Physical exercise-induced circAnks1b upregulation promotes protective endoplasmic reticulum stress and suppresses apoptosis via miR-130b-5p/Pak2 signaling in an ischemic stroke model

CNS Neurosci Ther. 2024 Sep;30(9):e70055. doi: 10.1111/cns.70055.

Abstract

Aims: Physical exercise (PE) can accelerate post-stroke recovery. This study investigated contributions of circRNAs to PE-induced improvements in post-stroke neurological function.

Methods: Rats subjected to transient middle cerebral artery occlusion were left sedentary or provided running-wheel access for 4 weeks during recovery. CircRNAs from peri-infarct cortex were identified by high-throughput sequencing, and interactions with miRNAs by immunoprecipitation, fluorescence in suit hybridization, and dual-luciferase reporter assays. In vivo circRNA knockdown was achieved using shRNA-AAVs and in vitro overexpression by plasmid transfection. Transmission electron microscopy, western blotting, and TUNEL assays were conducted to explore circRNA contributions to endoplasmic reticulum (ER) stress and neuronal apoptosis. CircRNA levels were measured in plasma from stroke patients by qRT-PCR and associations with neurological scores assessed by Pearson's correlation analysis.

Results: PE upregulated circAnks1b, reduced infarct volume, and mitigated neurological dysfunction, while circAnks1b knockdown exacerbated neurological dysfunction and increased infarct size despite PE. CircAnks1b sponged miR-130b-5p, thereby disinhibiting Pak2 expression. Conversely, Pak2 downregulation disrupted PE-mediated protective ER stress, leading to reduced IRE1/XBP1 and heightened apoptosis. Plasma circAnks1b was higher in stroke patients receiving PE than sedentary patients and correlated negatively with neurological scores.

Conclusions: CircAnks1b upregulation may be an effective therapeutic strategy for post-stroke recovery.

Keywords: ER stress; circAnks1b; ischemic stroke; physical exercise.

MeSH terms

  • Animals
  • Apoptosis
  • Disease Models, Animal
  • Endoplasmic Reticulum Stress* / genetics
  • Endoplasmic Reticulum Stress* / physiology
  • Humans
  • Infarction, Middle Cerebral Artery / genetics
  • Infarction, Middle Cerebral Artery / metabolism
  • Ischemic Stroke* / genetics
  • Ischemic Stroke* / metabolism
  • Ischemic Stroke* / pathology
  • Male
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Middle Aged
  • Physical Conditioning, Animal* / methods
  • Physical Conditioning, Animal* / physiology
  • RNA, Circular* / genetics
  • RNA, Circular* / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction* / physiology
  • Up-Regulation / physiology
  • p21-Activated Kinases / genetics
  • p21-Activated Kinases / metabolism

Substances

  • MicroRNAs
  • MIRN130 microRNA, human
  • MIRN130 microRNA, rat
  • p21-Activated Kinases
  • RNA, Circular