Dysregulated fatty acid metabolism in nasal polyp-derived eosinophils from patients with chronic rhinosinusitis

Allergy. 2019 Jun;74(6):1113-1124. doi: 10.1111/all.13726. Epub 2019 Feb 26.

Abstract

Background: Eosinophils are multifunctional granulocytes capable of releasing various cytokines, chemokines, and lipid mediators. We previously reported dysregulated fatty acid metabolism in peripheral blood-derived eosinophils from patients with severe asthma. However, functional characteristics of eosinophils present in allergic inflammatory tissues remain largely uncharacterized.

Methods: We established a method for isolating CD69hi CCR3low CXCR4- siglec-8int eosinophils from nasal polyps of patients with eosinophilic rhinosinusitis (NP-EOS). Multi-omics analysis including lipidomics, proteomics, and transcriptomics was performed to analyze NP-EOS as compared to peripheral blood-derived eosinophils from healthy subjects (PB-EOS).

Results: Lipidomic analysis revealed impaired synthesis of prostaglandins and 15-lipoxygenase (15-LOX)-derived mediators, and selective upregulation of leukotriene D4 production. Furthermore, proteomics and transcriptomics revealed changes in the expression of specific enzymes (GGT5, DPEP2, and 15-LOX) responsible for dysregulated lipid metabolism. Ingenuity pathway analysis indicated the importance of type 2 cytokines and pattern recognition receptor pathways. Stimulation of PB-EOS with eosinophil activators IL-5, GM-CSF, and agonists of TLR2 and NOD2 mimicked the observed changes in lipid metabolism.

Conclusion: Inflammatory tissue-derived eosinophils possess a specific phenotype with dysregulated fatty acid metabolism that may be targeted therapeutically to control eosinophilic inflammatory diseases.

Keywords: GGT5; chronic rhinosinusitis; human eosinophil; lipid mediator; multi-omics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Arachidonate 15-Lipoxygenase / metabolism
  • Blood Donors
  • Cells, Cultured
  • Chronic Disease
  • Cytokines / pharmacology
  • Eosinophils / drug effects
  • Eosinophils / metabolism*
  • Fatty Acids / metabolism*
  • Female
  • Humans
  • Leukotriene D4 / metabolism
  • Male
  • Middle Aged
  • Nasal Polyps / immunology
  • Nasal Polyps / pathology*
  • Phenotype
  • Prostaglandin-Endoperoxide Synthases / metabolism
  • Proteome
  • Rhinitis / metabolism*
  • Rhinitis / pathology
  • Signal Transduction / drug effects
  • Sinusitis / metabolism*
  • Sinusitis / pathology
  • Transcriptome
  • gamma-Glutamyltransferase / metabolism

Substances

  • Cytokines
  • Fatty Acids
  • Proteome
  • Leukotriene D4
  • ALOX15B protein, human
  • Arachidonate 15-Lipoxygenase
  • Prostaglandin-Endoperoxide Synthases
  • gamma-Glutamyltransferase