PUBLICATION

Chronic hyperammonemia causes a hypoglutamatergic and hyperGABAergic metabolic state associated with neurobehavioral abnormalities in zebrafish larvae

Authors
Probst, J., Kölker, S., Okun, J.G., Kumar, A., Gursky, E., Posset, R., Hoffmann, G.F., Peravali, R., Zielonka, M.
ID
ZDB-PUB-200428-5
Date
2020
Source
Experimental neurology   331: 113330 (Journal)
Registered Authors
Gursky, Eduard, Peravali, Ravindra
Keywords
Chronic hyperammonemia, GABAergic signaling, Glutamate metabolism, Neurobehavioral dysfunction, Urea cycle disorders, Zebrafish model
MeSH Terms
  • Animals
  • Behavior, Animal/physiology*
  • Disease Models, Animal
  • Glutamic Acid/metabolism*
  • Hyperammonemia/metabolism*
  • Larva
  • Zebrafish
  • gamma-Aminobutyric Acid/metabolism*
PubMed
32339612 Full text @ Exp. Neurol.
Abstract
Chronic hyperammonemia is a common condition affecting individuals with inherited urea cycle disorders resulting in progressive cognitive impairment and behavioral abnormalities. Altered neurotransmission has been proposed as major source of neuronal dysfunction during chronic hyperammonemia, but the molecular pathomechanism has remained incompletely understood. Here we show that chronic exposure to ammonium acetate induces locomotor dysfunction and abnormal feeding behavior in zebrafish larvae, indicative for an impairment of higher brain functions. Biochemically, chronically elevated ammonium concentrations cause enhanced activity of glutamate decarboxylase isoforms GAD1 and GAD2 with increased formation of GABA and concomitant depletion of glutamate, ultimately leading to a dysfunctional hypoglutamatergic and hyperGABAergic metabolic state. Moreover, elevated GABA concentrations are accompanied by increased expression of GABAA receptor subunits alpha-1, gamma-2 and delta, supporting the notion of an increased GABA tone in chronic hyperammonemia. Propionate oxidation as major anaplerotic reaction sufficiently compensates for the transamination-dependent withdrawal of 2-oxoglutarate, thereby preventing bioenergetic dysfunction under chronic hyperammonemic conditions. Thus, our study extends the hypothesis of alterations in the glutamatergic and GABAergic system being an important pathophysiological factor causing neurobehavioral impairment in chronic hyperammonemia. Given that zebrafish larvae have already been successfully used for high-throughput identification of novel compounds to treat inherited neurological disease, the reported zebrafish model should be considered an important tool for systematic drug screening targeting altered glutamatergic and GABAergic metabolism under chronic hyperammonemic conditions in the future.
Genes / Markers
Figures
Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping