Therapeutic potential of microglial SMEK1 in regulating H3K9 lactylation in cerebral ischemia-reperfusion

Commun Biol. 2024 Dec 26;7(1):1701. doi: 10.1038/s42003-024-07425-6.

Abstract

Acute ischemic stroke (AIS) triggers immune responses and neuroinflammation, contributing to brain injury. Histone lactylation, a metabolic stress-related histone modification, plays a critical role in various diseases, but its involvement in cerebral ischemia remains unclear. This study utilized a transient middle cerebral artery occlusion/reperfusion (MCAO/R) model and an oxygen-glucose deprivation/reoxygenation (OGD/R) model to investigate the role of microglial histone lactylation in ischemia-reperfusion injury. Lactate overload post-AIS increased histone lactylation, while reduced SMEK1 expression in microglia correlated with elevated lactate and neuroinflammation. Microglia-specific SMEK1 deficiency enhanced lactate production by inhibiting the pyruvate dehydrogenase kinase 3-pyruvate dehydrogenase (PDK3-PDH) pathway, increasing H3 lysine 9 lactylation (H3K9la), activating Ldha and Hif-1α transcription, and promoting glycolysis. SMEK1 overexpression improved neurological recovery in ischemic mice. This study highlights SMEK1 as a novel regulator of histone lactylation and a potential therapeutic target for mitigating neuroinflammation and enhancing recovery after AIS.

MeSH terms

  • Animals
  • Brain Ischemia* / genetics
  • Brain Ischemia* / metabolism
  • Disease Models, Animal
  • Glycolysis
  • Histones* / metabolism
  • Infarction, Middle Cerebral Artery / metabolism
  • Lactic Acid / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microglia* / metabolism
  • Reperfusion Injury* / genetics
  • Reperfusion Injury* / metabolism

Substances

  • Histones
  • Lactic Acid