Histamine receptor 2 modifies iNKT cell activity within the inflamed lung

Allergy. 2017 Dec;72(12):1925-1935. doi: 10.1111/all.13227. Epub 2017 Jun 30.

Abstract

Background: Histamine is a key immunoregulatory mediator and can dampen proinflammatory responses via activation of histamine receptor 2 (H2 R). The aim of this study was to determine the role of H2 R in modulating lung inflammatory responses.

Methods: H2 R was blocked using famotidine or activated using dimaprit in both the ovalbumin (OVA) and house dust mite extract (HDM) murine models of respiratory inflammation. H2 R-deficient animals and CD1d/H2 R-deficient animals were utilized to examine the CD1d presentation of lipid antigens (αGalCer or OCH) to invariant natural killer T (iNKT) cells.

Results: Famotidine treatment resulted in more severe airway disease in the OVA model, while dimaprit treatment significantly reduced disease severity. Both OVA and HDM-induced airway diseases were more severe in H2 R-deficient animals. Flow cytometric analysis of lung tissue from H2 R-deficient animals revealed increased numbers of CD1d+ dendritic cells and increased numbers of iNKT cells. In vitro, αGalCer-stimulated iNKT cells from H2 R-deficient mice secreted higher levels of IL-4, IL-5, and GM-CSF. In vivo, αGalCer or OCH administration to the lung resulted in enhanced mucus secretion, inflammatory cell recruitment, and cytokine production in H2 R-deficient or famotidine-treated animals, while dimaprit dampened the lung iNKT cell response to αGalCer. Removal of iNKT cells in H2 R-deficient (CD1d-/- H2 R-/- ) animals normalized the lung response to HDM.

Conclusion: The deliberate activation of H2 R, or its downstream signaling molecules, may represent a novel therapeutic target for chronic lung inflammatory diseases, especially when CD1d-mediated presentation of lipid antigens to iNKT cells is contributing to the pathology.

Keywords: CD1d; allergy; histamine; inflammation; invariant natural killer T cells.

MeSH terms

  • Animals
  • Antigens, CD1d / metabolism
  • Biomarkers
  • Disease Models, Animal
  • Disease Progression
  • Female
  • Immunophenotyping
  • Inflammation Mediators
  • Lymphocyte Activation / immunology
  • Lymphocyte Count
  • Mice
  • Mice, Knockout
  • Natural Killer T-Cells / immunology*
  • Natural Killer T-Cells / metabolism*
  • Phenotype
  • Pneumonia / genetics
  • Pneumonia / immunology*
  • Pneumonia / metabolism*
  • Pneumonia / pathology
  • Receptors, Histamine H2 / genetics
  • Receptors, Histamine H2 / metabolism*
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Antigens, CD1d
  • Biomarkers
  • Inflammation Mediators
  • Receptors, Histamine H2