Functional selectivity of 6'-guanidinonaltrindole (6'-GNTI) at κ-opioid receptors in striatal neurons

J Biol Chem. 2013 Aug 2;288(31):22387-98. doi: 10.1074/jbc.M113.476234. Epub 2013 Jun 17.

Abstract

There is considerable evidence to suggest that drug actions at the κ-opioid receptor (KOR) may represent a means to control pain perception and modulate reward thresholds. As a G protein-coupled receptor (GPCR), the activation of KOR promotes Gαi/o protein coupling and the recruitment of β-arrestins. It has become increasingly evident that GPCRs can transduce signals that originate independently via G protein pathways and β-arrestin pathways; the ligand-dependent bifurcation of such signaling is referred to as "functional selectivity" or "signaling bias." Recently, a KOR agonist, 6'-guanidinonaltrindole (6'-GNTI), was shown to display bias toward the activation of G protein-mediated signaling over β-arrestin2 recruitment. Therefore, we investigated whether such ligand bias was preserved in striatal neurons. Although the reference KOR agonist U69,593 induces the phosphorylation of ERK1/2 and Akt, 6'-GNTI only activates the Akt pathway in striatal neurons. Using pharmacological tools and β-arrestin2 knock-out mice, we show that KOR-mediated ERK1/2 phosphorylation in striatal neurons requires β-arrestin2, whereas Akt activation depends upon G protein signaling. These findings reveal a point of KOR signal bifurcation that can be observed in an endogenous neuronal setting and may prove to be an important indicator when developing biased agonists at the KOR.

Keywords: Arrestin; Brain; Drug Screening; G Protein-coupled Receptors (GPCR); Gene Knockout; MAP Kinases (MAPKs); Neurons; Opiate Opioid; Receptor Endocytosis; κ-Opioid Receptor.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • CHO Cells
  • Corpus Striatum / cytology
  • Corpus Striatum / drug effects*
  • Corpus Striatum / metabolism
  • Cricetinae
  • Cricetulus
  • Guanidines / pharmacology*
  • MAP Kinase Signaling System
  • Male
  • Mice
  • Naltrexone / analogs & derivatives*
  • Naltrexone / pharmacology
  • Neurons / drug effects*
  • Neurons / metabolism
  • Phosphorylation
  • Receptors, Opioid, kappa / drug effects*

Substances

  • 6'-guanidinonaltrindole
  • Guanidines
  • Receptors, Opioid, kappa
  • Naltrexone