Neuronal synapse formation induced by microglia and interleukin 10

PLoS One. 2013 Nov 22;8(11):e81218. doi: 10.1371/journal.pone.0081218. eCollection 2013.

Abstract

Recently, it was found that microglia regulated synaptic remodeling of the developing brain, but their mechanisms have not been well understood. In this study, the action of microglia on neuronal synapse formation was investigated, and the primary target of microglial processes was discovered. When the developing microglia were applied to cultured hippocampal neurons without direct contact, the numbers of dendritic spines and excitatory and inhibitory synapses significantly increased. In order to find out the main factor for synaptic formation, the effects of cytokines released from microglia were examined. When recombinant proteins of cytokines were applied to neuronal culture media, interleukin 10 increased the numbers of dendritic spines in addition to excitatory and inhibitory synapses. Interestingly, without external stimuli, the amount of interleukin 10 released from the intact microglia appeared to be sufficient for the induction of synaptic formation. The neutralizing antibodies of interleukin 10 receptors attenuated the induction of the synaptic formation by microglia. The expression of interleukin 10 receptor was newly found in the hippocampal neurons of early developmental stage. When interleukin 10 receptors on the hippocampal neurons were knocked down with specific shRNA, the induction of synaptic formation by microglia and interleukin 10 disappeared. Pretreatment with lipopolysaccharide inhibited microglia from inducing synaptic formation, and interleukin 1β antagonized the induction of synaptic formation by interleukin 10. In conclusion, the developing microglia regulated synaptic functions and neuronal development through the interactions of the interleukin 10 released from the microglia with interleukin 10 receptors expressed on the hippocampal neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Gene Expression
  • Gene Knockdown Techniques
  • Hippocampus / cytology
  • Hippocampus / metabolism
  • Interleukin-10 / metabolism*
  • Interleukin-10 / pharmacology
  • Interleukin-1beta / metabolism
  • Interleukin-1beta / pharmacology
  • Microglia / metabolism*
  • Neuroeffector Junction / drug effects
  • Neuroeffector Junction / metabolism*
  • Pyramidal Cells / metabolism
  • Rats
  • Receptors, Interleukin-10 / genetics
  • Receptors, Interleukin-10 / metabolism

Substances

  • Interleukin-1beta
  • Receptors, Interleukin-10
  • Interleukin-10

Grants and funding

National Research Foundation of Korea (NRF) grant funded by the Korea government (2012R1A2A2A02014520 and 2009-0087354 to J.R.L.) and a grant from KRIBB research initiative program (to J.R.L.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.