Increased metabolites of 5-lipoxygenase from hypoxic ovarian cancer cells promote tumor-associated macrophage infiltration

Oncogene. 2015 Mar 5;34(10):1241-52. doi: 10.1038/onc.2014.85. Epub 2014 Mar 24.

Abstract

5-lipoxygenase (5-LOX), a member of the lipoxygenase gene family, is a key enzyme assisting in the conversion of arachidonic acid to 5-HETE and leukotrienes. Tumor-associated macrophages (TAMs) have a critical role in the progression and metastasis of many tumors, including ovarian tumors. Moreover, TAMs are often found in a high density in the hypoxic areas of tumors. However, the relevant mechanisms have not been studied explicitly until now. In this study, we found that the expression of 5-LOX strongly correlated with the density of TAMs in hypoxic areas of human ovarian tumor tissues. In cultured ovarian cancer cells, 5-LOX metabolites were increased under hypoxic conditons. Increased 5-LOX metabolites from hypoxic ovarian cancer cells promoted migration and invasion of macrophages, which was further demonstrated to be mediated by the upregulation of matrix metalloproteinase (MMP)-7 expression through the p38 pathway. Besides, we also showed that 5-LOX metabolites enhanced the release of tumor necrosis factor (TNF-α) and heparin-binding epidermal growth factor-like growth factor through upregulation of MMP-7. Furthermore, in animal models, Zileuton (a selective and specific 5-LOX inhibitor) reduced the MMP-7 expression and the number of macrophages infiltrating in the xenograft. Our findings suggest for the first time that increased metabolites of 5-LOX from hypoxic ovarian cancer cells promote TAM infiltration. These results of this study have immediate translational implications for the therapeutic exploitation of TAMs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arachidonate 5-Lipoxygenase / metabolism*
  • Cell Line
  • Cell Line, Tumor
  • Chemotaxis, Leukocyte / drug effects
  • Chemotaxis, Leukocyte / immunology
  • Disease Models, Animal
  • Female
  • Heparin-binding EGF-like Growth Factor / metabolism
  • Heterografts
  • Humans
  • Hydroxyeicosatetraenoic Acids / metabolism
  • Hydroxyurea / analogs & derivatives
  • Hydroxyurea / pharmacology
  • Hypoxia / metabolism*
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Leukotriene B4 / metabolism
  • MAP Kinase Signaling System
  • Macrophages / drug effects
  • Macrophages / immunology
  • Macrophages / pathology*
  • Matrix Metalloproteinase 7 / metabolism
  • Mice
  • Neoplasm Metastasis
  • Ovarian Neoplasms / immunology
  • Ovarian Neoplasms / metabolism*
  • Ovarian Neoplasms / pathology*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Heparin-binding EGF-like Growth Factor
  • Hydroxyeicosatetraenoic Acids
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Tumor Necrosis Factor-alpha
  • Leukotriene B4
  • 5-hydroxy-6,8,11,14-eicosatetraenoic acid
  • Arachidonate 5-Lipoxygenase
  • Matrix Metalloproteinase 7
  • zileuton
  • Hydroxyurea