The involvement of SigmaR1K142 degradation mediated by ERAD in neural senescence linked with CdCl2 exposure

J Hazard Mater. 2024 Jul 5:472:134466. doi: 10.1016/j.jhazmat.2024.134466. Epub 2024 Apr 28.

Abstract

Alzheimer's disease (AD) is the most common cause of dementia worldwide. Due to its uncertain pathogenesis, there is currently no treatment available for AD. Increasing evidences have linked cellular senescence to AD, although the mechanism triggering cellular senescence in AD requires further exploration. To investigate the involvement of cellular senescence in AD, we explored the effects of cadmium chloride (CdCl2) exposure, one of the potential environmental risk factors for AD, on neuron senescence in vivo and in vitro. β-amyloid (Aβ) and tubulin-associated protein (tau) pathologies were found to be enhanced by CdCl2 exposure in the in vitro models, while p53/p21/Rb cascade-related neuronal senescence pathways were activated. Conversely, the use of melatonin, a cellular senescence inhibitor, or a cadmium ion chelator suppressed CdCl2-induced neuron senescence, along with the Aβ and tau pathologies. Mechanistically, CdCl2 exposure activated the suppressor enhancer Lin-12/Notch 1-like (SEL1L)/HMG-CoA reductase degradation 1 (HRD1)-regulated endoplasmic reticulum-associated degradation (ERAD), which enhanced the ubiquitin degradation of sigma-1 receptor (SigmaR1) by specifically recognizing its K142 site, resulting in the activation of the p53/p21/Rb pathway via the induction of Ca2+ dyshomeostasis and mitochondrial dysfunction. In the in vivo models, the administration of the SigmaR1 agonist ANAVEX2-73 rescues neurobehavioral inhibition and alleviates cellular senescence and AD-like pathology in the brain tissue of CdCl2-exposed mice. Consequently, the present study revealed a novel senescence-associated regulatory route for the SEL1L/HRD1/SigmaR1 axis that affects the pathological progression of CdCl2 exposure-associated AD. CdCl2 exposure activated SEL1L/HRD1-mediated ERAD and promoted the ubiquitinated degradation of SigmaR1, activating p53/p21/Rb pathway-regulated neuronal senescence. The results of the present study suggest that SigmaR1 may function as a neuroprotective biomarker of neuronal senescence, and pharmacological activation of SigmaR1 could be a promising intervention strategy for AD therapy.

Keywords: Alzheimer’s disease; Endoplasmic reticulum-associated degradation (ERAD); Environment CdCl(2) exposure; Neuronal senescence; Sigma-1 receptor (SigmaR1).

MeSH terms

  • Alzheimer Disease / metabolism
  • Amyloid beta-Peptides / metabolism
  • Animals
  • Cadmium Chloride* / toxicity
  • Cellular Senescence* / drug effects
  • Endoplasmic Reticulum-Associated Degradation* / drug effects
  • Humans
  • Male
  • Melatonin / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Neurons* / drug effects
  • Neurons* / metabolism
  • Receptors, sigma* / metabolism
  • tau Proteins / metabolism

Substances

  • Cadmium Chloride
  • Receptors, sigma
  • Amyloid beta-Peptides
  • tau Proteins
  • Melatonin