IgE(+), Kit(-), I-A/I-E(-) myeloid cells are the initial source of Il-4 after antigen challenge in a mouse model of allergic pulmonary inflammation

J Allergy Clin Immunol. 2002 Jul;110(1):117-24. doi: 10.1067/mai.2002.125828.

Abstract

Background: IL-4 is generated within hours after antigen lung challenge and influences events that take place early in the induction of pulmonary inflammation. However, the cells responsible for this early IL-4 production in the lung are unknown.

Objectives: We sought to characterize the initial inflammatory events in the lung after antigen challenge and to identify cells responsible for producing IL-4 at early time points.

Methods: Mice were sensitized with ovalbumin or passive IgE and challenged intranasally. Histologic measures of inflammation were used, and lung tissue cytokine production was analyzed by means of RT-PCR. Cells producing IL-4 were characterized by means of in situ hybridization and flow cytometry.

Results: IL-4 mRNA was detectable 100 minutes after challenge in sensitized animals. Blockade of this early IL-4 downregulated vascular cell adhesion molecule 1 mRNA expression and attenuated the early recruitment of eosinophils to the lung. CD4-depleted and mast cell-deficient mice both expressed early IL-4. Cellular analysis revealed the presence of IL-4 protein at 100 minutes exclusively in IgE(+) myeloid cells that did not express CD3, Kit, or I-A/I-E. Moreover, IL-4 production induced by means of passive IgE sensitization and abrogated in FcR gamma-chain-deficient mice supports the conclusion that this IL-4 production is dependent on IgE/gamma-chain interaction.

Conclusion: IL-4 production by an IgE/gamma-chain-dependent mechanism occurs rapidly after allergen challenge. At these early time points, IL-4 is produced by a myeloid cell with the characteristics of a mouse basophil (IgE(+), Kit(-), I-A/I-E(-)). These data thus suggest that strategies targeting basophils should be considered in the treatment of early lung inflammation.

MeSH terms

  • Administration, Intranasal
  • Animals
  • Antigens / administration & dosage*
  • Antigens / immunology
  • Basophils / immunology
  • Disease Models, Animal
  • Histocompatibility Antigens Class II / biosynthesis
  • Immunoglobulin E / biosynthesis*
  • Inflammation / etiology
  • Inflammation / immunology*
  • Interleukin-4 / biosynthesis*
  • Lung / cytology
  • Lung / immunology
  • Mice
  • Mice, Inbred BALB C
  • Myeloid Cells / cytology
  • Myeloid Cells / immunology*
  • Myeloid Cells / metabolism
  • Ovalbumin / administration & dosage
  • Ovalbumin / immunology
  • Proto-Oncogene Proteins c-kit / biosynthesis
  • Receptors, Fc / metabolism
  • Respiratory Hypersensitivity / etiology
  • Respiratory Hypersensitivity / immunology*

Substances

  • Antigens
  • Histocompatibility Antigens Class II
  • Receptors, Fc
  • Interleukin-4
  • Immunoglobulin E
  • Ovalbumin
  • Proto-Oncogene Proteins c-kit