Potato crop as a source of emetic bacillus cereus and cereulide-induced mammalian cell toxicity

Applied and Environmental Microbiology

Volumn 79, Issue 12, 2013, Pages 3534-3543

  Hoornstra, Douwe ^a   Andersson, Maria A ^a   Teplova, Vera V ^a,c   Mikkola, Raimo ^a   Uotila, Liisa M ^a   Andersson, Leif C ^b   Roivainen, Merja ^d   Gahmberg, Carl G ^a   Salkinoja Salonen, Mirja S ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c INSTITUTE OF THEORETICAL AND EXPERIMENTAL BIOPHYSICS   (Russian Federation)

^d NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL BIOMASS; EXTRACELLULAR SPACE; FOOD-BORNE ILLNESS; HUMAN PERIPHERAL BLOOD; INSULIN-PRODUCING CELLS; MAMMALIAN CELL TOXICITY; MURINE FIBROBLASTS; STARCH HYDROLYSIS;

BIOLOGICAL MEMBRANES; CELL CULTURE; CELLS; TISSUE;

BACILLUS CEREUS;

CEREULIDE; DEPSIPEPTIDE; EMETIC AGENT;

CROP PRODUCTION; DISEASE VECTOR; HYDROLYSIS; MEMBRANE; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; PATHOGEN; POTATO; STARCH; TOXICITY TEST;

ANIMAL; ARTICLE; BACILLUS CEREUS; CHEMISTRY; CYTOLOGY; DRUG EFFECT; EPITHELIUM CELL; GROWTH, DEVELOPMENT AND AGING; HUMAN; KERATINOCYTE; KIDNEY TUBULE; MALE; METABOLISM; MICROBIOLOGY; MITOCHONDRIAL MEMBRANE POTENTIAL; MONONUCLEAR CELL; PANCREAS ISLET BETA CELL; POTATO; SPERMATOZOON; SWINE; TIME; TOXICITY TESTING;

ANIMALS; BACILLUS CEREUS; DEPSIPEPTIDES; EMETICS; EPITHELIAL CELLS; HUMANS; INSULIN-SECRETING CELLS; KERATINOCYTES; KIDNEY TUBULES; LEUKOCYTES, MONONUCLEAR; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; SOLANUM TUBEROSUM; SPERMATOZOA; SWINE; TIME FACTORS; TOXICITY TESTS;

BACILLUS CEREUS; BACTERIA (MICROORGANISMS); MAMMALIA; MURINAE; PICEA; PICEA ABIES; SOLANUM TUBEROSUM; SUS;

EID: 84878657835     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00201-13     Document Type: Article

References (73)

