Carboxyl truncation of α-synuclein occurs early and is influenced by human APOE genotype in transgenic mouse models of α-synuclein pathogenesis

Acta Neuropathol Commun. 2023 Jul 23;11(1):119. doi: 10.1186/s40478-023-01623-9.

Abstract

Post-translational modifications to the carboxyl (C) terminus domain of α-synuclein can play an important role in promoting the pathologic aggregation of α-synuclein. Various cleavages that diminish this highly charged, proline-rich region can result in exposure of hydrophobic, aggregation-prone regions, thereby accelerating the aggregation kinetics of α-synuclein into misfolded, pathologic forms. C-terminally truncated forms of α-synuclein are abundant in human diseased brains compared to controls, suggesting a role in disease pathogenesis. Factors that alter the homeostatic proteolytic processing of α-synuclein may ultimately tip the balance towards a progressive disease state. Apolipoprotein E (APOE) has been implicated in the acceleration of cognitive impairment in patients with Lewy body diseases. The APOE4 isoform has been found to cause dysregulation in the endosomal-lysosomal pathway, which could result in altered α-synuclein degradation as a potential mechanism for promoting its pathologic misfolding. Herein, we investigate the spatiotemporal accumulation of C-terminally truncated α-synuclein in a seeded and progressive mouse model of synucleinopathy. Furthermore, we study how this process is influenced in the context of mice that are altered to express either the human APOE3 or APOE4 isoforms. We found that specific C-terminal truncation of α-synuclein occurs at early stages of pathogenesis. We also found that proteolytic processing of this domain differs across various brain regions and is influenced by the presence of different human APOE isoforms. Our data demonstrate an early pathogenic role for C-terminally truncated α-synuclein, and highlight the influence of APOE isoforms in modulating its impact.

Keywords: APOE; Alpha-synuclein; Alzheimer’s disease with amygdala predominant Lewy bodies; C-terminal truncation; Dementia with Lewy bodies; Multiple system atrophy; Parkinson’s disease; Post-translational modifications; Synucleinopathies.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Apolipoprotein E4* / genetics
  • Apolipoprotein E4* / metabolism
  • Apolipoproteins E / metabolism
  • Carrier Proteins
  • Humans
  • Mice
  • Mice, Transgenic
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • alpha-Synuclein* / genetics
  • alpha-Synuclein* / metabolism

Substances

  • alpha-Synuclein
  • Apolipoprotein E4
  • Apolipoproteins E
  • Carrier Proteins
  • Protein Isoforms
  • SNCA protein, human
  • ApoE protein, human