Antidepressant actions of ketamine engage cell-specific translation via eIF4E

Nature. 2021 Feb;590(7845):315-319. doi: 10.1038/s41586-020-03047-0. Epub 2020 Dec 16.

Abstract

Effective pharmacotherapy for major depressive disorder remains a major challenge, as more than 30% of patients are resistant to the first line of treatment (selective serotonin reuptake inhibitors)1. Sub-anaesthetic doses of ketamine, a non-competitive N-methyl-D-aspartate receptor antagonist2,3, provide rapid and long-lasting antidepressant effects in these patients4-6, but the molecular mechanism of these effects remains unclear7,8. Ketamine has been proposed to exert its antidepressant effects through its metabolite (2R,6R)-hydroxynorketamine ((2R,6R)-HNK)9. The antidepressant effects of ketamine and (2R,6R)-HNK in rodents require activation of the mTORC1 kinase10,11. mTORC1 controls various neuronal functions12, particularly through cap-dependent initiation of mRNA translation via the phosphorylation and inactivation of eukaryotic initiation factor 4E-binding proteins (4E-BPs)13. Here we show that 4E-BP1 and 4E-BP2 are key effectors of the antidepressant activity of ketamine and (2R,6R)-HNK, and that ketamine-induced hippocampal synaptic plasticity depends on 4E-BP2 and, to a lesser extent, 4E-BP1. It has been hypothesized that ketamine activates mTORC1-4E-BP signalling in pyramidal excitatory cells of the cortex8,14. To test this hypothesis, we studied the behavioural response to ketamine and (2R,6R)-HNK in mice lacking 4E-BPs in either excitatory or inhibitory neurons. The antidepressant activity of the drugs is mediated by 4E-BP2 in excitatory neurons, and 4E-BP1 and 4E-BP2 in inhibitory neurons. Notably, genetic deletion of 4E-BP2 in inhibitory neurons induced a reduction in baseline immobility in the forced swim test, mimicking an antidepressant effect. Deletion of 4E-BP2 specifically in inhibitory neurons also prevented the ketamine-induced increase in hippocampal excitatory neurotransmission, and this effect concurred with the inability of ketamine to induce a long-lasting decrease in inhibitory neurotransmission. Overall, our data show that 4E-BPs are central to the antidepressant activity of ketamine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Antidepressive Agents / pharmacology*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Depressive Disorder, Major / drug therapy
  • Eukaryotic Initiation Factor-4E / metabolism*
  • Eukaryotic Initiation Factors / genetics
  • Eukaryotic Initiation Factors / metabolism
  • Excitatory Postsynaptic Potentials / drug effects
  • Hippocampus / cytology
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Inhibitory Postsynaptic Potentials / drug effects
  • Interneurons / drug effects
  • Interneurons / metabolism
  • Ketamine / analogs & derivatives
  • Ketamine / metabolism
  • Ketamine / pharmacology*
  • Male
  • Mechanistic Target of Rapamycin Complex 1 / metabolism
  • Mice
  • Mutation
  • Neural Inhibition / drug effects
  • Neural Inhibition / genetics
  • Neurons / classification
  • Neurons / cytology
  • Neurons / drug effects*
  • Neurons / metabolism*
  • Protein Biosynthesis / drug effects*
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / metabolism
  • Synaptic Transmission / drug effects

Substances

  • Adaptor Proteins, Signal Transducing
  • Antidepressive Agents
  • Cell Cycle Proteins
  • Eif4ebp1 protein, mouse
  • Eif4ebp2 protein, mouse
  • Eukaryotic Initiation Factor-4E
  • Eukaryotic Initiation Factors
  • Ketamine
  • 6-hydroxynorketamine
  • Mechanistic Target of Rapamycin Complex 1