Loss of the zinc receptor ZnR/GPR39 in mice enhances anxiety-related behavior and motor deficits, and modulates KCC2 expression in the amygdala

Behav Brain Funct. 2024 Nov 24;20(1):31. doi: 10.1186/s12993-024-00254-x.

Abstract

Background: Mood disorders, particularly depression and anxiety, are associated with zinc dyshomeostasis and aberrant GABAergic signaling. Activation of ZnR/GPR39 by synaptic zinc in the hippocampus triggers phosphorylation of extracellular regulated kinase (ERK1/2), which regulates the K+/Cl- cotransporter (KCC2) and thereby GABAergic inhibitory neurotransmission and seizure activity. Therefore, we studied whether impaired ZnR/GPR39 signaling is linked to anxiety-related behavior in male or female mice.

Results: Using the acoustic startle response, elevated plus maze, and open field test, we found increased anxiety-related behavior in ZnR/GPR39 knockout (KO) mice. Despite a well-established sex difference, where females are typically more prone to anxiety, both male and female ZnR/GPR39 KO mice exhibited increased anxiety-related behavior compared to wildtype (WT) mice. Additionally, ZnR/GPR39 KO mice displayed impaired motor coordination in the pole and rotarod tests but did not show reduced muscle strength, as indicated by a grip test. Finally, we found intrinsic alterations in the expression level of KCC2, a major Cl- transporter regulating GABAergic signaling, in the amygdala of naïve ZnR/GPR39 KO mice compared to controls.

Conclusions: Our findings indicate that loss of ZnR/GPR39 enhances anxiety-related behavior in both male and female mice. Moreover, ZnR/GPR39 KO mice exhibit impaired motor coordination, which may be associated with increased anxiety. Finally, we demonstrate that loss of ZnR/GPR39 modulates the expression of KCC2 in the amygdala. Thus, we propose that ZnR/GPR39 can serve as a target for regulating GABAergic signaling in anxiety treatment.

Keywords: Anxiety-related; KCC2; Motor coordination; Zinc; Zinc signaling; ZnR/GPR39.

MeSH terms

  • Amygdala* / metabolism
  • Animals
  • Anxiety* / genetics
  • Anxiety* / metabolism
  • Anxiety* / psychology
  • Behavior, Animal / physiology
  • Female
  • K Cl- Cotransporters*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Motor Activity / physiology
  • Receptors, G-Protein-Coupled* / genetics
  • Receptors, G-Protein-Coupled* / metabolism
  • Symporters* / genetics
  • Symporters* / metabolism

Substances

  • Symporters
  • K Cl- Cotransporters
  • Receptors, G-Protein-Coupled
  • GPR39 protein, mouse