Distinct cortical and striatal actions of a β-arrestin-biased dopamine D2 receptor ligand reveal unique antipsychotic-like properties

Proc Natl Acad Sci U S A. 2016 Dec 13;113(50):E8178-E8186. doi: 10.1073/pnas.1614347113. Epub 2016 Dec 1.

Abstract

The current dopamine (DA) hypothesis of schizophrenia postulates striatal hyperdopaminergia and cortical hypodopaminergia. Although partial agonists at DA D2 receptors (D2Rs), like aripiprazole, were developed to simultaneously target both phenomena, they do not effectively improve cortical dysfunction. In this study, we investigate the potential for newly developed β-arrestin2 (βarr2)-biased D2R partial agonists to simultaneously target hyper- and hypodopaminergia. Using neuron-specific βarr2-KO mice, we show that the antipsychotic-like effects of a βarr2-biased D2R ligand are driven through both striatal antagonism and cortical agonism of D2R-βarr2 signaling. Furthermore, βarr2-biased D2R agonism enhances firing of cortical fast-spiking interneurons. This enhanced cortical agonism of the biased ligand can be attributed to a lack of G-protein signaling and elevated expression of βarr2 and G protein-coupled receptor (GPCR) kinase 2 in the cortex versus the striatum. Therefore, we propose that βarr2-biased D2R ligands that exert region-selective actions could provide a path to develop more effective antipsychotic therapies.

Keywords: antipsychotics; arrestin; biased signaling; dopamine D2R; fast-spiking interneurons.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antipsychotic Agents / pharmacology*
  • Behavior, Animal / drug effects
  • Behavior, Animal / physiology
  • Cerebral Cortex / drug effects*
  • Cerebral Cortex / metabolism*
  • Corpus Striatum / drug effects*
  • Corpus Striatum / metabolism*
  • Dopamine D2 Receptor Antagonists / pharmacology
  • Female
  • G-Protein-Coupled Receptor Kinase 2 / metabolism
  • GTP-Binding Proteins / metabolism
  • HEK293 Cells
  • Humans
  • Interneurons / metabolism
  • Ligands
  • Male
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phencyclidine / toxicity
  • Receptors, Dopamine D2 / agonists*
  • Receptors, Dopamine D2 / metabolism*
  • Signal Transduction / drug effects
  • beta-Arrestin 2 / metabolism*

Substances

  • Antipsychotic Agents
  • DRD2 protein, mouse
  • Dopamine D2 Receptor Antagonists
  • Ligands
  • Receptors, Dopamine D2
  • beta-Arrestin 2
  • GRK2 protein, human
  • GRK2 protein, mouse
  • G-Protein-Coupled Receptor Kinase 2
  • GTP-Binding Proteins
  • Phencyclidine