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Microglial pattern recognition via IL-33 promotes synaptic refinement in developing corticothalamic circuits in mice.

Rafael T Han1, Ilia D Vainchtein1, Johannes C M Schlachetzki2

  • 1Departments of Psychiatry and Behavioral Sciences/Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA.

The Journal of Experimental Medicine
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Interleukin-33 (IL-33) signaling reprograms microglia, enhancing synapse engulfment via pattern recognition receptors like MARCO. This IL-33/MARCO pathway is crucial for regulating brain development and preventing epilepsy.

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Area of Science:

  • Neuroscience
  • Immunology
  • Developmental Biology

Background:

  • Microglia are key players in brain development, clearing synaptic material during synapse remodeling.
  • The environmental cues and molecular mechanisms guiding microglial synapse remodeling remain incompletely understood.

Purpose of the Study:

  • To investigate the regulatory mechanisms of microglia function downstream of interleukin-33 (IL-33).
  • To explore the role of IL-33 in modulating microglial epigenetic landscapes and gene expression.
  • To determine the impact of IL-33 signaling on synaptic development and neuronal excitability.

Main Methods:

  • Analysis of microglial enhancer landscapes and transcription factor binding following IL-33 exposure.
  • RNA sequencing to identify IL-33-induced gene expression programs.
  • Generation of CNS-specific IL-33 knockout mice and MARCO-deficient mice.
  • Electrophysiological recordings and seizure susceptibility tests in mouse models.

Main Results:

  • IL-33 stimulation altered microglial epigenetics, increasing AP-1/FOS binding and upregulating pattern recognition receptors, including MARCO.
  • CNS-specific IL-33 deletion resulted in synaptic imbalance, absence-like seizures, and heightened seizure susceptibility.
  • MARCO deficiency led to excessive thalamic excitatory synapses and increased seizure susceptibility, indicating its role in synapse engulfment.

Conclusions:

  • IL-33 orchestrates epigenetic and functional changes in microglia, impacting postnatal synaptic refinement.
  • Pattern recognition receptors, such as MARCO, are identified as critical regulators of microglial synapse pruning.
  • Dysregulation of the IL-33/MARCO pathway contributes to aberrant synaptic development and epilepsy.