Resveratrol prevents inflammation-dependent hepatic melanoma metastasis by inhibiting the secretion and effects of interleukin-18

J Transl Med. 2011 May 12:9:59. doi: 10.1186/1479-5876-9-59.

Abstract

Background: Implantation and growth of metastatic cancer cells at distant organs is promoted by inflammation-dependent mechanisms. A hepatic melanoma metastasis model where a majority of metastases are generated via interleukin-18-dependent mechanisms was used to test whether anti-inflammatory properties of resveratrol can interfere with mechanisms of metastasis.

Methods: Two experimental treatment schedules were used: 1) Mice received one daily oral dose of 1 mg/kg resveratrol after cancer cell injection and the metastasis number and volume were determined on day 12. 2) Mice received one daily oral dose of 1 mg/kg resveratrol along the 5 days prior to the injection of cancer cells and both interleukin-18 (IL-18) concentration in the hepatic blood and microvascular retention of luciferase-transfected B16M cells were determined on the 18th hour. In vitro, primary cultured hepatic sinusoidal endothelial cells were treated with B16M-conditioned medium to mimic their in vivo activation by tumor-derived factors and the effect of resveratrol on IL-18 secretion, on vascular cell adhesion molecule-1 (VCAM-1) expression and on tumor cell adhesion were studied. The effect of resveratrol on melanoma cell activation by IL-18 was also studied.

Results: Resveratrol remarkably inhibited hepatic retention and metastatic growth of melanoma cells by 50% and 75%, respectively. The mechanism involved IL-18 blockade at three levels: First, resveratrol prevented IL-18 augmentation in the blood of melanoma cell-infiltrated livers. Second, resveratrol inhibited IL-18-dependent expression of VCAM-1 by tumor-activated hepatic sinusoidal endothelium, preventing melanoma cell adhesion to the microvasculature. Third, resveratrol inhibited adhesion- and proliferation-stimulating effects of IL-18 on metastatic melanoma cells through hydrogen peroxide-dependent nuclear factor-kappaB translocation blockade on these cells.

Conclusions: These results demonstrate multiple sites for therapeutic intervention using resveratrol within the prometastatic microenvironment generated by tumor-induced hepatic IL-18, and suggest a remarkable effect of resveratrol in the prevention of inflammation-dependent melanoma metastasis in the liver.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Adhesion / drug effects
  • Cell Proliferation / drug effects
  • Endothelium / drug effects
  • Endothelium / metabolism
  • Endothelium / pathology
  • Inflammation / complications
  • Inflammation / prevention & control*
  • Interleukin-18 / metabolism*
  • Liver / blood supply
  • Liver / drug effects
  • Liver / pathology
  • Liver Neoplasms / complications
  • Liver Neoplasms / pathology*
  • Melanoma / complications
  • Melanoma / metabolism
  • Melanoma / prevention & control*
  • Melanoma / secondary*
  • Melanoma, Experimental / complications
  • Melanoma, Experimental / pathology
  • Mice
  • Mice, Inbred C57BL
  • Microvessels / drug effects
  • Microvessels / pathology
  • Models, Biological
  • Neoplasm Transplantation
  • Resveratrol
  • Stilbenes / pharmacology
  • Stilbenes / therapeutic use*
  • Tumor Microenvironment / drug effects
  • Vascular Cell Adhesion Molecule-1 / metabolism

Substances

  • Interleukin-18
  • Stilbenes
  • Vascular Cell Adhesion Molecule-1
  • Resveratrol