Purkinje cell-specific deficiency in SEL1L-hrd1 endoplasmic reticulum-associated degradation causes progressive cerebellar ataxia in mice

JCI Insight. 2024 Nov 8;9(21):e174725. doi: 10.1172/jci.insight.174725.

Abstract

Recent studies have identified multiple genetic variants of SEL1L-HRD1 endoplasmic reticulum-associated degradation (ERAD) in humans with neurodevelopmental disorders and locomotor dysfunctions, including ataxia. However, the relevance and importance of SEL1L-HRD1 ERAD in the pathogenesis of ataxia remain unexplored. Here, we showed that SEL1L deficiency in Purkinje cells leads to early-onset progressive cerebellar ataxia with progressive loss of Purkinje cells with age. Mice with Purkinje cell-specific deletion of SEL1L (Sel1LPcp2Cre) exhibited motor dysfunction beginning around 9 weeks of age. Transmission electron microscopy analysis revealed dilated ER and fragmented nuclei in Purkinje cells of adult Sel1LPcp2Cre mice, indicative of altered ER homeostasis and cell death. Finally, loss of Purkinje cells was associated with a secondary neurodegeneration of granular cells, as well as robust activation of astrocytes and proliferation of microglia, in the cerebellums of Sel1LPcp2Cre mice. These data demonstrate the pathophysiological importance of SEL1L-HRD1 ERAD in Purkinje cells in the pathogenesis of cerebellar ataxia.

Keywords: Neurodegeneration; Neuroscience.

MeSH terms

  • Animals
  • Cerebellar Ataxia* / genetics
  • Cerebellar Ataxia* / metabolism
  • Cerebellar Ataxia* / pathology
  • Cerebellum / metabolism
  • Cerebellum / pathology
  • Disease Models, Animal
  • Endoplasmic Reticulum / metabolism
  • Endoplasmic Reticulum-Associated Degradation*
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Male
  • Mice
  • Mice, Knockout
  • Proteins / genetics
  • Proteins / metabolism
  • Purkinje Cells* / metabolism
  • Purkinje Cells* / pathology
  • Ubiquitin-Protein Ligases* / deficiency
  • Ubiquitin-Protein Ligases* / genetics
  • Ubiquitin-Protein Ligases* / metabolism

Substances

  • Syvn1 protein, mouse
  • Ubiquitin-Protein Ligases
  • Sel1h protein, mouse
  • Proteins
  • Intracellular Signaling Peptides and Proteins

Grants and funding

University of Michigan Animal Phenotyping Core for some of the behavioral tests (supported by P30 grants DK020572, DK089503 and 1U2CDK135066). This work was supported by RF1NS122060 (Z.Z.), 24AARG-D-NTF-1187603 and 1R35GM130292 (L.Q.). L.L.L. was supported in part by National Ataxia Foundation (NAF 918037).