial Hyperreactivity, and Lung Damage in Mice. Am. J. Respir. Crit. Care Med. 157: 210-218 [Abstract] [Full Text]
Chvatchko, Y., Kosco-Vilbois, M. H., Herren, S., Lefort, J., Bonnefoy, J.-Y. (1996). Germinal Center Formation and Local Immunoglobulin E (IgE) Production in the Lung after an Airway Antigenic Challenge. J. Exp. Med. 184: 2353-2360 [Abstract] [Full Text]