MicroRNA-24 antagonism prevents renal ischemia reperfusion injury

J Am Soc Nephrol. 2014 Dec;25(12):2717-29. doi: 10.1681/ASN.2013121329. Epub 2014 May 22.

Abstract

Ischemia-reperfusion (I/R) injury of the kidney is a major cause of AKI. MicroRNAs (miRs) are powerful regulators of various diseases. We investigated the role of apoptosis-associated miR-24 in renal I/R injury. miR-24 was upregulated in the kidney after I/R injury of mice and in patients after kidney transplantation. Cell-sorting experiments revealed a specific miR-24 enrichment in renal endothelial and tubular epithelial cells after I/R induction. In vitro, anoxia/hypoxia induced an enrichment of miR-24 in endothelial and tubular epithelial cells. Transient overexpression of miR-24 alone induced apoptosis and altered functional parameters in these cells, whereas silencing of miR-24 ameliorated apoptotic responses and rescued functional parameters in hypoxic conditions. miR-24 effects were mediated through regulation of H2A histone family, member X, and heme oxygenase 1, which were experimentally validated as direct miR-24 targets through luciferase reporter assays. In vitro, adenoviral overexpression of miR-24 targets lacking miR-24 binding sites along with miR-24 precursors rescued various functional parameters in endothelial and tubular epithelial cells. In vivo, silencing of miR-24 in mice before I/R injury resulted in a significant improvement in survival and kidney function, a reduction of apoptosis, improved histologic tubular epithelial injury, and less infiltration of inflammatory cells. miR-24 also regulated heme oxygenase 1 and H2A histone family, member X, in vivo. Overall, these results indicate miR-24 promotes renal ischemic injury by stimulating apoptosis in endothelial and tubular epithelial cell. Therefore, miR-24 inhibition may be a promising future therapeutic option in the treatment of patients with ischemic AKI.

Keywords: acute renal failure; apoptosis; endothelium; heme oxygenase; ischemia-reperfusion; proximal tubule.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Apoptosis
  • Binding Sites
  • Endothelial Cells / cytology
  • Endothelium / pathology
  • Epithelial Cells / metabolism
  • Female
  • Gene Silencing
  • Heme Oxygenase (Decyclizing) / metabolism
  • Heme Oxygenase-1 / metabolism
  • Histones / metabolism
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Inflammation / metabolism
  • Kidney / metabolism*
  • Kidney / pathology*
  • Kidney Tubules / metabolism*
  • Kidney Tubules / pathology
  • Male
  • Mice
  • MicroRNAs / antagonists & inhibitors*
  • MicroRNAs / genetics
  • Middle Aged
  • Receptors, Lysosphingolipid / metabolism
  • Reperfusion Injury / pathology*
  • Sphingosine-1-Phosphate Receptors

Substances

  • Histones
  • MIRN24 microRNA, human
  • MicroRNAs
  • Mirn24 microRNA, mouse
  • Receptors, Lysosphingolipid
  • S1PR1 protein, human
  • S1pr1 protein, mouse
  • Sphingosine-1-Phosphate Receptors
  • Heme Oxygenase (Decyclizing)
  • Heme Oxygenase-1