Dengue Envelope Protein as a Cytotoxic Factor Inducing Hemorrhage and Endothelial Cell Death in Mice

Int J Mol Sci. 2024 Oct 9;25(19):10858. doi: 10.3390/ijms251910858.

Abstract

Dengue virus (DENV) infection, prevalent in tropical and subtropical regions, can progress to dengue hemorrhagic fever (DHF), which increases mortality during secondary infections. DHF is characterized by endothelial damage and vascular leakage. Despite its severity, no specific antiviral treatments exist, and the viral factors responsible for endothelial damage remain unclear. This study examines the role of the DENV envelope protein domain III (EIII) in inducing endothelial apoptosis using a mouse model. Additionally, we aim to explore whether cell death-inducing pathways could serve as drug targets to ameliorate EIII-induced endothelial injury and hemorrhage. In vitro experiments using human endothelial HMEC-1 cells demonstrated that both recombinant EIII (rEIII) and DENV markedly induced caspase-3-mediated endothelial cell death, an effect that was attenuated by co-treatment with chondroitin sulfate B (CSB), N-acetyl cysteine (NAC), and the caspase-3 inhibitor z-DEVD-FMK. In vivo, sequential injections of rEIII and anti-platelet immunoglobulin in mice, designed to mimic the clinical phase of DHF with peak viremia followed by an increase in DENV-induced Ig, including autoantibodies, revealed that these dual treatments markedly triggered caspase-3-dependent apoptosis in vascular endothelial cells at hemorrhage sites. Treatments with z-DEVD-FMK effectively reduced DHF-like symptoms such as thrombocytopenia, hemorrhage, inflammation, hypercoagulation, and endothelial damage. Additionally, CSB and NAC alleviated hemorrhagic symptoms in the mice. These results suggest that targeting EIII, reactive oxygen species, and caspase-3-mediated apoptosis could offer potential therapeutic strategies for addressing EIII-induced hemorrhagic pathogenesis.

Keywords: N-acetyl cysteine; caspase-3; chondroitin sulfate B; dengue hemorrhagic fever; endothelial cell apoptosis; envelope protein domain III; z-DEVD-FMK.

MeSH terms

  • Animals
  • Apoptosis* / drug effects
  • Caspase 3 / metabolism
  • Cell Death / drug effects
  • Cell Line
  • Dengue / drug therapy
  • Dengue / pathology
  • Dengue Virus*
  • Disease Models, Animal
  • Endothelial Cells* / drug effects
  • Endothelial Cells* / metabolism
  • Hemorrhage* / drug therapy
  • Humans
  • Mice
  • Severe Dengue* / drug therapy
  • Severe Dengue* / pathology
  • Viral Envelope Proteins* / metabolism

Substances

  • Viral Envelope Proteins
  • Caspase 3