Bruton's tyrosine kinase inhibition ameliorated neuroinflammation during chronic white matter ischemia

J Neuroinflammation. 2024 Aug 3;21(1):195. doi: 10.1186/s12974-024-03187-4.

Abstract

Chronic cerebral hypoperfusion (CCH), a disease afflicting numerous individuals worldwide, is a primary cause of cognitive deficits, the pathogenesis of which remains poorly understood. Bruton's tyrosine kinase inhibition (BTKi) is considered a promising strategy to regulate inflammatory responses within the brain, a crucial process that is assumed to drive ischemic demyelination progression. However, the potential role of BTKi in CCH has not been investigated so far. In the present study, we elucidated potential therapeutic roles of BTK in both in vitro hypoxia and in vivo ischemic demyelination model. We found that cerebral hypoperfusion induced white matter injury, cognitive impairments, microglial BTK activation, along with a series of microglia responses associated with inflammation, oxidative stress, mitochondrial dysfunction, and ferroptosis. Tolebrutinib treatment suppressed both the activation of microglia and microglial BTK expression. Meanwhile, microglia-related inflammation and ferroptosis processes were attenuated evidently, contributing to lower levels of disease severity. Taken together, BTKi ameliorated white matter injury and cognitive impairments induced by CCH, possibly via skewing microglia polarization towards anti-inflammatory and homeostatic phenotypes, as well as decreasing microglial oxidative stress damage and ferroptosis, which exhibits promising therapeutic potential in chronic cerebral hypoperfusion-induced demyelination.

Keywords: Chronic cerebral hypoperfusion; Ferroptosis; Inflammation; Microglia; Tolebrutinib.

MeSH terms

  • Agammaglobulinaemia Tyrosine Kinase* / antagonists & inhibitors
  • Agammaglobulinaemia Tyrosine Kinase* / metabolism
  • Animals
  • Brain Ischemia* / drug therapy
  • Brain Ischemia* / metabolism
  • Brain Ischemia* / pathology
  • Chronic Disease
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microglia / drug effects
  • Microglia / metabolism
  • Microglia / pathology
  • Neuroinflammatory Diseases / drug therapy
  • Neuroinflammatory Diseases / metabolism
  • Neuroinflammatory Diseases / pathology
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinase Inhibitors / therapeutic use
  • White Matter* / drug effects
  • White Matter* / metabolism
  • White Matter* / pathology

Substances

  • Agammaglobulinaemia Tyrosine Kinase
  • Protein Kinase Inhibitors