Spliceosomal GTPase Eftud2 deficiency-triggered ferroptosis leads to Purkinje cell degeneration

Neuron. 2024 Oct 23;112(20):3452-3469.e9. doi: 10.1016/j.neuron.2024.07.020. Epub 2024 Aug 16.

Abstract

Spliceosomal GTPase elongation factor Tu GTP binding domain containing 2 (EFTUD2) is a causative gene for mandibulofacial dysostosis with microcephaly (MFDM) syndrome comprising cerebellar hypoplasia and motor dysfunction. How EFTUD2 deficiency contributes to these symptoms remains elusive. Here, we demonstrate that specific ablation of Eftud2 in cerebellar Purkinje cells (PCs) in mice results in severe ferroptosis, PC degeneration, dyskinesia, and cerebellar atrophy, which recapitulates phenotypes observed in patients with MFDM. Mechanistically, Eftud2 promotes Scd1 and Gch1 expression, upregulates monounsaturated fatty acid phospholipids, and enhances antioxidant activity, thereby suppressing PC ferroptosis. Importantly, we identified transcription factor Atf4 as a downstream target to regulate anti-ferroptosis effects in PCs in a p53-independent manner. Inhibiting ferroptosis efficiently rescued cerebellar deficits in Eftud2 cKO mice. Our data reveal an important role of Eftud2 in maintaining PC survival, showing that pharmacologically or genetically inhibiting ferroptosis may be a promising therapeutic strategy for EFTUD2 deficiency-induced disorders.

Keywords: EFTUD2; MFDM; Purkinje cells; alternative splicing; ferroptosis; mandibulofacial dysostosis with microcephaly.

MeSH terms

  • Activating Transcription Factor 4 / genetics
  • Activating Transcription Factor 4 / metabolism
  • Animals
  • Ferroptosis* / physiology
  • Mice
  • Mice, Knockout
  • Nerve Degeneration / genetics
  • Nerve Degeneration / metabolism
  • Nerve Degeneration / pathology
  • Peptide Elongation Factors* / genetics
  • Peptide Elongation Factors* / metabolism
  • Purkinje Cells* / metabolism
  • Purkinje Cells* / pathology
  • Ribonucleoprotein, U5 Small Nuclear* / genetics
  • Ribonucleoprotein, U5 Small Nuclear* / metabolism

Substances

  • Activating Transcription Factor 4
  • Atf4 protein, mouse
  • Peptide Elongation Factors
  • Ribonucleoprotein, U5 Small Nuclear