A kinesin signaling complex mediates the ability of GSK-3beta to affect mood-associated behaviors

Proc Natl Acad Sci U S A. 2010 Jun 22;107(25):11573-8. doi: 10.1073/pnas.0913138107. Epub 2010 Jun 7.

Abstract

Lithium has been the gold standard in the treatment of bipolar disorder (BPD) for 60 y. Like lithium, glycogen synthase kinase 3 (GSK-3) inhibitors display both antimanic-like and antidepressant-like effects in some animal models. However, the molecular mechanisms of both lithium and GSK-3 inhibitors remain unclear. Here we show that the GSK-3 inhibitor AR-A014418 regulated alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate (AMPA)-induced GluR1 and GluR2 internalization via phosphorylation of kinesin light chain 2 (KLC2), the key molecule of the kinesin cargo delivery system. Specifically, AMPA stimulation triggered serine phosphorylation of KLC2 and, subsequently, the dissociation of the GluR1/KLC2 protein complex. This suggests that GSK-3 phosphorylation of KLC2 led to the dissociation of AMPA-containing vesicles from the kinesin cargo system. The peptide TAT-KLCpCDK, a specific inhibitor for KLC2 phosphorylation by GSK-3beta, reduced the formation of long-term depression. Furthermore, the TAT-KLCpCDK peptide showed antimanic-like effects similar to lithium's on amphetamine-induced hyperactivity, a frequently used animal model of mania. It also induced antidepressant-like effects in the tail suspension and forced swim tests, two commonly used animal models of depression. Taken together, the results demonstrated that KLC2 is a cellular target of GSK-3beta capable of regulating synaptic plasticity, particularly AMPA receptor trafficking, as well as mood-associated behaviors in animal models. The kinesin cargo system may provide valuable novel targets for the development of new therapeutics for mood disorders.

Publication types

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

MeSH terms

  • Affect*
  • Animals
  • Antidepressive Agents / pharmacology
  • Bipolar Disorder / drug therapy*
  • Glycogen Synthase Kinase 3 / metabolism*
  • Glycogen Synthase Kinase 3 beta
  • Hippocampus / metabolism
  • Kinesins / metabolism*
  • Lithium / pharmacology
  • Male
  • Mice
  • Microtubule-Associated Proteins / metabolism
  • Models, Biological
  • Neuronal Plasticity / drug effects
  • Receptors, AMPA / metabolism
  • Synapses / metabolism
  • Thiazoles / pharmacology
  • Urea / analogs & derivatives
  • Urea / pharmacology
  • alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid / metabolism

Substances

  • Antidepressive Agents
  • Klc2 protein, mouse
  • Microtubule-Associated Proteins
  • Receptors, AMPA
  • Thiazoles
  • alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid
  • N-(4-methoxybenzyl)-N'-(5-nitro-1,3-thiazol-2-yl)urea
  • Urea
  • Lithium
  • Glycogen Synthase Kinase 3 beta
  • Gsk3b protein, mouse
  • Glycogen Synthase Kinase 3
  • Kinesins