Hydrogen attenuates sepsis-associated encephalopathy by NRF2 mediated NLRP3 pathway inactivation

Inflamm Res. 2020 Jul;69(7):697-710. doi: 10.1007/s00011-020-01347-9. Epub 2020 Apr 30.

Abstract

Objective: Sepsis-associated encephalopathy (SAE) is a major cause of mortality worldwide. Oxidative stress, inflammatory response and apoptosis participate in the pathogenesis of SAE. Nuclear factor erythroid 2-related factor 2 (Nrf2) and nucleotide-binding oligomerization domain-like receptor containing pyrin domain 3 (NLRP3) pathway is involved in oxidative stress and inflammatory response. We reported that hydrogen gas protected against sepsis in wild-type (WT) but not Nrf2 knockout (KO) mice. Therefore, it is vital to identify the underlying cause of hydrogen gas treatment of sepsis-associated encephalopathy.

Methods: SAE was induced in WT and Nrf2 KO mice by cecal ligation and puncture (CLP). As a NLRP3 inflammasome inhibitor, MCC950 (50 mg/kg) was administered by intraperitoneal (i.p.) injection before operation. Hydrogen gas (H2)-rich saline solution (5 mL/kg) was administered by i.p. injection at 1 h and 6 h after sham and CLP operations. Brain tissue was collected to assess the NLRP3 and Nrf2 pathways by western blotting, reverse transcription-polymerase chain reaction (RT-PCR) and immunofluorescence.

Results: SAE increased NLRP3 and Nrf2 expression in microglia. MCC950 inhibited SAE-induced NLRP3 expression, interleukin (IL)-1β and IL-18 cytokine release, neuronal apoptosis and mitochondrial dysfunction. SAE increased NLRP3 and caspase-1 expression in WT mice compared to Nrf2 KO mice. Hydrogen increased Nrf2 expression and inhibited the SAE-induced expression of NLRP3, caspase-1, cytokines IL-1β and IL-18, neuronal apoptosis, and mitochondrial dysfunction in WT mice but not Nrf2 KO mice.

Conclusion: SAE increased NLRP3 and Nrf2 expression in microglia. Hydrogen alleviated inflammation, neuronal apoptosis and mitochondrial dysfunction via inhibiting Nrf2-mediated NLRP3 pathway.

Keywords: Hydrogen; NLRP3; Nrf2; SAE.

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Brain / metabolism
  • Brain / pathology
  • Brain Chemistry
  • Cecum
  • Cerebral Cortex / ultrastructure
  • Cytokines / metabolism
  • Furans
  • Heterocyclic Compounds, 4 or More Rings / pharmacology
  • Hydrogen / administration & dosage*
  • Indenes
  • Male
  • Mice
  • Mice, Knockout
  • Microglia / physiology
  • Mitochondria / physiology
  • NF-E2-Related Factor 2 / deficiency
  • NF-E2-Related Factor 2 / physiology*
  • NLR Family, Pyrin Domain-Containing 3 Protein / analysis
  • NLR Family, Pyrin Domain-Containing 3 Protein / antagonists & inhibitors
  • NLR Family, Pyrin Domain-Containing 3 Protein / physiology*
  • Punctures
  • Sepsis-Associated Encephalopathy / pathology
  • Sepsis-Associated Encephalopathy / prevention & control*
  • Signal Transduction / drug effects*
  • Sulfonamides
  • Sulfones / pharmacology

Substances

  • Cytokines
  • Furans
  • Heterocyclic Compounds, 4 or More Rings
  • Indenes
  • NF-E2-Related Factor 2
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nfe2l2 protein, mouse
  • Nlrp3 protein, mouse
  • Sulfonamides
  • Sulfones
  • N-(1,2,3,5,6,7-hexahydro-S-indacen-4-ylcarbamoyl)-4-(2-hydroxy-2-propanyl)-2-furansulfonamide
  • Hydrogen