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Circulating extracellular vesicle microRNAs mediate immune modulation of social behavior in male mice

  • Ken Matoba
  • , Eisuke Dohi
  • , Phoebe A. Garcia
  • , Jose Francis-Oliveira
  • , Mirmohammadali Mirramezanializamini
  • , Inssaf Berkiks
  • , Frida Anguiano
  • , Jana H. Badrani
  • , Oluwaseun Fatoba
  • , Eric Y. Choi
  • , Julia See
  • , Md Sorwer Alam Parvez
  • , Takahiro Kochi
  • , Norimichi Ito
  • , Rei Mitani
  • , Indigo V.L. Rose
  • , Takashi Imai
  • , David K. Crossman
  • , Mikhail V. Pletnikov
  • , Kenneth W. Witwer
  • Minae Niwa, Shin Ichi Kano
  • University of Alabama at Birmingham
  • Johns Hopkins University
  • National Center of Neurology and Psychiatry Kodaira

Research output: Contribution to journalArticlepeer-review

Abstract

Extracellular vesicles (EVs) are cell-derived small membrane vesicles and circulate throughout the body, but the impact of circulating EVs on brain function and behavior remains elusive. Here, we report that wild-type (WT) mouse blood, particularly EVs, increases sociability in socially impaired immunodeficient Rag1-/- male mice, mimicking the effects of WT T cell transfer. These EVs are localized to neurons and regulate PKCε expression, GABAA receptor synaptic localization, and inhibitory postsynaptic signaling in prefrontal cortex (PFC) pyramidal neurons. Injection of Rag1-/- EVs supplemented with miR-23a-3p and miR-103-3p enhances synaptic function and sociability in Rag1-/- mice. T cells secrete miR-23a-3p via EVs, and Mir23a-/- T cells fail to increase sociability. Similar beneficial effects of WT blood EVs are observed in additional mouse models with sociability deficits, such as Cntnap2-/- and Shank3-/- mice. These findings uncover the role of EV miRNAs in mediating immune modulation of synaptic function and social behavior, revealing a non-canonical molecular pathway for immune-neuron communication.

Original languageEnglish
JournalNature Communications
Volume17
Issue number1
DOIs
StatePublished - Apr 3 2026

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