Antidepressants Accumulate in Lipid Rafts Independent of Monoamine Transporters to Modulate Redistribution of the G Protein, Gαs

J Biol Chem. 2016 Sep 16;291(38):19725-19733. doi: 10.1074/jbc.M116.727263. Epub 2016 Jul 18.

Abstract

Depression is a significant public health problem for which currently available medications, if effective, require weeks to months of treatment before patients respond. Previous studies have shown that the G protein responsible for increasing cAMP (Gαs) is increasingly localized to lipid rafts in depressed subjects and that chronic antidepressant treatment translocates Gαs from lipid rafts. Translocation of Gαs, which shows delayed onset after chronic antidepressant treatment of rats or of C6 glioma cells, tracks with the delayed onset of therapeutic action of antidepressants. Because antidepressants appear to specifically modify Gαs localized to lipid rafts, we sought to determine whether structurally diverse antidepressants accumulate in lipid rafts. Sustained treatment of C6 glioma cells, which lack 5-hydroxytryptamine transporters, showed marked concentration of several antidepressants in raft fractions, as revealed by increased absorbance and by mass fingerprint. Closely related molecules without antidepressant activity did not concentrate in raft fractions. Thus, at least two classes of antidepressants accumulate in lipid rafts and effect translocation of Gαs to the non-raft membrane fraction, where it activates the cAMP-signaling cascade. Analysis of the structural determinants of raft localization may both help to explain the hysteresis of antidepressant action and lead to design and development of novel substrates for depression therapeutics.

Keywords: G protein; G protein-coupled receptor (GPCR); cyclic AMP (cAMP); depression; drug action; gas chromatography-mass spectrometry (GC-MS); glia; glial cell; heterotrimeric G protein; intracellular trafficking; lipid; lipid raft; mass spectrometry (MS); membrane trafficking; monoamine transporter; plasma membrane; protein translocation; protein-drug interaction; protein-lipid interaction; selective serotonin reuptake inhibitor (SSRI); serotonin; serotonin transporter.

Publication types

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

MeSH terms

  • Animals
  • Antidepressive Agents / pharmacology*
  • Cell Line, Tumor
  • Chromogranins / genetics
  • Chromogranins / metabolism*
  • Cyclic AMP / genetics
  • Cyclic AMP / metabolism
  • GTP-Binding Protein alpha Subunits, Gs / genetics
  • GTP-Binding Protein alpha Subunits, Gs / metabolism*
  • Membrane Microdomains / genetics
  • Membrane Microdomains / metabolism*
  • Protein Transport / drug effects
  • Protein Transport / physiology
  • Rats
  • Second Messenger Systems / drug effects*
  • Second Messenger Systems / physiology
  • Serotonin Plasma Membrane Transport Proteins / genetics
  • Serotonin Plasma Membrane Transport Proteins / metabolism*

Substances

  • Antidepressive Agents
  • Chromogranins
  • Serotonin Plasma Membrane Transport Proteins
  • Cyclic AMP
  • Gnas protein, rat
  • GTP-Binding Protein alpha Subunits, Gs