A familial Alzheimer's disease associated mutation in presenilin-1 mediates amyloid-beta independent cell specific neurodegeneration

PLoS One. 2024 Sep 6;19(9):e0289435. doi: 10.1371/journal.pone.0289435. eCollection 2024.

Abstract

Mutations in the presenilin (PS) genes are a predominant cause of familial Alzheimer's disease (fAD). An ortholog of PS in the genetic model organism Caenorhabditis elegans (C. elegans) is sel-12. Mutations in the presenilin genes are commonly thought to lead to fAD by upregulating the expression of amyloid beta (Aβ), however this hypothesis has been challenged by recent evidence. As C. elegans lack amyloid beta (Aβ), the goal of this work was to examine Aβ-independent effects of mutations in sel-12 and PS1/PS2 on behaviour and sensory neuron morphology across the lifespan in a C. elegans model. Olfactory chemotaxis experiments were conducted on sel-12(ok2078) loss-of-function mutant worms. Adult sel-12 mutant worms showed significantly lower levels of chemotaxis to odorants compared to wild-type worms throughout their lifespan, and this deficit increased with age. The chemotaxis phenotype in sel-12 mutant worms is rescued by transgenic over-expression of human wild-type PS1, but not the classic fAD-associated variant PS1C410Y, when expression was driven by either the endogenous sel-12 promoter (Psel-12), a pan-neuronal promoter (Primb-1), or by a promoter whose primary expression was in the sensory neurons responsible for the chemotaxis behavior (Psra-6, Podr-10). The behavioural phenotype was also rescued by over-expressing an atypical fAD-linked mutation in PS1 (PS1ΔS169) that has been reported to leave the Notch pathway intact. An examination of the morphology of polymodal nociceptive (ASH) neurons responsible for the chemotaxis behavior also showed increased neurodegeneration over time in sel-12 mutant worms that could be rescued by the same transgenes that rescued the behaviour, demonstrating a parallel with the observed behavioral deficits. Thus, we report an Aβ-independent neurodegeneration in C. elegans that was rescued by cell specific over-expression of wild-type human presenilin.

MeSH terms

  • Alzheimer Disease* / genetics
  • Alzheimer Disease* / metabolism
  • Alzheimer Disease* / pathology
  • Amyloid beta-Peptides* / metabolism
  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Caenorhabditis elegans* / genetics
  • Caenorhabditis elegans* / metabolism
  • Chemotaxis / genetics
  • Disease Models, Animal
  • Humans
  • Mutation*
  • Presenilin-1* / genetics
  • Sensory Receptor Cells / metabolism
  • Sensory Receptor Cells / pathology

Substances

  • Amyloid beta-Peptides
  • Caenorhabditis elegans Proteins
  • Presenilin-1
  • SEL-12 protein, C elegans
  • PSEN1 protein, human

Grants and funding

This research was supported by a Canadian Institutes of Health Research Institute of Neurosciences, Mental Health and Addiction Grant #PJT 165947 to CHR, MP was supported by the Ecole Polytechnique Commemorative Award from the Canadian Federation of University Women (CFUW), JL was supported by an NSERC PGS-D. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.