AAV9-Mediated Cdk5 Inhibitory Peptide Reduces Hyperphosphorylated Tau and Inflammation and Ameliorates Behavioral Changes Caused by Overexpression of p25 in the Brain

J Alzheimers Dis. 2019;70(2):573-585. doi: 10.3233/JAD-190099.

Abstract

Background: Under stress stimulation, p25 is generated by cleavage of p35 and acts as an activator of cyclin-dependent kinase 5 (Cdk5) like p35. Unlike Cdk5/p35, which is important for brain development, aberrant activity of Cdk5/p25 plays a pathological role in neurodegenerative diseases, such as Alzheimer's disease, by inducing hyperphosphorylation of downstream substrates related to pathological progression. A truncated fragment of the c-terminus of p35, the Cdk5 inhibitory peptide (CIP), selectively inhibits Cdk5/ p25 activity in cultured neurons and in CIP/p25 tetra-transgenic mice.

Objective: First, we aimed to establish a p25 overexpression adult mouse model, then to evaluate whether CIP delivered by adeno-associated virus serotype 9 (AAV9) can ameliorate neuronal toxicity induced by p25.

Methods: The p25 overexpression mouse model was established by intracerebroventricular (i.c.v.) injection of AAV8-GFP-p25 in 8-week-old mice. One month later, these mice were i.c.v. injected with AAV9-CIP-T2A-mCherry or AAV9 vector as control. Pathological and behavioral changes were assessed 3-months post-injection in all mice.

Results: The p25 overexpression mice displayed hyperphosphorylation of tau at multiple sites, activation of astrocytes, and elevated inflammatory factors, including IL-1 and TNF-α, which were significantly decreased by the administration of CIP. However, Aβ deposition and microgliosis were not obvious in p25 overexpression mice. In addition, a significant learning decline and anxiety-like behavior were induced by p25 toxicity, and CIP treatment improved learning ability in p25 mice.

Conclusion: AAV-mediated p25 overexpression mouse model is easy to construct to study p25-induced neuronal toxicity. Application of CIP after p25 insult reverses the pathological changes and behavioral abnormalities.

Keywords: Adeno-associated virus; Cdk5 inhibitory peptide; hyperphosphorylation of tau; neurodegeneration; p25.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / metabolism*
  • Brain / pathology
  • Dependovirus* / genetics
  • Gene Expression
  • HEK293 Cells
  • Humans
  • Inflammation / genetics
  • Inflammation / metabolism
  • Inflammation / pathology
  • Injections, Intraventricular
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nerve Tissue Proteins / metabolism*
  • Peptide Fragments / metabolism*
  • Phosphorylation / physiology
  • Phosphotransferases / biosynthesis*
  • Phosphotransferases / genetics
  • tau Proteins / antagonists & inhibitors
  • tau Proteins / metabolism*

Substances

  • Cdk5 inhibitory peptide, human
  • Cdk5r1 protein, mouse
  • Mapt protein, mouse
  • Nerve Tissue Proteins
  • Peptide Fragments
  • tau Proteins
  • Phosphotransferases