Inhibition of the Glycolytic Activator PFKFB3 in Endothelium Induces Tumor Vessel Normalization, Impairs Metastasis, and Improves Chemotherapy

Cancer Cell. 2016 Dec 12;30(6):968-985. doi: 10.1016/j.ccell.2016.10.006. Epub 2016 Nov 17.

Abstract

Abnormal tumor vessels promote metastasis and impair chemotherapy. Hence, tumor vessel normalization (TVN) is emerging as an anti-cancer treatment. Here, we show that tumor endothelial cells (ECs) have a hyper-glycolytic metabolism, shunting intermediates to nucleotide synthesis. EC haplo-deficiency or blockade of the glycolytic activator PFKFB3 did not affect tumor growth, but reduced cancer cell invasion, intravasation, and metastasis by normalizing tumor vessels, which improved vessel maturation and perfusion. Mechanistically, PFKFB3 inhibition tightened the vascular barrier by reducing VE-cadherin endocytosis in ECs, and rendering pericytes more quiescent and adhesive (via upregulation of N-cadherin) through glycolysis reduction; it also lowered the expression of cancer cell adhesion molecules in ECs by decreasing NF-κB signaling. PFKFB3-blockade treatment also improved chemotherapy of primary and metastatic tumors.

Keywords: angiogenesis; chemotherapy; glycolysis; metastasis; tumor endothelial cell metabolism; tumor vessel normalization.

Publication types

  • Comment

MeSH terms

  • Animals
  • Cadherins / genetics
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Cisplatin / administration & dosage*
  • Cisplatin / pharmacology
  • Drug Synergism
  • Drug Therapy
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology
  • Gene Expression Regulation, Neoplastic / drug effects
  • Glycolysis / drug effects
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Mice
  • Neoplasm Invasiveness
  • Neoplasm Metastasis
  • Neoplasm Transplantation
  • Neoplasms / blood supply
  • Neoplasms / drug therapy
  • Neoplasms / metabolism*
  • Phosphofructokinase-2 / antagonists & inhibitors*
  • Tamoxifen / administration & dosage*
  • Tamoxifen / pharmacology

Substances

  • Cadherins
  • Cdh2 protein, mouse
  • Tamoxifen
  • PFKFB3 protein, human
  • Phosphofructokinase-2
  • Cisplatin