Presenilin Loss Impairs Synaptic Transmission and Causes Axonal Degeneration through Ryanodine Receptor Dysfunction, Independent of γ-Secretase Activity

J Neurosci. 2025 Oct 22;45(43):e1052252025. doi: 10.1523/JNEUROSCI.1052-25.2025.

Abstract

Presenilin mutations are the most common cause of familial Alzheimer's disease (FAD), but the mechanisms by which they disrupt neuronal function remain unresolved, particularly in relation to γ-secretase activity. Using Caenorhabditis elegans, we show that the presenilin ortholog SEL-12 supports synaptic transmission and axonal integrity through a pathway involving the ryanodine receptor RYR-1. Loss-of-function mutations in either sel-12 or ryr-1 reduce neurotransmitter release and cause neuronal structural defects, with no additional impairment in double mutants, suggesting a shared pathway. Transgenic expression of a γ-secretase-inactive SEL-12 variant or human presenilin 1 restores normal synaptic transmission in sel-12 mutants. Notably, sel-12 loss does not alter ryr-1 transcript or protein levels. These findings define a novel γ-secretase-independent role of presenilin in maintaining neuronal function via ryanodine receptor signaling, providing new mechanistic insight into presenilin-linked neurodegeneration and pointing to potential therapeutic strategies for FAD.

Keywords: neurodegeneration; neurotransmitter release; presenilin; ryanodine receptor; sel-12; γ-secretase.

MeSH terms

  • Amyloid Precursor Protein Secretases* / genetics
  • Amyloid Precursor Protein Secretases* / metabolism
  • Animals
  • Animals, Genetically Modified
  • Axons* / metabolism
  • Axons* / pathology
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Humans
  • Nerve Degeneration* / genetics
  • Nerve Degeneration* / metabolism
  • Nerve Degeneration* / pathology
  • Presenilin-1 / genetics
  • Presenilins* / genetics
  • Presenilins* / metabolism
  • Ryanodine Receptor Calcium Release Channel* / genetics
  • Ryanodine Receptor Calcium Release Channel* / metabolism
  • Ryanodine Receptor Calcium Release Channel* / physiology
  • Synaptic Transmission* / genetics
  • Synaptic Transmission* / physiology

Substances

  • Ryanodine Receptor Calcium Release Channel
  • Caenorhabditis elegans Proteins
  • Presenilins
  • Amyloid Precursor Protein Secretases
  • Presenilin-1