A novel interaction between aging and ER overload in a protein conformational dementia

Genetics. 2013 Mar;193(3):865-76. doi: 10.1534/genetics.112.149088. Epub 2013 Jan 18.

Abstract

Intraneuronal deposition of aggregated proteins in tauopathies, Parkinson disease, or familial encephalopathy with neuroserpin inclusion bodies (FENIB) leads to impaired protein homeostasis (proteostasis). FENIB represents a conformational dementia, caused by intraneuronal polymerization of mutant variants of the serine protease inhibitor neuroserpin. In contrast to the aggregation process, the kinetic relationship between neuronal proteostasis and aggregation are poorly understood. To address aggregate formation dynamics, we studied FENIB in Caenorhabditis elegans and mice. Point mutations causing FENIB also result in aggregation of the neuroserpin homolog SRP-2 most likely within the ER lumen in worms, recapitulating morphological and biochemical features of the human disease. Intriguingly, we identified conserved protein quality control pathways to modulate protein aggregation both in worms and mice. Specifically, downregulation of the unfolded protein response (UPR) pathways in the worm favors mutant SRP-2 accumulation, while mice overexpressing a polymerizing mutant of neuroserpin undergo transient induction of the UPR in young but not in aged mice. Thus, we find that perturbations of proteostasis through impairment of the heat shock response or altered UPR signaling enhance neuroserpin accumulation in vivo. Moreover, accumulation of neuroserpin polymers in mice is associated with an age-related induction of the UPR suggesting a novel interaction between aging and ER overload. These data suggest that targets aimed at increasing UPR capacity in neurons are valuable tools for therapeutic intervention.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Age Factors
  • Amino Acid Sequence
  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / genetics*
  • Caenorhabditis elegans Proteins / metabolism
  • Endoplasmic Reticulum / metabolism*
  • Endoplasmic Reticulum Stress*
  • Heat-Shock Response
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Humans
  • Inclusion Bodies / metabolism*
  • Mice
  • Mice, Mutant Strains
  • Molecular Sequence Data
  • Neurons / metabolism
  • Neurons / pathology
  • Neuropeptides / chemistry
  • Neuropeptides / genetics
  • Neuropeptides / metabolism*
  • Neuroserpin
  • Point Mutation
  • Polymerization
  • Protein Conformation
  • Protein Folding
  • Serpins / chemistry
  • Serpins / genetics*
  • Serpins / metabolism*
  • Signal Transduction
  • Unfolded Protein Response

Substances

  • Caenorhabditis elegans Proteins
  • Neuropeptides
  • SRP-2 protein, C elegans
  • Serpins