MicroRNA-24 regulates vascularity after myocardial infarction

Circulation. 2011 Aug 9;124(6):720-30. doi: 10.1161/CIRCULATIONAHA.111.039008. Epub 2011 Jul 25.

Abstract

Background: Myocardial infarction leads to cardiac remodeling and development of heart failure. Insufficient myocardial capillary density after myocardial infarction has been identified as a critical event in this process, although the underlying mechanisms of cardiac angiogenesis are mechanistically not well understood.

Methods and results: Here, we show that the small noncoding RNA microRNA-24 (miR-24) is enriched in cardiac endothelial cells and considerably upregulated after cardiac ischemia. MiR-24 induces endothelial cell apoptosis, abolishes endothelial capillary network formation on Matrigel, and inhibits cell sprouting from endothelial spheroids. These effects are mediated through targeting of the endothelium-enriched transcription factor GATA2 and the p21-activated kinase PAK4, which were identified by bioinformatic predictions and validated by luciferase gene reporter assays. Respective downstream signaling cascades involving phosphorylated BAD (Bcl-XL/Bcl-2-associated death promoter) and Sirtuin1 were identified by transcriptome, protein arrays, and chromatin immunoprecipitation analyses. Overexpression of miR-24 or silencing of its targets significantly impaired angiogenesis in zebrafish embryos. Blocking of endothelial miR-24 limited myocardial infarct size of mice via prevention of endothelial apoptosis and enhancement of vascularity, which led to preserved cardiac function and survival.

Conclusions: Our findings indicate that miR-24 acts as a critical regulator of endothelial cell apoptosis and angiogenesis and is suitable for therapeutic intervention in the setting of ischemic heart disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Arterioles / pathology
  • Capillaries / pathology
  • Cell Hypoxia
  • Cells, Cultured / drug effects
  • Cells, Cultured / metabolism
  • Collagen
  • Drug Combinations
  • Drug Evaluation, Preclinical
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • GATA2 Transcription Factor / biosynthesis
  • GATA2 Transcription Factor / genetics
  • Gene Expression Profiling
  • Heart Failure / etiology
  • Heme Oxygenase-1 / biosynthesis
  • Heme Oxygenase-1 / genetics
  • Laminin
  • Male
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / antagonists & inhibitors
  • MicroRNAs / genetics
  • MicroRNAs / physiology*
  • Myocardial Infarction / complications
  • Myocardial Infarction / genetics
  • Myocardial Infarction / physiopathology*
  • Neovascularization, Physiologic / drug effects
  • Neovascularization, Physiologic / genetics
  • Oligoribonucleotides / pharmacology
  • Proteoglycans
  • RNA Interference
  • RNA, Small Interfering / pharmacology
  • RNA, Small Interfering / therapeutic use
  • Spheroids, Cellular
  • Ventricular Remodeling
  • Zebrafish / embryology
  • Zebrafish Proteins / biosynthesis
  • Zebrafish Proteins / genetics
  • p21-Activated Kinases / biosynthesis
  • p21-Activated Kinases / genetics

Substances

  • Drug Combinations
  • GATA2 Transcription Factor
  • GATA2 protein, human
  • Gata2a protein, zebrafish
  • Laminin
  • MIRN24 microRNA, human
  • MicroRNAs
  • Mirn24 microRNA, mouse
  • Oligoribonucleotides
  • Proteoglycans
  • RNA, Small Interfering
  • Zebrafish Proteins
  • matrigel
  • Collagen
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • PAK4 protein, human
  • p21-Activated Kinases