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Basic Science and Pathogenesis.

Alexandre Pelletier1, Lu Qian1, Tony Tuck1

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Summary
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The apolipoprotein E4 (APOE4) gene variant significantly disrupts mRNA splicing in excitatory neurons, impacting neuronal projection and contributing to early Alzheimer's disease neuropathology.

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Area of Science:

  • Neuroscience
  • Genetics
  • Molecular Biology

Background:

  • The apolipoprotein E4 (APOE4) allele is the primary genetic risk factor for late-onset Alzheimer's disease (AD).
  • APOE4 homozygotes (APOE4/4) have a high likelihood of developing AD pathology by age 65.
  • Understanding APOE4-driven neuropathology remains incomplete.

Purpose of the Study:

  • To investigate the molecular mechanisms underlying APOE4-mediated neuropathology.
  • To compare the effects of APOE4 versus neutral APOE3 alleles on cellular and molecular pathways.

Main Methods:

  • Proteomics and transcriptomics analysis of human induced pluripotent stem cell-derived cortical cultures (hiMCCs) from APOE4/4 and APOE3 carriers.
  • Validation using CRISPR/Cas9-edited isogenic hiMCCs and postmortem brain multi-omics data.
  • Single-cell RNA sequencing (scRNA-seq) to identify specific cell populations affected.

Main Results:

  • APOE4 impacts extracellular matrix and lipid transport pathways.
  • APOE4 significantly reduces mRNA spliceosome machinery at the protein level.
  • APOE4 induces intron retention in genes critical for neuronal projection, leading to protein reduction, particularly in a subpopulation of excitatory neurons.
  • These splicing defects are observed in early-stage APOE4 carrier brains and correlate with amyloid and tau pathology.

Conclusions:

  • Disruption of mRNA splicing in excitatory neurons is a key mechanism in APOE4-mediated neuropathology.
  • These splicing defects manifest early in Alzheimer's disease progression.
  • Targeting splicing defects may offer therapeutic strategies for APOE4-associated Alzheimer's disease.