IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation

J Immunol. 2009 Nov 15;183(10):6469-77. doi: 10.4049/jimmunol.0901575. Epub 2009 Oct 19.

Abstract

Alternatively activated macrophages (AAM) play a crucial role in type 2 immunity. Mice deficient in ST2, a receptor for the latest member of the IL-1 family, IL-33, have impaired type 2 immune responses. We therefore reasoned that IL-33/ST2 signaling may be involved in the differentiation and activation of AAM during airway inflammation. We report here that IL-33 changed the quiescent phenotype of alveolar macrophages toward an AAM phenotype that expressed mannose receptor, IL-4Ralpha, and produced high levels of CCL24 and CCL17 in an IL-13-dependent manner during IL-33-induced airway inflammation. Neutralization of AAM-derived CCL24 led to an amelioration of IL-33-induced eosinophilia in the lungs. Moreover, depletion of alveolar macrophages reduced IL-33-induced airway inflammation. Additionally, the attenuated OVA-induced airway inflammation in ST2(-/-) mice was associated with a decrease in AAM differentiation. In vitro, IL-33 amplified IL-13-induced polarization of alveolar- and bone marrow-derived macrophage toward an AAM phenotype by increasing the expression of arginase I, Ym1, as well as the production of CCL24 and CCL17. IL-13/IL-4Ralpha signaling was crucial for IL-33-driven AAM amplification by inducing the expression of ST2L. Finally, we showed that IL-33 was more abundantly expressed in the lung epithelial cells of asthma patients than those from healthy controls, suggesting that IL-33 may be involved in lung macrophage activation in clinical asthma. Taken together, we demonstrate here that IL-33/ST2 plays a significant role in the amplification of AAM polarization and chemokine production which contribute to innate and Ag-induced airway inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Asthma / immunology
  • Asthma / metabolism
  • Cell Polarity / immunology*
  • Chemokine CCL17 / immunology
  • Chemokine CCL17 / metabolism
  • Chemokine CCL24 / immunology
  • Chemokine CCL24 / metabolism
  • Eosinophilia / immunology
  • Epithelial Cells / immunology*
  • Epithelial Cells / metabolism
  • Female
  • Humans
  • Inflammation / immunology*
  • Inflammation / metabolism
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-13 / immunology
  • Interleukin-13 / metabolism
  • Interleukin-33
  • Interleukin-4 / genetics
  • Interleukin-4 / immunology
  • Interleukin-4 / metabolism
  • Interleukins / immunology*
  • Interleukins / metabolism
  • Lung / immunology
  • Lung / pathology
  • Macrophage Activation / immunology
  • Macrophages, Alveolar / immunology*
  • Macrophages, Alveolar / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Middle Aged
  • Ovalbumin / immunology
  • Receptors, Interleukin / genetics
  • Receptors, Interleukin / immunology*
  • Receptors, Interleukin / metabolism
  • Receptors, Interleukin-1 / immunology
  • Receptors, Interleukin-1 / metabolism
  • Receptors, Interleukin-4 / genetics
  • Receptors, Interleukin-4 / immunology
  • Receptors, Interleukin-4 / metabolism
  • Recombinant Proteins / immunology
  • Recombinant Proteins / metabolism
  • Signal Transduction / immunology

Substances

  • Chemokine CCL17
  • Chemokine CCL24
  • IL33 protein, human
  • Il1rl1 protein, mouse
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-13
  • Interleukin-33
  • Interleukins
  • Receptors, Interleukin
  • Receptors, Interleukin-1
  • Receptors, Interleukin-4
  • Recombinant Proteins
  • ST2L protein, mouse
  • Interleukin-4
  • Ovalbumin