Allergen immunotherapy induces a suppressive memory response mediated by IL-10 in a mouse asthma model

J Allergy Clin Immunol. 2004 Jun;113(6):1204-10. doi: 10.1016/j.jaci.2004.02.041.

Abstract

Background: Human studies have demonstrated that allergen immunotherapy induces memory suppressive responses and IL-10 production by allergen-specific T cells. Previously, we established a mouse model in which allergen immunotherapy was effective in the suppression of allergen-induced asthma manifestations.

Objective: In this study, we examined whether immunotherapy induces a long-lasting effect and investigated the role of IL-10 in successful immunotherapy.

Methods: Ovalbumin-sensitized BALB/c mice were treated with 3 injections of ovalbumin (1 mg, subcutaneous) on alternate days. After a short interval (1 week) and after a long interval (5 weeks), mice were challenged by ovalbumin inhalation, and subsequently, airway reactivity, airway eosinophilia, ovalbumin-specific IgE, and T(H)2 cytokine profile were measured. Flow cytometry and blocking of IL-10 receptors in vivo were used to gain insight in the role of IL-10 in the beneficial effects of allergen immunotherapy.

Results: After a long interval between ovalbumin immunotherapy and ovalbumin challenge, the development of airway eosinophilia and hyperresponsiveness to methacholine were as strongly suppressed as after a short interval. These suppressive effects coincided with significantly reduced serum ovalbumin-specific IgE levels and T(H)2 cytokine production. On immunotherapy, the IL-5:IL-10 ratio in the bronchoalveolar lavage fluid shifted toward IL-10. In ovalbumin-restimulated lung cell and thoracic lymph node cultures from these mice, IL-5 levels dramatically decreased, whereas the percentage of IL-10(+)CD4(+) T cells was not affected. Finally, in mice treated with mAb against IL-10 receptors, the beneficial effects of immunotherapy were largely abrogated.

Conclusion: These data demonstrate that allergen immunotherapy induces a memory suppressive effect in which IL-10 is essential.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Asthma / immunology
  • Asthma / therapy*
  • Bronchoalveolar Lavage Fluid / chemistry
  • Cytokines / biosynthesis
  • Desensitization, Immunologic*
  • Immune Tolerance*
  • Immunoglobulin E / blood
  • Immunologic Memory*
  • Interleukin-10 / physiology*
  • Interleukin-5 / analysis
  • Lung / immunology
  • Lymph Nodes / immunology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Ovalbumin / immunology

Substances

  • Cytokines
  • Interleukin-5
  • Interleukin-10
  • Immunoglobulin E
  • Ovalbumin