UCP2 knockout exacerbates sepsis-induced intestinal injury by promoting NLRP3-mediated pyroptosis

Int Immunopharmacol. 2024 Nov 15:141:112935. doi: 10.1016/j.intimp.2024.112935. Epub 2024 Aug 18.

Abstract

Sepsis-induced intestinal injury is a common complication that increases the morbidity and mortality associated with sepsis. UCP2, a mitochondrial membrane protein, is involved in numerous cellular processes, including metabolism, inflammation, and pyroptosis. According to our previous studies, UCP2 expression increases in septic intestinal tissue. However, its function in intestinal damage is not known. This work investigated UCP2's role in intestinal injury caused by sepsis. A sepsis mouse model was established in wild-type and UCP2-knockout (UCP2-KO) animals using cecal ligation and puncture (CLP). MCC950, an NLRP3 inflammasome inhibitor, was injected intraperitoneally 3 h before CLP surgery. Overall, significantly higher levels of UCP2 were observed in the intestines of septic mice. UCP2-KO mice subjected to CLP exhibited exacerbated intestinal damage, characterized by enhanced mucosal erosion, inflammatory cell infiltration, and increased intestinal permeability. Furthermore, UCP2 knockout significantly increased oxidative stress, inflammation, and pyroptosis in the CLP mouse intestines. Interestingly, MCC950 not only inhibited pyroptosis but also reversed inflammation, oxidative stress as well as damage to intestinal tissues as a result of UCP2 knockout. Our results highlighted the protective functions of UCP2 in sepsis-associated intestinal injury through modulation of inflammation and oxidative stress via NLRP3 inflammasome-induced pyroptosis.

Keywords: NLRP3; Pyroptosis; Sepsis-induced intestinal injury; UCP2.

MeSH terms

  • Animals
  • Disease Models, Animal
  • Furans / pharmacology
  • Indenes
  • Inflammasomes / metabolism
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / pathology
  • Intestines / immunology
  • Intestines / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Mice, Knockout*
  • NLR Family, Pyrin Domain-Containing 3 Protein* / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein* / metabolism
  • Oxidative Stress
  • Pyroptosis*
  • Sepsis* / complications
  • Sepsis* / immunology
  • Sepsis* / metabolism
  • Sulfonamides / pharmacology
  • Sulfones / pharmacology
  • Uncoupling Protein 2* / genetics
  • Uncoupling Protein 2* / metabolism

Substances

  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Uncoupling Protein 2
  • Nlrp3 protein, mouse
  • Ucp2 protein, mouse
  • N-(1,2,3,5,6,7-hexahydro-S-indacen-4-ylcarbamoyl)-4-(2-hydroxy-2-propanyl)-2-furansulfonamide
  • Inflammasomes
  • Sulfonamides
  • Indenes
  • Furans
  • Sulfones