A MicroRNA302-367-Erk1/2-Klf2-S1pr1 Pathway Prevents Tumor Growth via Restricting Angiogenesis and Improving Vascular Stability

Circ Res. 2017 Jan 6;120(1):85-98. doi: 10.1161/CIRCRESAHA.116.309757. Epub 2016 Oct 18.

Abstract

Rationale: Angiogenic hypersprouting and leaky vessels are essential for tumor growth. MicroRNAs have unique therapeutic advantages by targeting multiple pathways of tumor-associated angiogenesis, but the function of individual miRNAs of miR302-367 cluster in angiogenesis and tumors has not yet been fully evaluated.

Objective: To investigate the functions of miR302-367 in developmental angiogenesis and tumor angiogenesis and explore the molecular mechanisms of microRNA for the treatment of pathological neovascularization-related diseases.

Methods and results: Here, we show that miR302-367 elevation in endothelial cells reduces retinal sprouting angiogenesis and promotes vascular stability in vivo, ex vivo, and in vitro. Erk1/2 is identified as direct target of miR302-367, and downregulation of Erk1/2 on miR302-367 elevation in endothelial cells increases the expression of Klf2 and in turn S1pr1 and its downstream target VE-cadherin, suppressing angiogenesis and improving vascular stability. Conversely, both pharmacological blockade and genetic deletion of S1pr1 in endothelial cells reverse the antiangiogenic and vascular stabilizing effect of miR302-367 in mice. Tumor angiogenesis shares features of developmental angiogenesis, and endothelial specific elevation of miR302-367 reduces tumor growth by restricting sprout angiogenesis and decreasing vascular permeability via the same Erk1/2-Klf2-S1pr1 pathways.

Conclusions: MiR302-367 regulation of an Erk1/2-Klf2-S1pr1 pathway in the endothelium advances our understanding of angiogenesis, meanwhile also provides opportunities for therapeutic intervention of tumor growth.

Keywords: angiogenesis; blood vessel tumor; endothelial cells; microRNAs.

MeSH terms

  • Angiogenesis Inhibitors / biosynthesis
  • Animals
  • Carcinoma, Lewis Lung
  • Coculture Techniques
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Kruppel-Like Transcription Factors / biosynthesis*
  • MAP Kinase Signaling System / physiology*
  • Melanoma, Experimental
  • Mice
  • Mice, Transgenic
  • MicroRNAs / biosynthesis*
  • Neoplasms / metabolism*
  • Neoplasms / pathology
  • Neoplasms / prevention & control
  • Neovascularization, Pathologic / metabolism*
  • Neovascularization, Pathologic / pathology
  • Neovascularization, Pathologic / prevention & control
  • Receptors, Lysosphingolipid / biosynthesis*
  • Sphingosine-1-Phosphate Receptors
  • Xenograft Model Antitumor Assays / methods

Substances

  • Angiogenesis Inhibitors
  • Klf2 protein, mouse
  • Kruppel-Like Transcription Factors
  • MIRN302 microRNA, mouse
  • MIRN367 microRNA, mouse
  • MicroRNAs
  • Receptors, Lysosphingolipid
  • S1pr1 protein, mouse
  • Sphingosine-1-Phosphate Receptors