The myc-miR-17~92 axis blunts TGF{beta} signaling and production of multiple TGF{beta}-dependent antiangiogenic factors

Cancer Res. 2010 Oct 15;70(20):8233-46. doi: 10.1158/0008-5472.CAN-10-2412. Epub 2010 Oct 12.

Abstract

c-Myc stimulates angiogenesis in tumors through mechanisms that remain incompletely understood. Recent work indicates that c-Myc upregulates the miR-17∼92 microRNA cluster and downregulates the angiogenesis inhibitor thrombospondin-1, along with other members of the thrombospondin type 1 repeat superfamily. Here, we show that downregulation of the thrombospondin type 1 repeat protein clusterin in cells overexpressing c-Myc and miR-17∼92 promotes angiogenesis and tumor growth. However, clusterin downregulation by miR-17∼92 is indirect. It occurs as a result of reduced transforming growth factor-β (TGFβ) signaling caused by targeting of several regulatory components in this signaling pathway. Specifically, miR-17-5p and miR-20 reduce the expression of the type II TGFβ receptor and miR-18 limits the expression of Smad4. Supporting these results, in human cancer cell lines, levels of the miR-17∼92 primary transcript MIR17HG negatively correlate with those of many TGFβ-induced genes that are not direct targets of miR-17∼92 (e.g., clusterin and angiopoietin-like 4). Furthermore, enforced expression of miR-17∼92 in MIR17HG(low) cell lines (e.g., glioblastoma) results in impaired gene activation by TGFβ. Together, our results define a pathway in which c-Myc activation of miR-17∼92 attenuates the TGFβ signaling pathway to shut down clusterin expression, thereby stimulating angiogenesis and tumor cell growth.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Angiogenesis Inhibitors / antagonists & inhibitors
  • Angiogenesis Inhibitors / biosynthesis*
  • Animals
  • Base Sequence
  • Clusterin / genetics
  • Colonic Neoplasms / genetics
  • Down-Regulation
  • Genes, Reporter
  • Humans
  • Luciferases / genetics
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / genetics*
  • MicroRNAs / physiology
  • Molecular Sequence Data
  • Mutation
  • Proto-Oncogene Proteins c-myc / physiology*
  • Receptors, Transforming Growth Factor beta / genetics
  • Ribonuclease III / genetics
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / physiology*
  • Untranslated Regions

Substances

  • Angiogenesis Inhibitors
  • Clusterin
  • MIRN17 microRNA, human
  • MIRN92 microRNA, human
  • MicroRNAs
  • Mirn92 microRNA, mouse
  • Proto-Oncogene Proteins c-myc
  • Receptors, Transforming Growth Factor beta
  • Transforming Growth Factor beta
  • Untranslated Regions
  • Luciferases
  • Ribonuclease III