Amygdalar κ-opioid receptor-dependent upregulating glutamate transporter 1 mediates depressive-like behaviors of opioid abstinence

Cell Rep. 2021 Nov 2;37(5):109913. doi: 10.1016/j.celrep.2021.109913.

Abstract

Opiates produce a strong rewarding effect, but abstinence from opiate use emerges with severe negative emotions. Depression is one of the most frequent emotion disorders associated with opiate abstinence, which is thought to be a main cause for relapse. However, neurobiological bases of such an aversive emotion processing are poorly understood. Here, we find that morphine abstinence activates κ-opioid receptors (KORs) by increasing endogenous KOR ligand dynorphin expression in the amygdala, which in turn facilitates glutamate transporter 1 (GLT1) expression by activation of p38 mitogen-activated protein kinase (MAPK). Upregulation of GLT1 expression contributes to opiate-abstinence-elicited depressive-like behaviors through modulating amygdalar glutamatergic inputs to the nucleus accumbens (NAc). Intra-amygdala injection of GLT1 inhibitor DHK or knockdown of GLT1 expression in the amygdala significantly suppresses morphine-abstinence-induced depressive-like behaviors. Pharmacological and pharmacogenetic activation of amygdala-NAc projections prevents morphine-abstinence-induced behaviors. Overall, our study provides key molecular and circuit insights into the mechanisms of depression associated with opiate abstinence.

Keywords: amygdala; depression; dynorphin/κ-opioid receptor; glutamate transporter 1; morphine abstinence; nucleus accumbens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amygdala / metabolism*
  • Amygdala / physiopathology
  • Animals
  • Behavior, Animal*
  • Depression / chemically induced
  • Depression / metabolism*
  • Depression / physiopathology
  • Depression / psychology
  • Disease Models, Animal
  • Dynorphins / metabolism
  • Excitatory Postsynaptic Potentials
  • Glucose Transporter Type 1 / genetics
  • Glucose Transporter Type 1 / metabolism*
  • Glutamic Acid / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Morphine*
  • Neural Pathways / metabolism
  • Neural Pathways / physiopathology
  • Nucleus Accumbens / metabolism*
  • Nucleus Accumbens / physiopathology
  • Receptors, Opioid, kappa / genetics
  • Receptors, Opioid, kappa / metabolism*
  • Signal Transduction
  • Substance Withdrawal Syndrome / metabolism*
  • Substance Withdrawal Syndrome / physiopathology
  • Substance Withdrawal Syndrome / psychology
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Glucose Transporter Type 1
  • Receptors, Opioid, kappa
  • Slc2a1 protein, mouse
  • Glutamic Acid
  • Dynorphins
  • Morphine
  • p38 Mitogen-Activated Protein Kinases