1. Agata N, Ohta M, Mori M, Isobe M. 1995. A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus. FEMS Microbiol. Lett. 129: 17-20.
2. Andersson MA, Mikkola R, Helin J, Andersson MC, Salkinoja-Salonen M. 1998. A novel sensitive bioassay for detection of Bacillus cereus emetic toxin and related depsipeptide ionophores. Appl. Environ. Microbiol. 64: 1338-1343.
3. Shiota M, Saitou K, Matsusaka H, Agata N, Nakayama M, Kage M, Tatsumi S, Okamoto A, Yamaguchi S, Ohta M, Hata D. 2010. Rapid detoxification of cereulide in Bacillus cereus food poisoning. Pediatrics 125:e951- e955.
4. Jääskeläinen EL, Teplova V, Andersson MA, Andersson LC, Tammela P, Andersson MC, Pirhonen TI, Saris NEL, Vuorela P, Salkinoja-Salonen MS. 2003. In vitro assay for human toxicity of cereulide, the emetic mitochondrial toxin produced by food poisoning Bacillus cereus. Toxicol. In Vitro 17:737-744.
5. Mahler H, Pasi A, Kramer J, Schulte P, Scoging A, Baer W, Kraehenbuehl S. 1997. Fulminant liver failure in association with the emetic toxin of Bacillus cereus. N. Engl. J. Med. 336:1143-1148.
6. Shinagawa K, Konuma H, Sekita H, Sugii S. 1995. Emesis of rhesus monkeys induced by intragastric administration with the Hep-2 vacuolation factor (cereulide) produced by Bacillus cereus. FEMS Microbiol. Lett. 130:87-90.
7. Pósfay-Barbe KM, Schrenzel J, Frey J, Studer R, Korff C, Belli DC, Parvex P, Rimensberger PC, Schäppi MG. 2008. Food poisoning as a cause of acute liver failure. Pediatr. Infect. Dis. J. 27:846-847.
8. Yatsumoto Y, Hasegawa Y, Kobayashi H, Uchida Y. 2009. Acute encephalopathy caused by Bacillus cereus infection in a 5-year boy. J. Jpn. Pediatr. Soc. 113:75-78. (In Japanese, with abstract and tables in English.)
9. Naranjo M, Denayer S, Botteldoorn N, Delbrassinne L, Veys J, Waegenaere J, Sirtaine N, Driesen RB, Sipido KR, Mahillon J, Dierick K. 2011. Sudden death of a young adult associated with Bacillus cereus food poisoning. J. Clin. Microbiol. 49:4379-4381.
10. Dierick K, Van Coillie E, Swiecicka I, Meyfroidt G, Devlieger H, Meulemans A, Hoedemaekers G, Fourie L, Heyndrickx M, Mahillon J. 2005. Fatal family outbreak of Bacillus cereus-associated food poisoning. J. Clin. Microbiol. 43:4277- 4279.
11. Dirnhofer D, Sonnabend O, Sonnabend W. 1977. A fatal food poisoning by Bacillus cereus. Rechtsmedizin 80:139 -151. (In German.)
12. Takabe F, Oya M. 1976. An autopsy case of food poisoning associated with Bacillus cereus. Forensic Sci. 7:97-101.
13. Temper K. 1963. Exitus Letalis nach Lebensmittelvergiftung durch Bacillus cereus. Z. Gesamte Hyg. Grenzgebiete 9:481- 490.
14. Turnbull PCB, Nottingham JF, Ghosh AC. 1977. A severe necrotic enterotoxin produced by certain food, food poisoning, and other clinical isolates of Bacillus cereus. Br. J. Exp. Pathol. 58:273-280.
15. Turnbull PCB, Kramer JM, Jörgensen Gilbert KRJ, Melling J. 1979. Properties and production characteristics of vomiting, diarrhea, and necrotizing toxins of Bacillus cereus. Am. J. Clin. Nutr. 32:219 -228.
16. Turnbull PCB. 1976. Studies on the production of enterotoxins by Bacillus cereus. J. Clin. Pathol. 29:941-948.
17. Ceuppens S, Rajkovic A, Heyndrickx M, Tsilia V, Van de Wiele T, Boon N, Uyttendaele M. 2011. Regulation of toxin production by Bacillus cereus and its food safety implications. Crit. Rev. Microbiol. 37:188 -213.
18. Messelhäusser U, Kämpf P, Fricker M, Ehling-Schulz M, Zucker R, Wagner B, Busch U, Höller C. 2010. Prevalence of emetic Bacillus cereus in different ice creams in Bavaria. J. Food Prot. 73:395-399.
19. Hoton FM, Fornelos N, N=Guessan E, Hu X, Swiecicka I, Dierick K, Jääskeläinen E, Salkinoja-Salonen M, Mahillon J. 2009. Family portrait of Bacillus cereus and Bacillus weihenstephanensis cereulide-producing strains. Environ. Microbiol. Rep. 1:177-183.
20. Pirttijärvi TS, Andersson MA, Scoging AC, Salkinoja-Salonen MS. 1999. Evaluation of methods for recognizing strains of the Bacillus cereus group with food poisoning potential among industrial and environmental contaminants. Syst. Appl. Microbiol. 22:133-144.
