A regulatory microRNA network controls endothelial cell phenotypic switch during sprouting angiogenesis

Elife. 2020 Jan 24:9:e48095. doi: 10.7554/eLife.48095.

Abstract

Angiogenesis requires the temporal coordination of the proliferation and the migration of endothelial cells. Here, we investigated the regulatory role of microRNAs (miRNAs) in harmonizing angiogenesis processes in a three-dimensional in vitro model. We described a microRNA network which contributes to the observed down- and upregulation of proliferative and migratory genes, respectively. Global analysis of miRNA-target gene interactions identified two sub-network modules, the first organized in upregulated miRNAs connected with downregulated target genes and the second with opposite features. miR-424-5p and miR-29a-3p were selected for the network validation. Gain- and loss-of-function approaches targeting these microRNAs impaired angiogenesis, suggesting that these modules are instrumental to the temporal coordination of endothelial migration and proliferation. Interestingly, miR-29a-3p and its targets belong to a selective biomarker that is able to identify colorectal cancer patients who are responding to anti-angiogenic treatments. Our results provide a view of higher-order interactions in angiogenesis that has potential to provide diagnostic and therapeutic insights.

Keywords: VEGF; angiogenesis; cell biology; computational biology; human; microRNA; network; systems biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiogenesis Inhibitors / pharmacology
  • Angiogenesis Inhibitors / therapeutic use
  • Biomarkers, Tumor
  • Cells, Cultured
  • Colorectal Neoplasms / drug therapy
  • Endothelial Cells* / cytology
  • Endothelial Cells* / physiology
  • Gene Expression Regulation, Neoplastic / drug effects
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Neovascularization, Pathologic / metabolism*
  • Neovascularization, Physiologic* / genetics
  • Neovascularization, Physiologic* / physiology
  • Phenotype

Substances

  • Angiogenesis Inhibitors
  • Biomarkers, Tumor
  • MicroRNAs

Associated data

  • GEO/GSE116039
  • GEO/GSE115954
  • GEO/GSE115817
  • GEO/GSE129276
  • GEO/GSE53127