Genetic suppression of transgenic APP rescues Hypersynchronous network activity in a mouse model of Alzeimer's disease

J Neurosci. 2014 Mar 12;34(11):3826-40. doi: 10.1523/JNEUROSCI.5171-13.2014.

Abstract

Alzheimer's disease (AD) is associated with an elevated risk for seizures that may be fundamentally connected to cognitive dysfunction. Supporting this link, many mouse models for AD exhibit abnormal electroencephalogram (EEG) activity in addition to the expected neuropathology and cognitive deficits. Here, we used a controllable transgenic system to investigate how network changes develop and are maintained in a model characterized by amyloid β (Aβ) overproduction and progressive amyloid pathology. EEG recordings in tet-off mice overexpressing amyloid precursor protein (APP) from birth display frequent sharp wave discharges (SWDs). Unexpectedly, we found that withholding APP overexpression until adulthood substantially delayed the appearance of epileptiform activity. Together, these findings suggest that juvenile APP overexpression altered cortical development to favor synchronized firing. Regardless of the age at which EEG abnormalities appeared, the phenotype was dependent on continued APP overexpression and abated over several weeks once transgene expression was suppressed. Abnormal EEG discharges were independent of plaque load and could be extinguished without altering deposited amyloid. Selective reduction of Aβ with a γ-secretase inhibitor has no effect on the frequency of SWDs, indicating that another APP fragment or the full-length protein was likely responsible for maintaining EEG abnormalities. Moreover, transgene suppression normalized the ratio of excitatory to inhibitory innervation in the cortex, whereas secretase inhibition did not. Our results suggest that APP overexpression, and not Aβ overproduction, is responsible for EEG abnormalities in our transgenic mice and can be rescued independently of pathology.

Keywords: EEG; amyloid precursor protein; epilepsy; seizure; sharp wave discharge; transgene suppression.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Alzheimer Disease / genetics*
  • Alzheimer Disease / physiopathology*
  • Amyloid Precursor Protein Secretases / antagonists & inhibitors
  • Amyloid beta-Protein Precursor / genetics*
  • Animals
  • Cerebral Cortex / physiopathology*
  • Disease Models, Animal
  • Electroencephalography*
  • Entropy
  • Female
  • Gene Knock-In Techniques
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Models, Neurological
  • Neural Inhibition / physiology
  • Presenilin-1 / genetics
  • Seizures / chemically induced
  • Seizures / physiopathology
  • Suppression, Genetic
  • Transgenes / physiology

Substances

  • APP protein, human
  • Amyloid beta-Protein Precursor
  • PSEN1 protein, human
  • Presenilin-1
  • Amyloid Precursor Protein Secretases