Foodborne cereulide causes beta-cell dysfunction and apoptosis

PLoS One. 2014 Aug 13;9(8):e104866. doi: 10.1371/journal.pone.0104866. eCollection 2014.

Abstract

Aims/hypothesis: To study the effects of cereulide, a food toxin often found at low concentrations in take-away meals, on beta-cell survival and function.

Methods: Cell death was quantified by Hoechst/Propidium Iodide in mouse (MIN6) and rat (INS-1E) beta-cell lines, whole mouse islets and control cell lines (HepG2 and COS-1). Beta-cell function was studied by glucose-stimulated insulin secretion (GSIS). Mechanisms of toxicity were evaluated in MIN6 cells by mRNA profiling, electron microscopy and mitochondrial function tests.

Results: 24 h exposure to 5 ng/ml cereulide rendered almost all MIN6, INS-1E and pancreatic islets apoptotic, whereas cell death did not increase in the control cell lines. In MIN6 cells and murine islets, GSIS capacity was lost following 24 h exposure to 0.5 ng/ml cereulide (P<0.05). Cereulide exposure induced markers of mitochondrial stress including Puma (p53 up-regulated modulator of apoptosis, P<0.05) and general pro-apoptotic signals as Chop (CCAAT/-enhancer-binding protein homologous protein). Mitochondria appeared swollen upon transmission electron microscopy, basal respiration rate was reduced by 52% (P<0.05) and reactive oxygen species increased by more than twofold (P<0.05) following 24 h exposure to 0.25 and 0.50 ng/ml cereulide, respectively.

Conclusions/interpretation: Cereulide causes apoptotic beta-cell death at low concentrations and impairs beta-cell function at even lower concentrations, with mitochondrial dysfunction underlying these defects. Thus, exposure to cereulide even at concentrations too low to cause systemic effects appears deleterious to the beta-cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • COS Cells
  • Cell Line
  • Chlorocebus aethiops
  • Depsipeptides / toxicity*
  • Food Microbiology*
  • Glucose / metabolism
  • Hep G2 Cells
  • Humans
  • Insulin / metabolism
  • Insulin-Secreting Cells / cytology
  • Insulin-Secreting Cells / drug effects*
  • Insulin-Secreting Cells / metabolism
  • Insulin-Secreting Cells / pathology*
  • Islets of Langerhans / cytology
  • Islets of Langerhans / drug effects
  • Islets of Langerhans / metabolism
  • Islets of Langerhans / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • Mitochondria / ultrastructure
  • Rats

Substances

  • Depsipeptides
  • Insulin
  • cereulide
  • Glucose

Grants and funding

This research was supported by grants from the Flemish Research Foundation (G.0857.13, www.fwo.be) and the University of Leuven (GOA 13/006 and IOF KP/12012, www.kuleuven.be/research/funding). C. Mathieu has a clinical research fellowship and W. D'Hertog a postdoctoral fellowship from the Flemish Research Foundation (FWO). I. Crèvecoeur has a grant from the Agency for Innovation of Science and Technology (IWT, 121086, www.IWT.be). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.