The parkin V380L variant is a genetic modifier of Machado-Joseph disease with impact on mitophagy

Acta Neuropathol. 2024 Aug 1;148(1):14. doi: 10.1007/s00401-024-02762-6.

Abstract

Machado-Joseph disease (MJD) is an autosomal dominant neurodegenerative spinocerebellar ataxia caused by a polyglutamine-coding CAG repeat expansion in the ATXN3 gene. While the CAG length correlates negatively with the age at onset, it accounts for approximately 50% of its variability only. Despite larger efforts in identifying contributing genetic factors, candidate genes with a robust and plausible impact on the molecular pathogenesis of MJD are scarce. Therefore, we analysed missense single nucleotide polymorphism variants in the PRKN gene encoding the Parkinson's disease-associated E3 ubiquitin ligase parkin, which is a well-described interaction partner of the MJD protein ataxin-3, a deubiquitinase. By performing a correlation analysis in the to-date largest MJD cohort of more than 900 individuals, we identified the V380L variant as a relevant factor, decreasing the age at onset by 3 years in homozygous carriers. Functional analysis in an MJD cell model demonstrated that parkin V380L did not modulate soluble or aggregate levels of ataxin-3 but reduced the interaction of the two proteins. Moreover, the presence of parkin V380L interfered with the execution of mitophagy-the autophagic removal of surplus or damaged mitochondria-thereby compromising cell viability. In summary, we identified the V380L variant in parkin as a genetic modifier of MJD, with negative repercussions on its molecular pathogenesis and disease age at onset.

Keywords: PRKN; Aggregation; Polyglutamine disease; SCA3; SNP; Spinocerebellar ataxia type 3.

MeSH terms

  • Adult
  • Age of Onset
  • Ataxin-3 / genetics
  • Female
  • Humans
  • Machado-Joseph Disease* / genetics
  • Machado-Joseph Disease* / pathology
  • Male
  • Middle Aged
  • Mitophagy* / genetics
  • Mitophagy* / physiology
  • Polymorphism, Single Nucleotide
  • Repressor Proteins
  • Ubiquitin-Protein Ligases* / genetics

Substances

  • Ubiquitin-Protein Ligases
  • parkin protein
  • Ataxin-3
  • ATXN3 protein, human
  • Repressor Proteins