PICALM rescues glutamatergic neurotransmission, behavioural function and survival in a Drosophila model of Aβ42 toxicity

Hum Mol Genet. 2020 Aug 11;29(14):2420-2434. doi: 10.1093/hmg/ddaa125.

Abstract

Alzheimer's disease (AD) is the most common form of dementia and the most prevalent neurodegenerative disease. Genome-wide association studies have linked PICALM to AD risk. PICALM has been implicated in Aβ42 production and turnover, but whether it plays a direct role in modulating Aβ42 toxicity remains unclear. We found that increased expression of the Drosophila PICALM orthologue lap could rescue Aβ42 toxicity in an adult-onset model of AD, without affecting Aβ42 level. Imbalances in the glutamatergic system, leading to excessive, toxic stimulation, have been associated with AD. We found that Aβ42 caused the accumulation of presynaptic vesicular glutamate transporter (VGlut) and increased spontaneous glutamate release. Increased lap expression reversed these phenotypes back to control levels, suggesting that lap may modulate glutamatergic transmission. We also found that lap modulated the localization of amphiphysin (Amph), the homologue of another AD risk factor BIN1, and that Amph itself modulated postsynaptic glutamate receptor (GluRII) localization. We propose a model where PICALM modulates glutamatergic transmission, together with BIN1, to ameliorate synaptic dysfunction and disease progression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / genetics*
  • Alzheimer Disease / pathology
  • Amyloid beta-Peptides / genetics
  • Animals
  • Behavior, Animal
  • CCAAT-Enhancer-Binding Protein-beta / genetics*
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster / genetics
  • Excitatory Amino Acid Agents
  • Humans
  • Monomeric Clathrin Assembly Proteins / genetics
  • Nerve Tissue Proteins / genetics
  • Peptide Fragments / genetics
  • Receptors, Ionotropic Glutamate / genetics*
  • Synaptic Transmission / genetics
  • Transcription Factors / genetics*
  • Vesicular Glutamate Transport Proteins / genetics*

Substances

  • Amyloid beta-Peptides
  • CCAAT-Enhancer-Binding Protein-beta
  • Drosophila Proteins
  • Excitatory Amino Acid Agents
  • Monomeric Clathrin Assembly Proteins
  • Nerve Tissue Proteins
  • PICALM protein, human
  • Peptide Fragments
  • Receptors, Ionotropic Glutamate
  • Transcription Factors
  • VGlut protein, Drosophila
  • Vesicular Glutamate Transport Proteins
  • amyloid beta-protein (1-42)
  • bicoid interacting protein 1, Drosophila
  • glutamate receptor IIA, Drosophila
  • amphiphysin