Transgenic autoinhibition of p21-activated kinase exacerbates synaptic impairments and fronto-dependent behavioral deficits in an animal model of Alzheimer's disease

Aging (Albany NY). 2017 May 16;9(5):1386-1403. doi: 10.18632/aging.101239.

Abstract

Defects in p21-activated kinase (PAK) lead to dendritic spine abnormalities and are sufficient to cause cognition impairment. The decrease in PAK in the brain of Alzheimer's disease (AD) patients is suspected to underlie synaptic and dendritic disturbances associated with its clinical expression, particularly with symptoms related to frontal cortex dysfunction. To investigate the role of PAK combined with Aβ and tau pathologies (3xTg-AD mice) in the frontal cortex, we generated a transgenic model of AD with a deficit in PAK activity (3xTg-AD-dnPAK mice). PAK inactivation had no effect on Aβ40 and Aβ42 levels, but increased the phosphorylation ratio of tau in detergent-insoluble protein fractions in the frontal cortex of 18-month-old heterozygous 3xTg-AD mice. Morphometric analyses of layer II/III pyramidal neurons in the frontal cortex showed that 3xTg-AD-dnPAK neurons exhibited significant dendritic attrition, lower spine density and longer spines compared to NonTg and 3xTg-AD mice. Finally, behavioral assessments revealed that 3xTg-AD-dnPAK mice exhibited pronounced anxious traits and disturbances in social behaviors, reminiscent of fronto-dependent symptoms observed in AD. Our results substantiate a critical role for PAK in the genesis of neuronal abnormalities in the frontal cortex underlying the emergence of psychiatric-like symptoms in AD.

Keywords: 3xTg-AD mice; Alzheimer; electrophysiology; frontal cortex; morphology; p21-activated kinase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / enzymology*
  • Alzheimer Disease / genetics
  • Alzheimer Disease / physiopathology
  • Alzheimer Disease / psychology
  • Amyloid beta-Peptides / metabolism
  • Amyloid beta-Protein Precursor / genetics
  • Amyloid beta-Protein Precursor / metabolism
  • Animals
  • Anxiety / enzymology
  • Anxiety / psychology
  • Behavior, Animal*
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / genetics
  • Disease Models, Animal
  • Exploratory Behavior
  • Frontal Lobe / enzymology*
  • Frontal Lobe / pathology
  • Frontal Lobe / physiopathology
  • Genetic Predisposition to Disease
  • Interpersonal Relations
  • Locomotion
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Peptide Fragments / metabolism
  • Phenotype
  • Phosphorylation
  • Presenilin-1 / genetics
  • Promoter Regions, Genetic
  • Pyramidal Cells / enzymology*
  • Pyramidal Cells / pathology
  • Synaptic Transmission
  • p21-Activated Kinases / genetics
  • p21-Activated Kinases / metabolism*
  • tau Proteins / genetics
  • tau Proteins / metabolism

Substances

  • Amyloid beta-Peptides
  • Amyloid beta-Protein Precursor
  • Peptide Fragments
  • Presenilin-1
  • amyloid beta-protein (1-40)
  • amyloid beta-protein (1-42)
  • tau Proteins
  • p21-Activated Kinases
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Camk2a protein, mouse

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