ALKBH5 demethylates the m6A modification of SOCS3 in microglia/macrophages and alleviates neuroinflammation after brain injury

Proc Natl Acad Sci U S A. 2025 Sep 30;122(39):e2504697122. doi: 10.1073/pnas.2504697122. Epub 2025 Sep 23.

Abstract

Microglia/macrophage-induced neuroinflammation plays a crucial role in the progression of traumatic brain injury (TBI). However, the involvement of N6-methyladenosine (m6A) RNA modifications in this process remains elusive. Single-cell RNA sequencing (scRNA-seq) and m6A RNA immunoprecipitation sequencing (MeRIP-seq) across multiple time points postinjury revealed a strong correlation between m6A modifications and genes enriched in microglia/macrophages. Furthermore, the m6A demethylase ALKBH5 was identified as a key regulator of dynamic m6A patterns at the injury site. ALKBH5 suppression in microglia/macrophages exacerbated neuroinflammation in vitro and worsened neurological deficits in controlled cortical impact (CCI) models. MeRIP-qPCR and RNA pull-down assays revealed SOCS3 was a downstream target of ALKBH5-mediated m6A demethylation. This demethylation stabilized Socs3 mRNA and enhanced its protein expression, which in turn suppressed neuroinflammation via inhibiting the JAK2-STAT3 pathway. Conversely, SOCS3 depletion impaired functional recovery after injury. These findings unveiled a critical ALKBH5-m6A-SOCS3 regulatory axis that mitigated microglia/macrophage-driven neuroinflammation after TBI, underscoring its potential as a therapeutic intervention target for TBI progression.

Keywords: ALKBH5; N6-methyladenosine; SOCS3; microglia; neuroinflammation.

MeSH terms

  • Adenosine* / analogs & derivatives
  • Adenosine* / metabolism
  • AlkB Homolog 5, RNA Demethylase* / genetics
  • AlkB Homolog 5, RNA Demethylase* / metabolism
  • Animals
  • Brain Injuries* / metabolism
  • Brain Injuries, Traumatic* / metabolism
  • Brain Injuries, Traumatic* / pathology
  • Demethylation
  • Macrophages* / metabolism
  • Macrophages* / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microglia* / metabolism
  • Microglia* / pathology
  • Neuroinflammatory Diseases* / metabolism
  • Neuroinflammatory Diseases* / pathology
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction
  • Suppressor of Cytokine Signaling 3 Protein* / genetics
  • Suppressor of Cytokine Signaling 3 Protein* / metabolism

Substances

  • Suppressor of Cytokine Signaling 3 Protein
  • AlkB Homolog 5, RNA Demethylase
  • Socs3 protein, mouse
  • N-methyladenosine
  • Adenosine
  • STAT3 Transcription Factor