Novel tissue-specific mechanism of regulation of angiogenesis and cancer growth in response to hyperglycemia

J Am Heart Assoc. 2012 Dec;1(6):e005967. doi: 10.1161/JAHA.112.005967. Epub 2012 Dec 19.

Abstract

Background: Hyperglycemia is an independent risk factor for the development of vascular diabetic complications, which are characterized by endothelial dysfunction and tissue-specific aberrant angiogenesis. Tumor growth is also dependent on angiogenesis. Diabetes affects several cancers in a tissue-specific way. For example, it positively correlates with the incidence of breast cancer but negatively correlates with the incidence of prostate cancer. The tissue-specific molecular mechanisms activated by hyperglycemia that control angiogenesis are unknown. Here we describe a novel tissue- and cell-specific molecular pathway that is activated by high glucose and regulates angiogenesis.

Methods and results: We have identified microRNA 467 (miR-467) as a translational suppressor of thrombospondin-1 (TSP-1), a potent antiangiogenic protein that is implicated in the pathogenesis of several diabetic complications. miR-467 was upregulated by hyperglycemia in a tissue-specific manner. It was induced by high glucose in microvascular endothelial cells and in breast cancer cells, where it suppressed the production of TSP-1 by sequestering mRNA in the nonpolysomal fraction. Mutation of the miR-467 binding site in TSP-1 3' UTR or miR-467 inhibitor relieved the translational silencing and restored TSP-1 production. In in vivo angiogenesis models, miR-467 promoted the growth of blood vessels, and TSP-1 was the main mediator of this effect. Breast cancer tumors showed increased growth in hyperglycemic mice and expressed higher levels of miR-467. The antagonist of miR-467 prevented the hyperglycemia-induced tumor growth.

Conclusions: Our results demonstrate that miR-467 is implicated in the control of angiogenesis in response to high glucose, which makes it an attractive tissue-specific potential target for therapeutic regulation of aberrant angiogenesis and cancer growth in diabetes.

Keywords: complications of diabetes; microRNA; thrombospondin‐1; translational regulation.

Publication types

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

MeSH terms

  • Animals
  • Blotting, Northern
  • Blotting, Western
  • Breast Neoplasms / etiology
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / physiopathology
  • Cell Line, Tumor
  • Cell Transformation, Neoplastic / pathology*
  • Cells, Cultured
  • DNA Primers / chemistry
  • Diabetes Mellitus / etiology
  • Diabetes Mellitus / physiopathology*
  • Female
  • Humans
  • Hyperglycemia / complications
  • Hyperglycemia / metabolism
  • Hyperglycemia / physiopathology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / antagonists & inhibitors
  • MicroRNAs / genetics
  • MicroRNAs / isolation & purification
  • MicroRNAs / metabolism
  • MicroRNAs / physiology*
  • Neovascularization, Physiologic / physiology*
  • Prostatic Neoplasms / etiology
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / physiopathology
  • Real-Time Polymerase Chain Reaction
  • Thrombospondin 1 / metabolism
  • Transfection
  • Up-Regulation

Substances

  • DNA Primers
  • MIRN467 microRNA, mouse
  • MicroRNAs
  • Thrombospondin 1