Clostridium perfringens beta-toxin induces necrostatin-inhibitable, calpain-dependent necrosis in primary porcine endothelial cells

PLoS One. 2013 May 29;8(5):e64644. doi: 10.1371/journal.pone.0064644. Print 2013.

Abstract

Clostridium perfringens β-toxin (CPB) is a β-barrel pore-forming toxin and an essential virulence factor of C. perfringens type C strains, which cause fatal hemorrhagic enteritis in animals and humans. We have previously shown that CPB is bound to endothelial cells within the intestine of affected pigs and humans, and that CPB is highly toxic to primary porcine endothelial cells (pEC) in vitro. The objective of the present study was to investigate the type of cell death induced by CPB in these cells, and to study potential host cell mechanisms involved in this process. CPB rapidly induced lactate dehydrogenase (LDH) release, propidium iodide uptake, ATP depletion, potassium efflux, a marked rise in intracellular calcium [Ca(2+)]i, release of high-mobility group protein B1 (HMGB1), and caused ultrastructural changes characteristic of necrotic cell death. Despite a certain level of caspase-3 activation, no appreciable DNA fragmentation was detected. CPB-induced LDH release and propidium iodide uptake were inhibited by necrostatin-1 and the two dissimilar calpain inhibitors PD150606 and calpeptin. Likewise, inhibition of potassium efflux, chelation of intracellular calcium and treatment of pEC with cyclosporin A also significantly inhibited CPB-induced LDH release. Our results demonstrate that rCPB primarily induces necrotic cell death in pEC, and that necrotic cell death is not merely a passive event caused by toxin-induced membrane disruption, but is propagated by host cell-dependent biochemical pathways activated by the rise in intracellular calcium and inhibitable by necrostatin-1, consistent with the emerging concept of programmed necrosis ("necroptosis").

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acrylates / pharmacology
  • Animals
  • Bacterial Toxins / pharmacology*
  • Blotting, Western
  • Calcium / metabolism
  • Calpain / antagonists & inhibitors
  • Calpain / metabolism*
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Cell Membrane / ultrastructure
  • Cells, Cultured
  • Cysteine Proteinase Inhibitors / pharmacology
  • DNA Fragmentation / drug effects
  • Dipeptides / pharmacology
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Flow Cytometry
  • HMGB1 Protein / metabolism
  • Imidazoles / pharmacology*
  • Indoles / pharmacology*
  • Intracellular Space / drug effects
  • Intracellular Space / metabolism
  • Ion Transport / drug effects
  • L-Lactate Dehydrogenase
  • Microscopy, Electron, Transmission
  • Necrosis
  • Potassium / metabolism
  • Swine

Substances

  • Acrylates
  • Bacterial Toxins
  • CPB protein, Clostridium perfringens
  • Cysteine Proteinase Inhibitors
  • Dipeptides
  • HMGB1 Protein
  • Imidazoles
  • Indoles
  • PD 150606
  • necrostatin-1
  • calpeptin
  • L-Lactate Dehydrogenase
  • Calpain
  • Potassium
  • Calcium

Grants and funding

This study was financially supported by the Swiss National Science Foundation (31000-120725 to SC), and by a Short International Visit Grant (HP) from the Swiss National Science Foundation (IZK0Z3_133953). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.