Knockout of HIF-1α in tumor-associated macrophages enhances M2 polarization and attenuates their pro-angiogenic responses

Carcinogenesis. 2010 Oct;31(10):1863-72. doi: 10.1093/carcin/bgq088. Epub 2010 Apr 28.

Abstract

Tumor-associated macrophages (TAMs) constitute major infiltrates of solid tumors and express a marker profile that characterizes alternatively activated macrophages (MФs). TAMs accumulate in hypoxic tumor regions, express high amounts of hypoxia-inducible factor-1 (HIF-1) and contribute to tumor angiogenesis and invasiveness. However, the precise role of HIF-1 on MФ infiltration and phenotype alterations remains poorly defined. Therefore, we cocultured wild type (wt) versus HIF-1α(-/-) MФs with tumor spheroids. Both, wt and HIF-1α(-/-) MФs, infiltrated hypoxic regions of tumor spheroids at equal rates and got alternatively activated. Interestingly, significantly higher amounts of HIF-1α(-/-) MФs expressed the TAM markers CD206 and stabilin-1 compared with wt phagocytes. Stimulation of infiltrated TAMs with lipopolysaccharide (LPS)/interferon-γ revealed a reduced expression of the pro-inflammatory markers interleukin (IL)-6, tumor necrosis factor-α and inducible nitric oxide synthase in HIF-1α(-/-) MФs. Furthermore, HIF-1α(-/-) MФs were less cytotoxic toward tumor cells. Although infiltration of MФs increased the invasive potential of tumor spheroids independently of HIF-1, the ability to stimulate differentiation of stem cells toward CD31-positive cells was triggered by wt but not by HIF-1α(-/-) MФs. Our data suggest that HIF-1α-deficient MФs develop a more prominent TAM marker profile accompanied by reduced cytotoxicity, whereas HIF-1 seems indispensable for the angiogenesis-promoting properties of TAMs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Adhesion Molecules, Neuronal / analysis
  • Cell Line, Tumor
  • Cell Polarity*
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / physiology*
  • Interferon-gamma / pharmacology
  • Interleukin-6 / biosynthesis
  • Lectins, C-Type / analysis
  • Lipopolysaccharides / pharmacology
  • Macrophages / physiology*
  • Mannose Receptor
  • Mannose-Binding Lectins / analysis
  • Mice
  • Neoplasm Invasiveness
  • Neoplasms / blood supply*
  • Neoplasms / pathology
  • Neovascularization, Pathologic / etiology*
  • Nitric Oxide Synthase Type II / biosynthesis
  • Platelet Endothelial Cell Adhesion Molecule-1 / analysis
  • Receptors, Cell Surface / analysis
  • Receptors, Lymphocyte Homing / analysis
  • Spheroids, Cellular / pathology
  • Tumor Necrosis Factor-alpha / biosynthesis

Substances

  • Cell Adhesion Molecules, Neuronal
  • HIF1A protein, human
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Interleukin-6
  • Lectins, C-Type
  • Lipopolysaccharides
  • Mannose Receptor
  • Mannose-Binding Lectins
  • Platelet Endothelial Cell Adhesion Molecule-1
  • Receptors, Cell Surface
  • Receptors, Lymphocyte Homing
  • STAB1 protein, human
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma
  • Nitric Oxide Synthase Type II