Interleukin-10 inhibits Mycobacterium bovis bacillus Calmette-Guérin (BCG)-induced macrophage cytotoxicity against bladder cancer cells

Clin Exp Immunol. 2010 Jun;160(3):359-68. doi: 10.1111/j.1365-2249.2010.04105.x. Epub 2010 Feb 10.

Abstract

The mechanisms underlying bacillus Calmette-Guérin (BCG) immunotherapy of bladder cancer currently remain elusive. Previously, we demonstrated that macrophages were cytotoxic to bladder cancer cells upon BCG stimulation in vitro. However, macrophages from C57BL/6 mice were less potent than those from C3H/HeN mice for the killing of bladder cancer cells. This study was to determine whether interleukin (IL)-10 produced by macrophages in response to BCG is a causative factor for the reduced cytotoxicity in BCG-stimulated C57BL/6 macrophages. Thioglycollate-elicited peritoneal macrophages were prepared and analysed for the BCG induction of cytotoxicity, cytokines and nitric oxide (NO) in vitro. Compared to BCG-stimulated C3H/HeN macrophages, BCG-stimulated C57BL/6 macrophages exhibited reduced killing of bladder cancer MBT-2 cells and MB49 cells. Studies demonstrated further that BCG-stimulated C57BL/6 macrophages produced a high level of IL-10, which correlated with reduced production of tumour necrosis factor (TNF)-alpha, IL-6 and NO. Neutralizing endogenous IL-10 during BCG stimulation increased C57BL/6 macrophage cytotoxicity against MB49 cells by 3.2-fold, along with increased production of TNF-alpha by 6.4-fold and NO by 3.6-fold, respectively. Macrophages from C57BL/6 IL-10(-/-) mice also exhibited increased killing of MB49 cells and production of TNF-alpha and NO upon BCG stimulation. In addition, supplementation of exogenous recombinant IL-10 reduced BCG-induced C3H/HeN macrophage cytotoxicity against both MBT-2 cells and MB49 cells in a dose-dependent manner. These results reveal the inhibitory role of IL-10 in BCG-induced macrophage cytotoxicity, suggesting that blockage of IL-10 may potentially enhance the effect of BCG in the treatment of bladder cancer patients.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Female
  • Humans
  • Immunotherapy / methods
  • Interleukin-10 / genetics
  • Interleukin-10 / immunology*
  • Interleukin-10 / pharmacology
  • Interleukin-6 / genetics
  • Interleukin-6 / immunology
  • Macrophage Activation / drug effects
  • Macrophage Activation / genetics
  • Macrophage Activation / immunology*
  • Macrophages, Peritoneal / immunology*
  • Mice
  • Mice, Knockout
  • Mycobacterium bovis / immunology*
  • Nitric Oxide / genetics
  • Nitric Oxide / immunology
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / immunology
  • Urinary Bladder Neoplasms / immunology*
  • Urinary Bladder Neoplasms / therapy

Substances

  • Interleukin-6
  • Tumor Necrosis Factor-alpha
  • Interleukin-10
  • Nitric Oxide