Autocrine secretion of 15d-PGJ2 mediates simvastatin-induced apoptotic burst in human metastatic melanoma cells

Br J Pharmacol. 2014 Dec;171(24):5708-27. doi: 10.1111/bph.12871.

Abstract

Background and purpose: Despite new therapeutic approaches, metastatic melanomas still have a poor prognosis. Statins reduce low-density lipoprotein cholesterol and exert anti-inflammatory and anti-proliferative actions. We have recently shown that simvastatin triggers an apoptotic burst in human metastatic melanoma cells by the synthesis of an autocrine factor.

Experimental approach: The current in vitro study was performed in human metastatic melanoma cell lines (A375, 518a2) and primary human melanocytes and melanoma cells. The secretome of simvastatin-stressed cells was analysed with two-dimensional difference gel electrophoresis and MS. The signalling pathways involved were analysed at the protein and mRNA level using pharmacological approaches and siRNA technology.

Key results: Simvastatin was shown to activate a stress cascade, leading to the synthesis of 15-deoxy-12,14-PGJ2 (15d-PGJ2 ), in a p38- and COX-2-dependent manner. Significant concentrations of 15d-PGJ2 were reached in the medium of melanoma cells, which were sufficient to activate caspase 8 and the mitochondrial pathway of apoptosis. Inhibition of lipocalin-type PGD synthase, a key enzyme for 15d-PGJ2 synthesis, abolished the apoptotic effect of simvastatin. Moreover, 15d-PGJ2 was shown to bind to the fatty acid-binding protein 5 (FABP5), which was up-regulated and predominantly detected in the secretome of simvastatin-stressed cells. Knockdown of FABP5 abolished simvastatin-induced activation of PPAR-γ and amplified the apoptotic response.

Conclusions and implications: We characterized simvastatin-induced activation of the 15d-PGJ2 /FABP5 signalling cascades, which triggered an apoptotic burst in melanoma cells but did not affect primary human melanocytes. These data support the rationale for the pharmacological targeting of 15d-PGJ2 in metastatic melanoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / drug effects*
  • Autocrine Communication
  • Caspase 8 / drug effects
  • Caspase 8 / metabolism
  • Cell Line, Tumor
  • Cells, Cultured
  • Fatty Acid-Binding Proteins / drug effects
  • Fatty Acid-Binding Proteins / genetics
  • Fatty Acid-Binding Proteins / metabolism
  • Gene Knockdown Techniques
  • Humans
  • Hydroxymethylglutaryl-CoA Reductase Inhibitors / pharmacology*
  • Intramolecular Oxidoreductases / antagonists & inhibitors
  • Lipocalins / antagonists & inhibitors
  • Melanocytes / drug effects*
  • Melanocytes / metabolism
  • Melanoma / metabolism*
  • Neoplasm Metastasis
  • Prostaglandin D2 / analogs & derivatives*
  • Prostaglandin D2 / metabolism
  • Simvastatin / pharmacology*

Substances

  • 15-deoxyprostaglandin J2
  • FABP5 protein, human
  • Fatty Acid-Binding Proteins
  • Hydroxymethylglutaryl-CoA Reductase Inhibitors
  • Lipocalins
  • Simvastatin
  • CASP8 protein, human
  • Caspase 8
  • Intramolecular Oxidoreductases
  • prostaglandin R2 D-isomerase
  • Prostaglandin D2