Modeling Glutaric Aciduria Type I in human neuroblastoma cells recapitulates neuronal damage that can be rescued by gene replacement

Gene Ther. 2024 Jan;31(1-2):12-18. doi: 10.1038/s41434-023-00428-8. Epub 2023 Nov 20.

Abstract

Glutaric Aciduria type I (GA1) is a rare neurometabolic disorder caused by mutations in the GDCH gene encoding for glutaryl-CoA dehydrogenase (GCDH) in the catabolic pathway of lysine, hydroxylysine and tryptophan. GCDH deficiency leads to increased concentrations of glutaric acid (GA) and 3-hydroxyglutaric acid (3-OHGA) in body fluids and tissues. These metabolites are the main triggers of brain damage. Mechanistic studies supporting neurotoxicity in mouse models have been conducted. However, the different vulnerability to some stressors between mouse and human brain cells reveals the need to have a reliable human neuronal model to study GA1 pathogenesis. In the present work we generated a GCDH knockout (KO) in the human neuroblastoma cell line SH-SY5Y by CRISPR/Cas9 technology. SH-SY5Y-GCDH KO cells accumulate GA, 3-OHGA, and glutarylcarnitine when exposed to lysine overload. GA or lysine treatment triggered neuronal damage in GCDH deficient cells. SH-SY5Y-GCDH KO cells also displayed features of GA1 pathogenesis such as increased oxidative stress vulnerability. Restoration of the GCDH activity by gene replacement rescued neuronal alterations. Thus, our findings provide a human neuronal cellular model of GA1 to study this disease and show the potential of gene therapy to rescue GCDH deficiency.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Metabolism, Inborn Errors*
  • Animals
  • Brain Diseases, Metabolic*
  • Genetic Therapy
  • Glutaryl-CoA Dehydrogenase / deficiency
  • Glutaryl-CoA Dehydrogenase / genetics
  • Glutaryl-CoA Dehydrogenase / metabolism
  • Humans
  • Lysine* / genetics
  • Mice
  • Mice, Knockout
  • Neuroblastoma*

Substances

  • Lysine
  • Glutaryl-CoA Dehydrogenase

Supplementary concepts

  • Glutaric Acidemia I