Role of Post-Transcriptional Control of Calpain by miR-124-3p in the Development of Alzheimer's Disease

J Alzheimers Dis. 2019;67(2):571-581. doi: 10.3233/JAD-181053.

Abstract

Alzheimer's disease (AD) is a neurodegenerative disease prevalent in aged people, clinically characterized by progressive memory loss, behavioral and learning dysfunction, and cognitive deficits. The pathogenesis of AD is hallmarked by formation of amyloid-β peptide aggregates (Aβ) and intraneuronal neurofibrillary tangles (NFTs), which are induced by hyperphosphorylation of amyloid-β protein precursor and tau protein, respectively. The hyperphosphorylation is controlled by cyclin-dependent kinase-5 (CDK5), the aberrant activation of which is mediated by calpain (CAPN)-induced cleavage of p35 into p25. However, the regulation of CAPN in AD remains largely unknown. Here, we studied the post-transcriptional control of CAPN1 by microRNAs (miRNAs) in the setting of AD. We found that miR-124-3p, previously reported as a miRNA that was downregulated in AD, was a CAPN1-targeting miRNA that functionally inhibited the protein translation of CAPN1 in a human neural cell line, HCN-2. In vitro, transfection with miR-124-3p reduced the levels of CAPN1 protein, the cleavage of p35 into p25, and cell apoptosis dose-dependently in HCN-2 cells. Moreover, a significant inverse correlation was detected between the levels of miR-124-3p and CAPN1 in AD specimens. Furthermore, intracranial injection of adeno-associated virus expressing miR-124-3p into APP/PS1-AD mice significantly reduced Aβ deposition and significantly improved the AD-mouse behavior in the social recognition test and plus-maze discriminative avoidance task. Together, our data suggest that post-transcriptional control of calpain by miR-124-3p plays an essential role in the development of AD.

Keywords: Alzheimer’s disease; CDK5; amyloid-β peptide aggregates; calpain 1; miR-124-3p.

MeSH terms

  • Alzheimer Disease / metabolism*
  • Alzheimer Disease / psychology
  • Animals
  • Avoidance Learning
  • Calpain / biosynthesis*
  • Calpain / genetics
  • Cell Line
  • Cyclin-Dependent Kinase 5 / biosynthesis
  • Cyclin-Dependent Kinase 5 / genetics
  • Down-Regulation
  • Humans
  • Mice
  • MicroRNAs / biosynthesis
  • MicroRNAs / genetics
  • MicroRNAs / pharmacology*
  • Protein Processing, Post-Translational / drug effects*
  • Recognition, Psychology
  • Social Behavior
  • Transfection

Substances

  • MIRN124 microRNA, human
  • MicroRNAs
  • Cyclin-Dependent Kinase 5
  • Cdk5 protein, mouse
  • Calpain
  • Capn1 protein, mouse