Glycolytic enzyme PGK1 promotes M1 macrophage polarization and induces pyroptosis of acute lung injury via regulation of NLRP3

Respir Res. 2024 Jul 30;25(1):291. doi: 10.1186/s12931-024-02926-8.

Abstract

Acute lung injury (ALI) is characterized by an unregulated inflammatory reaction, often leading to severe morbidity and ultimately death. Excessive inflammation caused by M1 macrophage polarization and pyroptosis has been revealed to have a critical role in ALI. Recent study suggests that glycolytic reprogramming is important in the regulation of macrophage polarization and pyroptosis. However, the particular processes underlying ALI have yet to be identified. In this study, we established a Lipopolysaccharide(LPS)-induced ALI model and demonstrated that blocking glycolysis by using 2-Deoxy-D-glucose(2-DG) significantly downregulated the expression of M1 macrophage markers and pyroptosis-related genes, which was consistent with the in vitro results. Furthermore, our research has revealed that Phosphoglycerate Kinase 1(PGK1), an essential enzyme in the glycolysis pathway, interacts with NOD-, LRR- and pyrin domain-containing protein 3(NLRP3). We discovered that LPS stimulation improves the combination of PGK1 and NLRP3 both in vivo and in vitro. Interestingly, the absence of PGK1 reduces the phosphorylation level of NLRP3. Based on in vitro studies with mice bone marrow-derived macrophages (BMDMs), we further confirmed that siPGK1 plays a protective role by inhibiting macrophage pyroptosis and M1 macrophage polarization. The PGK1 inhibitor NG52 suppresses the occurrence of excessive inflammation in ALI. In general, it is plausible to consider a therapeutic strategy that focuses on modulating the relationship between PGK1 and NLRP3 as a means to mitigate the activation of inflammatory macrophages in ALI.

Keywords: Acute lung injury; Glycolytic reprogramming; Macrophage polarization; Pyroptosis.

MeSH terms

  • Acute Lung Injury* / chemically induced
  • Acute Lung Injury* / enzymology
  • Acute Lung Injury* / metabolism
  • Acute Lung Injury* / pathology
  • Animals
  • Cells, Cultured
  • Glycolysis / drug effects
  • Glycolysis / physiology
  • Lipopolysaccharides / toxicity
  • Macrophages* / drug effects
  • Macrophages* / enzymology
  • Macrophages* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Mice, Knockout
  • NLR Family, Pyrin Domain-Containing 3 Protein* / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein* / metabolism
  • Phosphoglycerate Kinase* / genetics
  • Phosphoglycerate Kinase* / metabolism
  • Pyroptosis* / drug effects
  • Pyroptosis* / physiology

Substances

  • Phosphoglycerate Kinase
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Pgk1 protein, mouse
  • Nlrp3 protein, mouse
  • Lipopolysaccharides