Hepatic pannexin-1 mediates ST2+ regulatory T cells promoting resolution of inflammation in lipopolysaccharide-induced endotoxemia

Clin Transl Med. 2022 May;12(5):e849. doi: 10.1002/ctm2.849.

Abstract

Sepsis remains the most lethal infectious disease and substantially impairs patient prognosis after liver transplantation (LT). Our previous study reported a role of the pannexin 1 (PANX1)-interleukin-33 (IL-33) axis in activating innate immunity to protect against methicillin-resistant Staphylococcus aureus infection; however, the role of PANX1 in regulating adaptive immunity in sepsis and the underlying mechanism are unclear. In this study, we examined the role of the PANX1-IL-33 axis in protecting against sepsis caused by a gram-negative bacterial infection in an independent LT cohort. Next, in animal studies, we assessed the immunological state of Panx1-/- mice with lipopolysaccharide (LPS)-induced endotoxemia and then focused on the cytokine storm and regulatory T cells (Tregs), which are crucial for the resolution of inflammation. To generate liver-specific Panx1-deficient mice and mimic clinical LT procedures, a mouse LT model was established. We demonstrated that hepatic PANX1 deficiency exacerbated LPS-induced endotoxemia and dysregulated the immune response in the mouse LT model. In hepatocytes, we confirmed that PANX1 positively regulated IL-33 synthesis after LPS administration. We showed that the adenosine triphosphate-P2X7 pathway regulated the hepatic PANX1-IL-33 axis during endotoxemia in vitro and in vivo. Recombinant IL-33 treatment rescued LPS-induced endotoxemia by increasing the numbers of liver-infiltrating ST2+ Tregs and attenuating the cytokine storm in hepatic PANX1-deficient mice. In conclusion, our findings revealed that the hepatic PANX1-IL-33 axis protects against endotoxemia and liver injury by targeting ST2+ Tregs and promoting the early resolution of hyperinflammation.

Keywords: ATP; IL-33; Panx1; Tregs; endotoxemia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Connexins / genetics
  • Connexins / metabolism
  • Cytokine Release Syndrome
  • Disease Models, Animal
  • Endotoxemia* / chemically induced
  • Humans
  • Inflammation / chemically induced
  • Inflammation / complications
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-33
  • Lipopolysaccharides / toxicity
  • Liver / metabolism
  • Methicillin-Resistant Staphylococcus aureus* / metabolism
  • Mice
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Sepsis* / complications
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Connexins
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-33
  • Lipopolysaccharides
  • Nerve Tissue Proteins
  • PANX1 protein, human
  • Panx1 protein, mouse