3-Ureidopropionate contributes to the neuropathology of 3-ureidopropionase deficiency and severe propionic aciduria: a hypothesis

J Neurosci Res. 2001 Nov 15;66(4):666-73. doi: 10.1002/jnr.10012.

Abstract

3-Ureidopropionate (3-UPA) is a physiologic metabolite in pyrimidine degradation. Pathological accumulation of 3-UPA in body fluids is found in 3-ureidopropionase deficiency and severe forms of propionic aciduria. Both diseases clinically present with a severe neuropathology involving gray and white matter as well as with a dystonic dyskinetic movement disorder. To date nothing is known about the toxic nature of this metabolite. The aim of the present study was to elucidate whether 3-UPA may act as endogenous neurotoxin. Exposure of cultured chick neurons to 3-UPA induced a concentration- and time-dependent neurodegeneration. Neuronal damage was reduced by the antioxidant alpha-tocopherol and the N-methyl-D-aspartate (NMDA) receptor antagonist MK-801. In contrast, the non-NMDA receptor antagonist CNQX, the metabotropic glutamate receptor antagonist L-AP3, and succinate showed no protective effect. Furthermore, 3-UPA elicited an increased production of reactive oxygen species followed by a delayed increase in intracellular calcium concentrations. Activity measurement of single respiratory chain complexes I-V revealed an inhibition of complex V activity, but not of the electron-transferring complexes I-IV by 3-UPA. In contrast, 3-UPA did not affect the mitochondrial beta-oxidation of fatty acids. In conclusion, our results provide strong evidence that 3-UPA acts as endogenous neurotoxin via inhibition of mitochondrial energy metabolism, resulting in the initiation of secondary, energy-dependent excitotoxic mechanisms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Diseases, Metabolic / metabolism*
  • Brain Diseases, Metabolic / physiopathology
  • Calcium / metabolism
  • Cell Death / drug effects
  • Cell Death / physiology
  • Cells, Cultured / drug effects
  • Cells, Cultured / metabolism
  • Central Nervous System / metabolism*
  • Central Nervous System / physiopathology
  • Chick Embryo
  • Citrulline / pharmacology
  • Electron Transport / drug effects
  • Electron Transport / physiology
  • Energy Metabolism / drug effects
  • Energy Metabolism / physiology*
  • Enzyme Inhibitors / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Formamides / pharmacology
  • Glutamic Acid / pharmacology
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Neurons / drug effects
  • Neurons / metabolism
  • Neurotoxins / metabolism*
  • Neurotoxins / pharmacology
  • Oxidative Stress / physiology*
  • Propionates / toxicity
  • Propionates / urine*
  • Reactive Oxygen Species / metabolism
  • Receptors, N-Methyl-D-Aspartate / agonists
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Urea / pharmacology
  • beta-Alanine / analogs & derivatives*
  • beta-Alanine / deficiency*
  • beta-Alanine / toxicity

Substances

  • Enzyme Inhibitors
  • Excitatory Amino Acid Antagonists
  • Formamides
  • Neurotoxins
  • Propionates
  • Reactive Oxygen Species
  • Receptors, N-Methyl-D-Aspartate
  • beta-Alanine
  • Citrulline
  • Glutamic Acid
  • N-carbamoyl-beta-alanine
  • Urea
  • Calcium