Gene delivery of SUMO1-derived peptide rescues neuronal degeneration and motor deficits in a mouse model of Parkinson's disease

Mol Ther. 2025 Jul 2;33(7):3056-3072. doi: 10.1016/j.ymthe.2025.04.005. Epub 2025 Apr 5.

Abstract

Developing α-synuclein aggregation inhibitors is challenging because its aggregation process involves several microscopic steps and heterogeneous intermediates. Previously, we identified a SUMO1-derived peptide, SUMO1(15-55), that exhibits tight binding to monomeric α-synuclein via SUMO-SUMO-interacting motif (SIM) interactions, and effectively blocks the initiation of aggregation and formation of toxic aggregates in vitro. In cellular and Drosophila models, SUMO1(15-55) was efficacious in protecting neuronal cells from α-synuclein-induced neurotoxicity and neuronal degeneration. Given the demonstrated ability of SUMO1(15-55) to sequester α-synuclein monomers thereby blocking oligomer formation, we sought to evaluate whether it could be equally effective against the aggregation-prone familial mutant α-synuclein-A53T. Herein, we show that SUMO1(15-55) selectively binds to monomeric α-synuclein-A53T, inhibits primary nucleation, and prevents the formation of structured protofibrils in vitro, thereby protecting neuronal cells from protofibril-induced cell death. We further demonstrate that larval feeding of a designed His10-SUMO1(15-55) that exhibits enhanced sub-stoichiometric suppression of α-synuclein-A53T aggregation in vitro can ameliorate Parkinson's disease (PD)-related symptoms in α-synuclein-A53T transgenic Drosophila models, while its rAAV-mediated gene delivery can relieve the PD-related histological and behavioral deficiencies in an rAAV-α-synuclein-A53T mouse PD model. Our findings suggest that gene delivery of His10-SUMO1(15-55) may serve as a clinical therapy for a spectrum of α-synuclein-aggregation associated synucleinopathies.

Keywords: gene therapy; mouse behavioral tests; recombinant adeno-associated virus; small ubiquitin-like modifier; α-synuclein-Α53Τ aggregation.

MeSH terms

  • Animals
  • Disease Models, Animal
  • Gene Transfer Techniques
  • Genetic Therapy
  • Humans
  • Mice
  • Nerve Degeneration* / genetics
  • Nerve Degeneration* / therapy
  • Neurons / metabolism
  • Neurons / pathology
  • Parkinson Disease* / genetics
  • Parkinson Disease* / metabolism
  • Parkinson Disease* / pathology
  • Parkinson Disease* / physiopathology
  • Parkinson Disease* / therapy
  • Peptides* / genetics
  • SUMO-1 Protein* / chemistry
  • SUMO-1 Protein* / genetics
  • SUMO-1 Protein* / metabolism
  • alpha-Synuclein / chemistry
  • alpha-Synuclein / genetics
  • alpha-Synuclein / metabolism

Substances

  • alpha-Synuclein
  • SUMO-1 Protein
  • Peptides