miR-383-5p Regulated by the Transcription Factor CTCF Affects Neuronal Impairment in Cerebral Ischemia by Mediating Deacetylase HDAC9 Activity

Mol Neurobiol. 2022 Oct;59(10):6307-6320. doi: 10.1007/s12035-022-02840-4. Epub 2022 Aug 4.

Abstract

Stroke, the leading cause of long-term disability worldwide, is caused by the blockage or hemorage of cerebral arteries. The resultant cerebral ischemia causes local neuronal death and brain injury. Histone deacetylase 9 (HDAC9) has been reported to be elevated in ischemic brain injury, but its mechanism in stroke is still enigmatic. The present study aimed to unveil the manner of regulation of HDAC9 expression and the effect of HDAC9 activation on neuronal function in cerebral ischemia. MicroRNAs (miRNAs) targeting HDAC9 were predicted utilizing bioinformatics analysis. We then constructed the oxygen glucose deprivation (OGD) cell model and the middle cerebral artery occlusion (MCAO) rat model, and elucidated the expression of CCCTC binding factor (CTCF)/miR-383-5p/HDAC9. Targeting between miR-383-5p and HDAC9 was verified by dual-luciferase reporter assay and RNAi. After conducting an overexpression/knockdown assay, we assessed neuronal impairment and brain injury. We found that CTCF inhibited miR-383-5p expression via its enrichment in the promoter region of miR-383-5p, whereas the miR-383-5p targeted and inhibited HDAC9 expression. In the OGD model and the MCAO model, we confirmed that elevation of HDAC9 regulated by the CTCF/miR-383-5p/HDAC9 pathway mediated apoptosis induced by endoplasmic reticulum stress, while reduction of HDAC9 alleviated apoptosis and the symptoms of cerebral infarction in MCAO rats. Thus, the CTCF/miR-383-5p/HDAC9 pathway may present a target for drug development against ischemic brain injury.

Keywords: Apoptosis; CTCF; Cerebral ischemia; Endoplasmic reticulum stress; HDAC9; Neuronal impairment; miR-383-5p.

MeSH terms

  • Animals
  • Apoptosis
  • Brain Injuries*
  • Brain Ischemia* / genetics
  • Brain Ischemia* / metabolism
  • CCCTC-Binding Factor
  • Glucose / metabolism
  • Histone Deacetylases
  • Infarction, Middle Cerebral Artery / complications
  • Infarction, Middle Cerebral Artery / metabolism
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Oxygen
  • Rats
  • Reperfusion Injury* / metabolism
  • Stroke* / metabolism
  • Transcription Factors

Substances

  • CCCTC-Binding Factor
  • Ctcf protein, rat
  • MIRN383 microRNA, rat
  • MicroRNAs
  • Transcription Factors
  • HDAC9 protein, rat
  • Histone Deacetylases
  • Glucose
  • Oxygen