tDCS Regulates ASBT-3-OxoLCA-PLOD2-PTEN Signaling Pathway to Confer Neuroprotection Following Rat Cerebral Ischemia-Reperfusion Injury

Mol Neurobiol. 2023 Nov;60(11):6715-6730. doi: 10.1007/s12035-023-03504-7. Epub 2023 Jul 21.

Abstract

Humans exhibit a rich intestinal microbiome that contain high levels of bacteria capable of producing 3-oxo-lithocholic acid (3-oxoLCA) and other secondary bile acids (BAs). The molecular mechanism mediating the role of 3-oxoLCA in cerebral ischemia-reperfusion (I/R) injury remains unclear. We investigated the role of 3-oxoLCA in a rat cerebral I/R injury model. We found that the concentrations of 3-oxoLCA within the cerebrospinal fluid were increased following I/R. In the in vitro oxygen-glucose deprivation (OGD) model, the levels of intraneuronal 3-oxoLCA was elevated following OGD insult. We showed that the increase of membrane ASBT (apical sodium-dependent bile acid transporter) contributed to OGD-induced elevation of intraneuronal 3-oxoLCA. Increasing intraneuronal 3-oxoLCA promoted ischemia-induced neuronal death, whereas reducing 3-oxoLCA levels were neuroprotective. Our results revealed that PLOD2 (procollagen-lysine, 2-oxoglutarate 5-dioxygenases 2) functioned upstream of PTEN (the phosphatase and tensin homolog deleted on chromosome 10) and downstream of 3-oxoLCA to promote OGD-induced neuronal injury. We further demonstrated that direct-current stimulation (DCS) decreased the levels of intraneuronal 3-oxoLCA and membrane ASBT in OGD-insulted neurons, while bilateral transcranial DCS (tDCS) reduced brain infarct volume following I/R by inhibiting ASBT. Together, these data suggest that increased expression of ASBT promotes neuronal death via 3-oxoLCA-PLOD2-PTEN signaling pathway. Importantly, bilateral tDCS suppresses ischemia-induced increase of ASBT, thereby conferring neuroprotection after cerebral I/R injury.

Keywords: 3-OxoLCA; Cerebral ischemic stroke; Neuroprotection; PLOD2.

MeSH terms

  • Animals
  • Apoptosis
  • Brain Ischemia* / metabolism
  • Cerebral Infarction
  • Glucose / metabolism
  • Humans
  • Neuroprotection
  • Oxygen / metabolism
  • PTEN Phosphohydrolase / metabolism
  • Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase / metabolism
  • Rats
  • Reperfusion Injury* / metabolism
  • Signal Transduction
  • Transcranial Direct Current Stimulation*

Substances

  • Oxygen
  • Glucose
  • PLOD2 protein, human
  • Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase
  • PTEN protein, human
  • PTEN Phosphohydrolase