Cell-type-specific role for nucleus accumbens neuroligin-2 in depression and stress susceptibility

Proc Natl Acad Sci U S A. 2018 Jan 30;115(5):1111-1116. doi: 10.1073/pnas.1719014115. Epub 2018 Jan 16.

Abstract

Behavioral coping strategies are critical for active resilience to stress and depression; here we describe a role for neuroligin-2 (NLGN-2) in the nucleus accumbens (NAc). Neuroligins (NLGN) are a family of neuronal postsynaptic cell adhesion proteins that are constituents of the excitatory and inhibitory synapse. Importantly, NLGN-3 and NLGN-4 mutations are strongly implicated as candidates underlying the development of neuropsychiatric disorders with social disturbances such as autism, but the role of NLGN-2 in neuropsychiatric disease states is unclear. Here we show a reduction in NLGN-2 gene expression in the NAc of patients with major depressive disorder. Chronic social defeat stress in mice also decreases NLGN-2 selectively in dopamine D1-positive cells, but not dopamine D2-positive cells, within the NAc of stress-susceptible mice. Functional NLGN-2 knockdown produces bidirectional, cell-type-specific effects: knockdown in dopamine D1-positive cells promotes subordination and stress susceptibility, whereas knockdown in dopamine D2-positive cells mediates active defensive behavior. These findings establish a behavioral role for NAc NLGN-2 in stress and depression; provide a basis for targeted, cell-type specific therapy; and highlight the role of active behavioral coping mechanisms in stress susceptibility.

Keywords: depression; dominance; medium spiny neuron; neuroligin-2; social defeat stress.

Publication types

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

MeSH terms

  • Aggression
  • Animals
  • Antidepressive Agents / pharmacology
  • Behavior, Animal
  • Cell Adhesion Molecules, Neuronal / metabolism*
  • Cell Line
  • Depressive Disorder, Major / physiopathology*
  • Disease Models, Animal
  • Dominance-Subordination*
  • Heterozygote
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • MicroRNAs / metabolism
  • Nerve Tissue Proteins / metabolism*
  • Nucleus Accumbens / metabolism*
  • RNA, Messenger / metabolism
  • Receptors, Dopamine D1 / metabolism
  • Receptors, Dopamine D2 / metabolism
  • Social Behavior
  • Stress, Psychological / physiopathology*
  • Synapses / metabolism

Substances

  • Antidepressive Agents
  • Cell Adhesion Molecules, Neuronal
  • MicroRNAs
  • Nerve Tissue Proteins
  • RNA, Messenger
  • Receptors, Dopamine D1
  • Receptors, Dopamine D2
  • neuroligin 2