Targeting the Dvl-1/β-arrestin2/JNK3 interaction disrupts Wnt5a-JNK3 signaling and protects hippocampal CA1 neurons during cerebral ischemia reperfusion

Neuropharmacology. 2018 Jun:135:11-21. doi: 10.1016/j.neuropharm.2018.03.006. Epub 2018 Mar 3.

Abstract

It is well known that Wnt5a activation plays a pivotal role in brain injury and β-arrestin2 induces c-Jun N-terminal kinase (JNK3) activation is involved in neuronal cell death. Nonetheless, the relationship between Wnt5a and JNK3 remains unexplored during cerebral ischemia/reperfusion (I/R). In the present study, we tested the hypothesis that Wnt5a-mediated JNK3 activation via the Wnt5a-Dvl-1-β-arrestin2-JNK3 signaling pathway was correlated with I/R brain injury. We found that cerebral I/R could enhance the assembly of the Dvl-1-β-arrestin2-JNK3 signaling module, Dvl-1 phosphorylation and JNK3 activation. Activated JNK3 could phosphorylate the transcription factor c-Jun, prompt caspase-3 activation and ultimately lead to neuronal cell death. To further explore specifically Wnt5a mediated JNK3 pathway activation in neuronal injury, we used Foxy-5 (a peptide that mimics the effects of Wnt5a) and Box5 (a Wnt5a antagonist) both in vitro and in vivo. AS-β-arrestin2 (an antisense oligonucleotide against β-arrestin2) and RRSLHL (a small peptide that competes with β-arrestin2 for binding to JNK3) were applied to confirm the positive signal transduction effect of the Dvl-1-β-arrestin2-JNK3 signaling module during cerebral I/R. Furthermore, Box5 and the RRSLHL peptide were found to play protective roles in neuronal death both in vivo global and focal cerebral I/R rat models and in vitro oxygen glucose deprivation (OGD) neural cells. In summary, our results indicate that Wnt5a-mediated JNK3 activation participates in I/R brain injury by targeting the Dvl-1-β-arrestin2/JNK3 interaction. Our results also point to the possibility that disrupting Wnt5a-JNK3 signaling pathway may provide a new approach for stroke therapy.

Keywords: Dvl-1; Ischemia-reperfusion (I/R); JNK3; Wnt5a; c-Jun; β-arrestin2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CA1 Region, Hippocampal / cytology
  • CA1 Region, Hippocampal / metabolism*
  • Cell Death / drug effects
  • Dishevelled Proteins / metabolism*
  • Male
  • Mitogen-Activated Protein Kinase 10 / metabolism*
  • Neuroprotection* / drug effects
  • Oligopeptides / pharmacology
  • Oligoribonucleotides, Antisense / pharmacology
  • Peptides / pharmacology
  • Phosphorylation
  • Rats
  • Reperfusion Injury / metabolism*
  • Reperfusion Injury / pathology
  • Signal Transduction / drug effects*
  • Wnt-5a Protein / agonists
  • Wnt-5a Protein / metabolism*
  • beta-Arrestin 2 / antagonists & inhibitors
  • beta-Arrestin 2 / metabolism*

Substances

  • Dishevelled Proteins
  • Dvl1 protein, rat
  • Foxy-5 peptide
  • N-butyloxycarbonyl-methionyl-aspartyl-glycyl-cysteinyl-glutamyl-leucine
  • Oligopeptides
  • Oligoribonucleotides, Antisense
  • Peptides
  • RRSLHL peptide
  • Wnt-5a Protein
  • Wnt5a protein, rat
  • beta-Arrestin 2
  • Mitogen-Activated Protein Kinase 10