ATP depletion in anthrax edema toxin pathogenesis

PLoS Pathog. 2025 Apr 1;21(4):e1013017. doi: 10.1371/journal.ppat.1013017. eCollection 2025 Apr.

Abstract

Anthrax lethal toxin (LT) and edema toxin (ET) are two of the major virulence factors of Bacillus anthracis, the causative pathogen of anthrax disease. While the roles of LT in anthrax pathogenesis have been extensively studied, the pathogenic mechanism of ET remains poorly understood. ET is a calmodulin-dependent adenylate cyclase that elevates intracellular cAMP by converting ATP to cAMP. Thus, it was postulated that the ET-induced in vivo toxicity is mediated by certain cAMP-dependent events. However, mechanisms linking cAMP elevation and ET-induced damage have not been established. Cholera toxin is another bacterial toxin that increases cAMP. This toxin is known to cause severe intestinal fluid secretion and dehydration by cAMP-mediated activation of protein kinase A (PKA), which in turn activates cystic fibrosis transmembrane conductance regulator (CFTR). The cAMP-activated PKA phosphorylation of CFTR on the surface of intestinal epithelial cells leads to an efflux of chloride ions accompanied by secretion of H2O into the intestinal lumen, causing rapid fluid loss, severe diarrhea and dehydration. Due to similar in vivo effects, it was generally believed that ET and cholera toxin would exhibit a similar pathogenic mechanism. Surprisingly, in this work, we found that cAMP-mediated PKA/CFTR activation is not essential for ET to exert its in vivo toxicity. Instead, our data suggest that ET-induced ATP depletion may play an important role in the toxin's pathogenesis.

MeSH terms

  • Adenosine Triphosphate* / metabolism
  • Animals
  • Anthrax* / metabolism
  • Anthrax* / pathology
  • Antigens, Bacterial* / metabolism
  • Antigens, Bacterial* / toxicity
  • Bacillus anthracis* / metabolism
  • Bacillus anthracis* / pathogenicity
  • Bacterial Toxins* / metabolism
  • Bacterial Toxins* / toxicity
  • Cyclic AMP / metabolism
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Cystic Fibrosis Transmembrane Conductance Regulator / metabolism
  • Humans
  • Mice

Substances

  • Bacterial Toxins
  • anthrax toxin
  • Antigens, Bacterial
  • Adenosine Triphosphate
  • Cyclic AMP
  • Cystic Fibrosis Transmembrane Conductance Regulator
  • Cyclic AMP-Dependent Protein Kinases