Postinjury Inhibition of miR-181a Promotes Restoration of Hippocampal CA1 Neurons after Transient Forebrain Ischemia in Rats

eNeuro. 2019 Aug 29;6(4):ENEURO.0002-19.2019. doi: 10.1523/ENEURO.0002-19.2019. Print 2019 Jul/Aug.

Abstract

The cellular and molecular mechanisms regulating postinjury neurogenesis in the adult hippocampus remain undefined. We have previously demonstrated that preinjury treatment with anti-microRNA (miR)-181a preserved neurons and prevented astrocyte dysfunction in the hippocampal cornu ammonis-1 (CA1) following transient forebrain ischemia. In the present study, we assessed postinjury treatment with anti-miR-181a on recovery of CA1 neurons following transient forebrain ischemia in rats. Stereotactic CA1 injection of miR-181a antagomir at either 2 h or 7 d postinjury resulted in improved restoration of CA1 measured at 28 d postinjury. Treatment with antagomir was associated with overexpression of the mir-181a target cell adhesion-associated, oncogene-related protein and enhanced expression of the neuroprogenitor cell marker doublecortin (DCX) in the CA1. Assessment of GFAP+ cell fate by Cre/Lox-mediated deletion demonstrated that some GFAP+ cells in CA1 exhibited de novo DCX expression in response to injury. In vitro experiments using primary neuronal stem cells confirmed that miR-181a inhibition augmented the expression of DCX and directed cellular differentiation toward a neuronal fate. These results suggest that miR-181a inhibition plays a central role in the restoration of CA1 neurons via augmentation of early latent neurogenic gene activation in neural progenitor cells, including some reactive astrocytes. Therapeutic interventions targeting this restorative process may represent a novel postinjury approach to improve clinical outcomes in survivors of forebrain ischemia.

Keywords: astrocytes; forebrain ischemia; hippocampus; microRNA; neurogenesis.

Publication types

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

MeSH terms

  • Animals
  • Antagomirs / administration & dosage*
  • Astrocytes / drug effects
  • Astrocytes / metabolism
  • Brain Ischemia / metabolism*
  • CA1 Region, Hippocampal / drug effects
  • CA1 Region, Hippocampal / metabolism*
  • Doublecortin Protein
  • Male
  • MicroRNAs / antagonists & inhibitors*
  • Neural Stem Cells / drug effects
  • Neural Stem Cells / metabolism
  • Neurogenesis / drug effects
  • Neurons / drug effects
  • Neurons / metabolism*
  • Prosencephalon / drug effects
  • Prosencephalon / physiopathology
  • Rats, Sprague-Dawley

Substances

  • Antagomirs
  • Dcx protein, rat
  • Doublecortin Protein
  • MIRN181 microRNA, rat
  • MicroRNAs