Prostaglandin E₂ suppresses allergic sensitization and lung inflammation by targeting the E prostanoid 2 receptor on T cells

J Allergy Clin Immunol. 2014 Feb;133(2):379-87. doi: 10.1016/j.jaci.2013.07.037. Epub 2013 Sep 24.

Abstract

Background: Endogenous prostanoids have been suggested to modulate sensitization during experimental allergic asthma, but the specific role of prostaglandin (PG) E₂ or of specific E prostanoid (EP) receptors is not known.

Objective: Here we tested the role of EP2 signaling in allergic asthma.

Methods: Wild-type (WT) and EP2(-/-) mice were subjected to ovalbumin sensitization and acute airway challenge. The PGE2 analog misoprostol was administered during sensitization in both genotypes. In vitro culture of splenocytes and flow-sorted dendritic cells and T cells defined the mechanism by which EP2 exerted its protective effect. Adoptive transfer of WT and EP2(-/-) CD4 T cells was used to validate the importance of EP2 expression on T cells.

Results: Compared with WT mice, EP2(-/-) mice had exaggerated airway inflammation in this model. Splenocytes and lung lymph node cells from sensitized EP2(-/-) mice produced more IL-13 than did WT cells, suggesting increased sensitization. In WT but not EP2(-/-) mice, subcutaneous administration of misoprostol during sensitization inhibited allergic inflammation. PGE₂ decreased cytokine production and inhibited signal transducer and activator of transcription 6 phosphorylation by CD3/CD28-stimulated CD4(+) T cells. Coculture of flow cytometry-sorted splenic CD4(+) T cells and CD11c(+) dendritic cells from WT or EP2(-/-) mice suggested that the increased IL-13 production in EP2(-/-) mice was due to the lack of EP2 specifically on T cells. Adoptive transfer of CD4(+) EP2(-/-) T cells caused greater cytokine production in the lungs of WT mice than did transfer of WT CD4(+) T cells.

Conclusion: We conclude that the PGE2-EP2 axis is an important endogenous brake on allergic airway inflammation and primarily targets T cells and that its agonism represents a potential novel therapeutic approach to asthma.

Keywords: Asthma; BALF; Bronchoalveolar lavage fluid; CD4 T cells; Cyclic AMP; DC; DMSO; Dendritic cell; Dimethyl sulfoxide; E prostanoid; EP; Epac; Guanine nucleotide exchange protein directly activated by cAMP; NSAID; Nonsteroidal anti-inflammatory drug; OVA; Ovalbumin; PG; PKA; Prostaglandin; Protein kinase A; STAT; Signal transducer and activator of transcription; WT; Wild-type; allergic sensitization; cAMP; prostaglandin E(2).

Publication types

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

MeSH terms

  • Adoptive Transfer
  • Allergens
  • Animals
  • Asthma / immunology*
  • Bronchoalveolar Lavage Fluid / cytology
  • Bronchoalveolar Lavage Fluid / immunology
  • CD4-Positive T-Lymphocytes / immunology*
  • Cells, Cultured
  • Cytokines / immunology
  • Dendritic Cells / immunology
  • Dinoprostone / immunology*
  • Lymph Nodes / immunology
  • Male
  • Mice
  • Mice, Knockout
  • Misoprostol / pharmacology
  • Ovalbumin
  • Pneumonia / immunology*
  • Receptors, Prostaglandin E, EP2 Subtype / genetics
  • Receptors, Prostaglandin E, EP2 Subtype / immunology*
  • Spleen / immunology

Substances

  • Allergens
  • Cytokines
  • Receptors, Prostaglandin E, EP2 Subtype
  • Misoprostol
  • Ovalbumin
  • Dinoprostone