Global microRNA depletion suppresses tumor angiogenesis

Genes Dev. 2014 May 15;28(10):1054-67. doi: 10.1101/gad.239681.114. Epub 2014 May 1.

Abstract

MicroRNAs delicately regulate the balance of angiogenesis. Here we show that depletion of all microRNAs suppresses tumor angiogenesis. We generated microRNA-deficient tumors by knocking out Dicer1. These tumors are highly hypoxic but poorly vascularized, suggestive of deficient angiogenesis signaling. Expression profiling revealed that angiogenesis genes were significantly down-regulated as a result of the microRNA deficiency. Factor inhibiting hypoxia-inducible factor 1 (HIF-1), FIH1, is derepressed under these conditions and suppresses HIF transcription. Knocking out FIH1 using CRISPR/Cas9-mediated genome engineering reversed the phenotypes of microRNA-deficient cells in HIF transcriptional activity, VEGF production, tumor hypoxia, and tumor angiogenesis. Using multiplexed CRISPR/Cas9, we deleted regions in FIH1 3' untranslated regions (UTRs) that contain microRNA-binding sites, which derepresses FIH1 protein and represses hypoxia response. These data suggest that microRNAs promote tumor responses to hypoxia and angiogenesis by repressing FIH1.

Keywords: CRISPR/Cas9; Dicer; angiogenesis; gene regulation; hypoxia; microRNA.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Cell Line, Tumor
  • DEAD-box RNA Helicases / genetics*
  • DEAD-box RNA Helicases / metabolism*
  • Disease Models, Animal
  • Gene Expression Regulation, Neoplastic*
  • Gene Knockout Techniques
  • Genotype
  • Mice
  • Mice, Nude
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism*
  • Neovascularization, Pathologic / genetics*
  • Neovascularization, Pathologic / metabolism
  • Ribonuclease III / genetics*
  • Ribonuclease III / metabolism*
  • Transcriptome

Substances

  • MicroRNAs
  • Dicer1 protein, mouse
  • Ribonuclease III
  • DEAD-box RNA Helicases

Associated data

  • GEO/GSE57043