Inhibition of human natural killer cell activity by cereulide, an emetic toxin from<i>Bacillus cereus</i>

Paananen, Auli; Mikkola, Raimo; Sareneva, Timo; Matikainen, Sampsa; Hess, Michael W.; Andersson, Maria A.; Julkunen, Ilkka; Salkinoja‐Salonen, Mirja; Timonen, Tuomo

doi:10.1046/j.1365-2249.2002.01898.x

Cited by 93 publications

(49 citation statements)

References 32 publications

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“…Cereulide is a small, heat-and acid-stable cyclic dodecadepsipeptide (Agata et al, 1994) and is synthesized by a non-ribosomal peptide synthetase, encoded by the ces genes (Ehling-Schulz et al, 2005). It has been shown to cause cellular damage in animal models (Shinagawa et al, 1995) and it has been reported that cereulide inhibits human natural killer cells and might therefore have an immunomodulating effect (Paananen et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains

Svensson²,

et al. 2005

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An in-depth polyphasic approach was applied to study the population structure of the human pathogen Bacillus cereus. To assess the intraspecific biodiversity of this species, which is the causative agent of gastrointestinal diseases, a total of 90 isolates from diverse geographical origin were studied by genetic [M13-PCR, random amplification of polymorphic DNA (RAPD), multilocus sequence typing (MLST)] and phenetic [Fourier transform Infrared (FTIR), protein profiling, biochemical assays] methods. The strain set included clinical strains, isolates from food remnants connected to outbreaks, as well as isolates from diverse food environments with a well documented strain history. The phenotypic and genotypic analysis of the compiled panel of strains illustrated a considerable diversity among B. cereus connected to diarrhoeal syndrome and other non-emetic food strains, but a very low diversity among emetic isolates. Using all typing methods, cluster analysis revealed a single, distinct cluster of emetic B. cereus strains. The isolates belonging to this cluster were neither able to degrade starch nor could they ferment salicin; they did not possess the genes encoding haemolysin BL (Hbl) and showed only weak or no haemolysis. In contrast, haemolytic-enterotoxin-producing B. cereus strains showed a high degree of heterogeneity and were scattered over different clusters when different typing methods were applied. These data provide evidence for a clonal population structure of cereulide-producing emetic B. cereus and indicate that emetic strains represent a highly clonal complex within a potentially panmictic or weakly clonal background population structure of the species. It may have originated only recently through acquisition of specific virulence factors such as the cereulide synthetase gene.Abbreviations: FTIR, Fourier transform Infrared; Hbl, haemolysin BL; MLST, multilocus sequence typing; Nhe, non-haemolytic enterotoxin; RAPD, random amplification of polymorphic DNA.The GenBank/EMBL/DDBJ accession numbers for the sequences of the internal gene fragments used for MLST and for the sporulation stage III AB genes reported in this paper are AY762151-AY762213 and AY578317-AY578349, respectively.

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Section: Introductionmentioning

confidence: 99%

Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains

Svensson²,

et al. 2005

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“…The emetic toxin is produced by vegetative B. cereus cells in food before ingestion and remains active upon stomach transit. It is toxic to mitochondria by acting as a potassium ionophore (38) and has been reported to inhibit human natural killer cells (43). The diarrheal syndrome is caused by enterotoxins secreted by vegetative cells in the small intestine, where they can act by disrupting the integrity of the membrane of epithelial cells (56).…”

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Comparative Transcriptomic and Phenotypic Analysis of the Responses ofBacillus cereusto Various Disinfectant Treatments

Ceragioli

Mols

Moezelaar

et al. 2010

Appl Environ Microbiol

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Antimicrobial chemicals are widely applied to clean and disinfect food-contacting surfaces. However, the cellular response of bacteria to various disinfectants is unclear. In this study, the physiological and genome-wide transcriptional responses of Bacillus cereus ATCC 14579 exposed to four different disinfectants (benzalkonium chloride, sodium hypochlorite, hydrogen peroxide, and peracetic acid) were analyzed. For each disinfectant, concentrations leading to the attenuation of growth, growth arrest, and cell death were determined. The transcriptome analysis revealed that B. cereus, upon exposure to the selected concentrations of disinfectants, induced common and specific responses. Notably, the common response included genes involved in the general and oxidative stress responses. Exposure to benzalkonium chloride, a disinfectant known to induce membrane damage, specifically induced genes involved in fatty acid metabolism. Membrane damage induced by benzalkonium chloride was confirmed by fluorescence microscopy, and fatty acid analysis revealed modulation of the fatty acid composition of the cell membrane. Exposure to sodium hypochlorite induced genes involved in metabolism of sulfur and sulfur-containing amino acids, which correlated with the excessive oxidation of sulfhydryl groups observed in sodium hypochlorite-stressed cells. Exposures to hydrogen peroxide and peracetic acid induced highly similar responses, including the upregulation of genes involved in DNA damage repair and SOS response. Notably, hydrogen peroxide-and peracetic acid-treated cells exhibited high mutation rates correlating with the induced SOS response.

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“…Besides these less acute symptoms, a number of studies have indicated a high toxicity potential concerning immunomodulatory and neuro-and hepatotoxic modes of action (4,39,44). Due to their lower toxic capacity, children and immunosuppressed individuals are especially vulnerable, and cases of fatal liver failure or encephalopathy have been reported (10,31,49,59).…”

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Inhibition of Cereulide Toxin Synthesis by Emetic Bacillus cereus via Long-Chain Polyphosphates

Frenzel

Letzel

Scherer

et al. 2011

Appl Environ Microbiol

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Severe intoxications caused by the Bacillus cereus emetic toxin cereulide can hardly be prevented due to the ubiquitous distribution and heat resistance of spores and the extreme thermal and chemical stability of cereulide. It would therefore be desirable to inhibit cereulide synthesis during food manufacturing processes or in prepared foods, which are stored under time-temperature abuse conditions. Toward this end, the impacts of three long-chain polyphosphate (polyP) formulations on growth and cereulide production were examined. The inhibition was dependent on the concentration and the type of the polyP blend, indicating that polyPs and not the orthophosphates were effective. Quantitative PCR (qPCR) monitoring at sublethal concentrations revealed that polyPs reduced the transcription of ces nonribosomal peptide synthetase (NRPS) genes by 3-to 4-fold along with a significantly reduced toxin production level. At lower concentrations, toxin synthesis was decreased, although the growth rate was not affected. These data indicate a differential effect on toxin synthesis independent of growth inhibition. The inhibition of toxin synthesis in food was also observed. Despite the growth of B. cereus, toxin synthesis was reduced by 70 to 100% in two model food systems (reconstituted infant food and oat milk), which were analyzed with HEp-2 cell culture assays and high-performance liquid chromatography (HPLC)/electrospray ionization-time of flight mass spectrometry (ESI-TOF-MS). Accordingly, ces promoter activity was strongly downregulated, as visualized by using a lux-based reporter strain. These data illustrate the potential of polyphosphate formulations to reduce the risk of cereulide synthesis in food and may contribute to targeted hurdle concepts.

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Inhibition of human natural killer cell activity by cereulide, an emetic toxin fromBacillus cereus

Cited by 93 publications

References 32 publications

Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains

Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains

Comparative Transcriptomic and Phenotypic Analysis of the Responses ofBacillus cereusto Various Disinfectant Treatments

Inhibition of Cereulide Toxin Synthesis by Emetic Bacillus cereus via Long-Chain Polyphosphates

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