The cathelicidin LL-37 activates human mast cells and is degraded by mast cell tryptase: counter-regulation by CXCL4

J Immunol. 2009 Aug 15;183(4):2223-31. doi: 10.4049/jimmunol.0803587. Epub 2009 Jul 22.

Abstract

The cathelicidin LL-37 represents a potent antimicrobial and cell-stimulating agent, most abundantly expressed in peripheral organs such as lung and skin during inflammation. Because mast cells (MC) overtake prominent immunomodulatory roles in these organs, we wondered whether interactions exist between MC and LL-37. In this study, we show for the first time to our knowledge that physiological concentrations of LL-37 induce degranulation in purified human lung MC. Intriguingly, as a consequence LL-37 rapidly undergoes limited cleavage by a released protease. The enzyme was identified as beta-tryptase by inhibitor studies and by comparison to the recombinant protease. Examining the resulting LL-37 fragments for their functional activity, we found that none of the typical capacities of intact LL-37, i.e., MC degranulation, bactericidal activity, and neutralization of LPS, were retained. Conversely, we found that another inflammatory protein, the platelet-derived chemokine CXCL4, protects LL-37 from cleavage by beta-tryptase. Interestingly, CXCL4 did not act as a direct enzyme inhibitor, but destabilized active tetrameric beta-tryptase by antagonizing the heparin component required for the integrity of the tetramer. Altogether our results suggest that interaction of LL-37 and MC initiates an effective feedback loop to limit cathelicidin activity during inflammation, whereas CXCL4 may represent a physiological counter-regulator of beta-tryptase activity.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antimicrobial Cationic Peptides
  • Cathelicidins / antagonists & inhibitors
  • Cathelicidins / metabolism*
  • Cathelicidins / physiology
  • Cell Degranulation / immunology
  • Cells, Cultured
  • Feedback, Physiological / immunology
  • Humans
  • Inflammation Mediators / antagonists & inhibitors
  • Inflammation Mediators / metabolism
  • Inflammation Mediators / physiology
  • Lung / enzymology
  • Lung / immunology
  • Lung / metabolism
  • Mast Cells / enzymology*
  • Mast Cells / immunology*
  • Mast Cells / metabolism
  • Platelet Factor 4 / physiology*
  • Protein Processing, Post-Translational / immunology
  • Tryptases / metabolism
  • Tryptases / physiology*

Substances

  • Antimicrobial Cationic Peptides
  • Cathelicidins
  • Inflammation Mediators
  • Platelet Factor 4
  • Tryptases