The antimicrobial peptide LL-37 induces synthesis and release of cysteinyl leukotrienes from human eosinophils--implications for asthma

Allergy. 2013 Mar;68(3):304-11. doi: 10.1111/all.12087. Epub 2013 Jan 18.

Abstract

Background: Eosinophils and their products, including leukotrienes and eosinophil cationic protein (ECP), are well-known mediators of inflammation and tissue damage in asthma. The antimicrobial peptide LL-37 exhibits a variety of immunomodulatory activities. However, the role of LL-37 in asthma has not been fully addressed. Here, we aim to investigate the effect of LL-37 on inducing inflammatory mediators in human eosinophils, probe the underlying mechanisms, and search for a clinical correlate.

Methods: Primary eosinophils were isolated from peripheral blood. Leukotriene and ECP levels were measured using EIAs or ELISAs. Activation of leukotriene-synthesizing enzymes and signaling kinases was analyzed by Western blot or immunofluorescent imaging. LL-37/its proform hCAP18 expression was analyzed by Western blot.

Results: LL-37, via formyl peptide receptor-2 (FPR-2), triggered the release of cysteinyl leukotrienes (cys-LTs) from eosinophils. The release was more prominent in cells primed with the eosinophilopoietic cytokine GM-CSF or IL-5 or cells from asthmatic patients. LL-37 stimulates lipid body formation and activates cys-LT-synthesizing enzymes by multiple mechanisms: enhancing cPLA(2) activity by pERK1/2-mediated phosphorylation and inducing intracellular translocation and assembly of 5-LO and LTC(4) S at perinuclear locations and lipid bodies. In addition to cys-LTs, LL-37 enhances ECP release from eosinophils via pERK1/2. The expression of hCAP18 and its release following leukotriene stimulation are significantly higher in eosinophils from asthmatics.

Conclusions: This study identifies LL-37 as an eosinophil-activating peptide that triggers release of inflammatory mediators. The clinical correlation suggests that LL-37/hCAP18 and its signaling pathway represent potential therapeutic targets for this disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Antimicrobial Cationic Peptides
  • Arachidonate 5-Lipoxygenase / metabolism
  • Asthma / immunology*
  • Asthma / metabolism*
  • Cathelicidins / pharmacology*
  • Cysteine / immunology
  • Cysteine / metabolism*
  • Eosinophil Cationic Protein / metabolism
  • Eosinophils / drug effects*
  • Eosinophils / immunology*
  • Female
  • Glutathione Transferase / metabolism
  • Group IV Phospholipases A2 / metabolism
  • Humans
  • Leukotrienes / immunology
  • Leukotrienes / metabolism*
  • Lipid Metabolism
  • Male
  • Middle Aged
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Phosphorylation / drug effects
  • Protein Binding
  • Protein Transport / drug effects
  • Receptors, Formyl Peptide / metabolism
  • Receptors, Lipoxin / metabolism
  • Signal Transduction / drug effects
  • Young Adult

Substances

  • Antimicrobial Cationic Peptides
  • Cathelicidins
  • FPR2 protein, human
  • Leukotrienes
  • Receptors, Formyl Peptide
  • Receptors, Lipoxin
  • cysteinyl-leukotriene
  • Arachidonate 5-Lipoxygenase
  • Glutathione Transferase
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Group IV Phospholipases A2
  • Eosinophil Cationic Protein
  • leukotriene-C4 synthase
  • Cysteine