Enantiomers of 4-aminopentanoic acid act as false GABAergic neurotransmitters and impact mouse behavior

J Neurochem. 2021 Sep;158(5):1074-1082. doi: 10.1111/jnc.15474. Epub 2021 Aug 2.

Abstract

Imbalance in the metabolic pathway linking excitatory and inhibitory neurotransmission has been implicated in multiple psychiatric and neurologic disorders. Recently, we described enantiomer-specific effects of 2-methylglutamate, which is not decarboxylated to the corresponding methyl analogue of gamma-aminobutyric acid (GABA): 4-aminopentanoic acid (4APA). Here, we tested the hypothesis that 4APA also has enantiomer-specific actions in brain. Mouse cerebral synaptosome uptake (nmol/mg protein over 30 min) of (R)-4APA or (S)-4APA was time and temperature dependent; however, the R enantiomer had greater uptake, reduction of endogenous GABA concentration, and release following membrane depolarization than did the S enantiomer. (S)-4APA exhibited some weak agonist (GABAA α4β3δ, GABAA α5β2γ2, and GABAB B1/B2) and antagonist (GABAA α6β2γ2) activity while (R)-4APA showed weak agonist activity only with GABAA α5β2γ2. Both 4APA enantiomers (100 mg/kg IP) were detected in mouse brain 10 min after injection, and by 1 hr had reached concentrations that were stable over 6 hr; both enantiomers were cleared rapidly from mouse serum over 6 hr. Two-month-old mice had no mortality following 100-900 mg/kg IP of each 4APA enantiomer but did have similar dose-dependent reduction in distance moved in a novel cage. Neither enantiomer at 30 or 100 mg/kg impacted outcomes in 23 measures of well-being, activity chamber, or withdrawal from hot plate. Our results suggest that enantiomers of 4APA are active in mouse brain, and that (R)-4APA may act as a novel false neurotransmitter of GABA. Future work will focus on disease models and on possible applications as neuroimaging agents.

Keywords: GABA; Synaptic metabolism; mouse behavior.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / metabolism
  • Brain Chemistry
  • Dose-Response Relationship, Drug
  • Exploratory Behavior / drug effects
  • Exploratory Behavior / physiology*
  • Locomotion / drug effects
  • Locomotion / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neurotransmitter Agents / chemistry*
  • Neurotransmitter Agents / metabolism
  • Pentanoic Acids / chemistry*
  • Pentanoic Acids / metabolism
  • Pentanoic Acids / pharmacology
  • Receptors, GABA-A / chemistry
  • Receptors, GABA-A / metabolism
  • Stereoisomerism
  • Synaptosomes / metabolism
  • gamma-Aminobutyric Acid / chemistry*
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Neurotransmitter Agents
  • Pentanoic Acids
  • Receptors, GABA-A
  • gamma-Aminobutyric Acid

Grants and funding