Cathelicidin LL-37 induces time-resolved release of LTB4 and TXA2 by human macrophages and triggers eicosanoid generation in vivo

FASEB J. 2014 Aug;28(8):3456-67. doi: 10.1096/fj.14-251306. Epub 2014 Apr 15.

Abstract

In humans, LL-37 and eicosanoids are important mediators of inflammation and immune responses. Here we report that LL-37 promotes leukotriene B4 (LTB4) and thromboxane A2 (TXA2) generation by human monocyte-derived macrophages (HMDMs). LL-37 evokes calcium mobilization apparently via the P2X7 receptor (P2X7R), activation of ERK1/2 and p38 MAPKs, as well as cytosolic phospholipase A2 (cPLA2) and 5-lipoxygenase in HMDMs, leading to an early (1 h) release of LTB4. Similarly, TXA2 production at an early time involved the same signaling sequence along an LL-37-P2X7R-cPLA2-cyclooxygenase-1 (COX-1) axis. However, at later (6-8 h) time points, internalized LL-37 up-regulates COX-2 expression, promoting TXA2 production. Furthermore, intraperitoneal injection of mice with murine cathelicidin-related antimicrobial peptide (mCRAMP) induces significantly higher levels of LTB4 and TXA2 in mouse ascites rich in macrophages. Conversely, cathelicidin-deficient (Cnlp(-/-)) mice produce much less LTB4 and TXB2 in vivo in response to TNF-α compared with control mice. We conclude that LL-37 elicits a biphasic release of eicosanoids in macrophages with early, Ca(2+)-dependent formation of LTB4 and TXA2 followed by a late peak of TXA2, generated via induction of COX-2 by internalized LL-37, thus allowing eicosanoid production in a temporally controlled manner. Moreover, our findings provide evidence that LL-37 is an endogenous regulator of eicosanoid-dependent inflammatory responses in vivo.

Keywords: P2X7R; antimicrobial peptides; inflammation; leukotriene; thromboxane.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Antimicrobial Cationic Peptides / deficiency
  • Antimicrobial Cationic Peptides / physiology*
  • Arachidonate 5-Lipoxygenase / metabolism
  • Calcium Signaling
  • Cathelicidins / deficiency
  • Cathelicidins / physiology
  • Cathelicidins / toxicity
  • Cells, Cultured
  • Eicosanoids / biosynthesis*
  • Humans
  • Inflammation / physiopathology
  • Leukotriene B4 / metabolism*
  • MAP Kinase Signaling System
  • Macrophages / drug effects*
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Molecular Sequence Data
  • Peritonitis / chemically induced
  • Peritonitis / metabolism*
  • Peritonitis / pathology
  • Phospholipases A2, Cytosolic / metabolism
  • Phosphorylation
  • Prostaglandin-Endoperoxide Synthases / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Protein Processing, Post-Translational
  • Receptors, Purinergic P2X7 / physiology
  • Recombinant Proteins / toxicity
  • Thromboxane A2 / metabolism*
  • Tumor Necrosis Factor-alpha / toxicity

Substances

  • Antimicrobial Cationic Peptides
  • Cathelicidins
  • Eicosanoids
  • Protein Kinase Inhibitors
  • Receptors, Purinergic P2X7
  • Recombinant Proteins
  • Tumor Necrosis Factor-alpha
  • Leukotriene B4
  • Thromboxane A2
  • Arachidonate 5-Lipoxygenase
  • Prostaglandin-Endoperoxide Synthases
  • Phospholipases A2, Cytosolic