IL-4 induces IL-13-independent allergic airway inflammation

J Allergy Clin Immunol. 2006 Aug;118(2):410-9. doi: 10.1016/j.jaci.2006.06.004.

Abstract

Background: The related T(H)2 cytokines IL-4 and IL-13 are produced during allergic responses, signal through receptors that contain IL-4 receptor (IL-4R) alpha, and promote allergic inflammation by activating signal transducer and activator of transcription 6. IL-4 promotes T(H)2 response induction, and IL-13 is necessary and sufficient to induce airways hyperresponsiveness (AHR) and goblet cell hyperplasia in some mouse models of asthma. The nonredundant role of IL-13 could reflect unique IL-13 activation of a signaling pathway, inhibitory effects induced by IL-4 but not IL-13, or greater production-potency of IL-13 than IL-4.

Objectives: We sought to distinguish among these possibilities by determining whether IL-4 inhalation can induce acute allergic airways disease in the absence of IL-13.

Methods: Mice were inoculated intratracheally with IL-13 or a long-acting formulation of IL-4. Responses of IL-13-deficient and IL-13-sufficient mice were compared, as were responses in mice treated with a potent IL-13 antagonist, anti-IL-4Ralpha antibody, or control reagents.

Results: IL-4 inhalation stimulated bronchoalveolar lavage fluid eosinophilia, AHR, and goblet cell hyperplasia. These responses were similar in IL-13-deficient and IL-13-sufficient mice and were not inhibited by an IL-13 antagonist but were blocked by anti-IL-4Ralpha antibody.

Conclusion: IL-4 can induce IL-13-independent AHR and goblet cell hyperplasia. Thus the greater role for IL-13 than IL-4 in the induction of these acute allergy-related changes reflects increased production, potency, or both of IL-13 relative to IL-4 rather than a unique IL-13-signaling pathway or a suppressive effect of IL-4.

Clinical implications: Dual IL-4/IL-13 inhibition might be more effective than selective IL-13 inhibition at suppressing allergic inflammation in some circumstances.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Bronchial Hyperreactivity / chemically induced*
  • Bronchoalveolar Lavage Fluid / cytology
  • Eosinophilia / chemically induced
  • Female
  • Goblet Cells / drug effects*
  • Goblet Cells / pathology
  • Hyperplasia
  • Immunoglobulin Fc Fragments / pharmacology
  • Interleukin-13 / antagonists & inhibitors
  • Interleukin-13 / deficiency*
  • Interleukin-13 / genetics
  • Interleukin-4 / immunology
  • Interleukin-4 / pharmacology*
  • Leukocyte Count
  • Lung / drug effects
  • Lung / pathology
  • Lung / physiopathology
  • Male
  • Methacholine Chloride / pharmacology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Pneumonia
  • Recombinant Fusion Proteins / pharmacology
  • Respiratory Hypersensitivity / chemically induced*

Substances

  • Antibodies, Monoclonal
  • Immunoglobulin Fc Fragments
  • Interleukin-13
  • Recombinant Fusion Proteins
  • Methacholine Chloride
  • Interleukin-4