Dual effect of the novel peptide antagonist K-14585 on proteinase-activated receptor-2-mediated signalling

Br J Pharmacol. 2009 Dec;158(7):1695-704. doi: 10.1111/j.1476-5381.2009.00415.x.

Abstract

Background and purpose: Here we have examined the effects of the novel peptide antagonist N-[1-(2,6-dichlorophenyl)methyl]-3-(1-pyrrolidinylmethyl)-1H-indol-5-yl]aminocarbonyl]-glycinyl-L-lysinyl-L-phenylalanyl-N-benzhydrylamide (K-14585) on proteinase-activated receptor (PAR)(2)-mediated intracellular signalling events.

Experimental approach: Using NCTC2544 cells expressing PAR(2), we assessed the effects of K-14585 on PAR(2)-mediated [(3)H] inositol phosphate accumulation, MAP kinase activation, p65 NFkappaB phosphorylation and DNA binding and IL-8 production.

Key results: Pretreatment with K-14585 (5 microM) inhibited [(3)H] inositol phosphate levels stimulated by PAR(2)-activating peptide Ser-Leu-Ile-Gly-Lys-Val (SLIGKV-OH) in PAR(2)-expressing NCTC2544 cells. K-14585 pretreatment did not influence PAR(2)-mediated extracellular regulated kinase activation but inhibited p38 MAP kinase phosphorylation. At a higher concentration (30 microM), K-14585 alone stimulated p38 MAP kinase activation. These effects were replicated in EAhy926 cells, endogenously expressing PAR(2), but not in parental or PAR(4)-expressing NCTC2544 cells, suggesting these effects were PAR(2)-dependent. SLIGKV-mediated stimulation of p38 MAP kinase phosphorylation was substantially reduced by the G(q/11) inhibitor YM-254890, without affecting K-14585-mediated phosphorylation. Pretreatment with K-14585 inhibited PAR(2)-mediated p65 NFkappaB phosphorylation and NFkappaB-DNA binding. K-14585 (30 microM) alone stimulated comparable NFkappaB reporter activity to SLIGKV-OH. K-14585 inhibited SLIGKV-stimulated IL-8 production, but given alone increased IL-8. While SLIGKV-induced IL-8 formation was reduced by both SB203580 and YM-254890, the response to K-14585 was sensitive to SB203580 but not YM-254890.

Conclusions and implications: These data reveal that K-14585 has a duality of action functioning both as an antagonist and agonist due to either partial agonist actions or possible agonist-directed signalling. The data also suggest two modes of p38 MAP kinase activation emanating from PAR(2), one G(q/11)-dependent and the other G(q/11)-independent.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Dose-Response Relationship, Drug
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • GTP-Binding Protein alpha Subunits, Gq-G11 / metabolism
  • Humans
  • Imidazoles / pharmacology
  • Oligopeptides / administration & dosage
  • Oligopeptides / pharmacology*
  • Peptides, Cyclic / pharmacology
  • Phosphorylation
  • Pyridines / pharmacology
  • Receptor, PAR-2 / agonists
  • Receptor, PAR-2 / antagonists & inhibitors*
  • Receptor, PAR-2 / metabolism
  • Signal Transduction / drug effects*
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • Imidazoles
  • K-14585
  • Oligopeptides
  • Peptides, Cyclic
  • Pyridines
  • Receptor, PAR-2
  • YM-254890
  • seryl-leucyl-isoleucyl--glycyl-lysyl-valine
  • p38 Mitogen-Activated Protein Kinases
  • GTP-Binding Protein alpha Subunits, Gq-G11
  • SB 203580