HMGB1 released from pyroptotic vascular endothelial cells promotes immune disorders in exertional heatstroke

Int J Hyperthermia. 2024;41(1):2378867. doi: 10.1080/02656736.2024.2378867. Epub 2024 Aug 8.

Abstract

Background and objective: Exertional heatstroke (EHS) mainly occurs in healthy young people with rapid onset and high mortality. EHS immune disorders can cause systemic inflammatory responses and multiple organ failure; however, the underlying mechanisms remain unclear. As high mobility group box 1 (HMGB1) is a prototypical alarmin that activates inflammatory and immune responses, this study aimed to investigate the effect and mechanism of HMGB1 in the pathogenesis of EHS.

Methods: Peripheral blood mononuclear cell (PBMC) transcriptome sequencing of healthy volunteers, classical heatstroke patients, and EHS patients was performed. A mouse model of EHS was established and murine tissue damage was evaluated by H&E staining. HMGB1 localization and release were visualized using immunofluorescence staining. Human umbilical vein endothelial cells (HUVECs) and THP-1 cells were co-cultured to study the effects of HMGB1 on macrophages. A neutralizing anti-HMGB1 antibody was used to evaluate the efficacy of EHS treatment in mice.

Results: Plasma and serum HMGB1 levels were significantly increased in EHS patients or mice. EHS-induced endothelial cell pyroptosis promoted HMGB1 release in mice. HMGB1 derived from endothelial cell pyroptosis enhanced macrophage pyroptosis, resulting in immune disorders under EHS conditions. Administration of anti-HMGB1 markedly alleviated tissue injury and systemic inflammatory responses after EHS.

Conclusions: The release of HMGB1 from pyroptotic endothelial cells after EHS promotes pyroptosis of macrophages and systemic inflammatory response, and HMGB1-neutralizing antibody therapy has good application prospects for EHS.

Keywords: Exertional heatstroke; HMGB1; endothelial cells; macrophages; pyroptosis.

MeSH terms

  • Animals
  • Endothelial Cells / metabolism
  • Female
  • HMGB1 Protein* / metabolism
  • Heat Stroke* / complications
  • Heat Stroke* / immunology
  • Heat Stroke* / metabolism
  • Humans
  • Immune System Diseases
  • Male
  • Mice

Substances

  • HMGB1 Protein
  • HMGB1 protein, human
  • HMGB1 protein, mouse