IMPDH2 filaments protect from neurodegeneration in AMPD2 deficiency

EMBO Rep. 2024 Sep;25(9):3990-4012. doi: 10.1038/s44319-024-00218-2. Epub 2024 Jul 29.

Abstract

Metabolic dysregulation is one of the most common causes of pediatric neurodegenerative disorders. However, how the disruption of ubiquitous and essential metabolic pathways predominantly affect neural tissue remains unclear. Here we use mouse models of a childhood neurodegenerative disorder caused by AMPD2 deficiency to study cellular and molecular mechanisms that lead to selective neuronal vulnerability to purine metabolism imbalance. We show that mouse models of AMPD2 deficiency exhibit predominant degeneration of the hippocampal dentate gyrus, despite a general reduction of brain GTP levels. Neurodegeneration-resistant regions accumulate micron-sized filaments of IMPDH2, the rate limiting enzyme in GTP synthesis, while these filaments are barely detectable in the hippocampal dentate gyrus. Furthermore, we show that IMPDH2 filament disassembly reduces GTP levels and impairs growth of neural progenitor cells derived from individuals with human AMPD2 deficiency. Together, our findings suggest that IMPDH2 polymerization prevents detrimental GTP deprivation, opening the possibility of exploring the induction of IMPDH2 assembly as a therapy for neurodegeneration.

Keywords: Ampd2; Impdh2 Filaments; Metabolons; Pontocerebellar Hypoplasia; Purine Nucleotides.

MeSH terms

  • AMP Deaminase* / deficiency
  • AMP Deaminase* / metabolism
  • Animals
  • Disease Models, Animal
  • Guanosine Triphosphate / metabolism
  • Humans
  • IMP Dehydrogenase* / genetics
  • IMP Dehydrogenase* / metabolism
  • Mice
  • Mice, Knockout
  • Neural Stem Cells / metabolism
  • Neurodegenerative Diseases* / etiology
  • Neurodegenerative Diseases* / genetics
  • Neurodegenerative Diseases* / metabolism
  • Sphingomyelin Phosphodiesterase

Substances

  • Guanosine Triphosphate
  • IMP Dehydrogenase
  • Smpd3 protein, mouse
  • Sphingomyelin Phosphodiesterase
  • AMPD2 protein, human
  • AMP Deaminase