21. Shaheen R, Andersson MA, Apetroaie C, Schulz A, Ehling-Schulz M, Ollilainen VM, Salkinoja-Salonen MS. 2006. Potential of selected infant food formulas for production of Bacillus cereus emetic toxin, cereulide. Int. J. Food Microbiol. 107:287-294.
22. Altayar M, Sutherland AD. 2006. Bacillus cereus is common in the environment but emetic toxin producing isolates are rare. J. Appl. Microbiol. 100:7-14.
23. Ankolekar C, Rahmati T, Labbe RG. 2009. Detection of toxigenic Bacillus cereus and Bacillus thuringiensis spores in U.S. rice. Int. J. Food Microbiol. 128:460-466.
24. Svensson B, Monthan A, Shaheen R, Andersson A, Salkinoja-Salonen M, Christiansson A. 2006. Occurrence of emetic toxin-producing Bacillus cereus in the dairy production chain. Int. Dairy J. 16:740 -749.
25. Swiecicka I, Mahillon J. 2006. Diversity of commensal Bacillus cereus sensu lato isolated from the common sow bug (Porcellio scaber, Isopoda). FEMS Microbiol. Ecol. 56:132-140.
26. Vassileva M, Torii K, Oshimoto M, Okamoto A, Agata N, Yamada K, Hasgawa T, Ohta M. 2007. A new phylogenetic cluster of cereulide producing Bacillus strains. J. Clin. Microbiol. 45:1274 -1277.
27. Garbeva P, van Overbeek LS, van Vuurde JWL, van Elsas JD. 2001. Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA-based PCR fragments. Microb. Ecol. 41:369 -383.
28. Melnick RL, Testen AL, Poleatewich AM, Backman PA, Bailey BA. 2012. Detection and expression of enterotoxin genes in endophytic strains of Bacillus cereus. Lett. Appl. Microbiol. 54:468-474.
29. Corratge-Faillie C, Jabnoune M, Zimmermann S, Very AA, Fizames C, Sentenac H. 2010. Potassium and sodium transport in non-animal cells: the Trk/Ktr/HKT transporter family. Cell. Mol. Life Sci. 67:2511-2532.
30. Leigh RA. 2001. Potassium homeostasis and membrane transport. J. Plant Nutr. Soil Sci. 164:193-198.
31. Rajkovic A, Uyttendaele M, Vermeulen A, Andjelkovic M, Fitz-James I, in't Veld P, Denon Q, Verhe R, Devebere J. 2008. Heat resistance of Bacillus cereus emetic toxin, cereulide. Lett. Appl. Microbiol. 46:536 -541.
32. Melling J, Capel BJ. 1978. Characteristics of Bacillus cereus emetic toxin. FEMS Microbiol. Lett. 4:133-135.
33. Mikkola R, Saris NE, Grigoriev PA, Andersson MA, Salkinoja-Salonen MS. 1999. Ionophoretic properties and mitochondrial effects of cereulide: the emetic toxin of Bacillus cereus. Eur. J. Biochem. 263:112-117.
34. Teplova VV, Mikkola R, Tonshin AA, Saris NE, Salkinoja-Salonen MS. 2006. The higher toxicity of cereulide relative to valinomycin is due to its higher affinity for potassium at physiological plasma concentration. Toxicol. Appl. Pharmacol. 210:39-46.
35. Makarasen A, Yoza K, Isobe M. 2009. Higher structure of cereulide, an emetic toxin from Bacillus cereus and special comparison with valinomycin, an antibiotic from Streptomyces fulvissimus. Chem. Asian J. 4:688- 698.
36. Ekman JV, Kruglov A, Andersson MA, Mikkola R, Raulio M, Salkinoja-Salonen MS. 2012. Cereulide produced by Bacillus cereus increases fitness of the producer organism in low potassium environment. Microbiology 158:1106 -1116.
37. Hallaksela AM, Väisänen O, Salkinoja-Salonen M. 1991. Identification of Bacillus species isolated from Picea abies by physiological tests, phage typing, and fatty acid analysis. Scand. J. Forest Res. 6:365-377.
38. Andersson MA, Jääskeläinen EL, Shaheen R, Pirhonen T, Wijnands LM, Salkinoja-Salonen MS. 2004. Sperm bioassay for rapid detection of cereulide producing Bacillus cereus in food and related environment. Int. J. Food Microbiol. 94:175-183.
39. Smibert RM, Krieg NR. 1994. Phenotypic characterization, p 630. In Gerhardt P, Murray RGE, Wood WA, Krieg NR (ed), Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC.40.
40. Rasimus S, Mikkola R, Andersson MA, Teplova VV, Venediktova N, Ek-Kommonen C, Salkinoja-Salonen M. 2012. Psychotolerant Paenibacillus tundrae from barley grains produces new cereulide-like depsipeptides, paenilide, and homopaenilide, highly toxic to mammalian cells. Appl. Environ. Microbiol. 78:3732-3743.
41. Echard G. 1975. Chromosomal banding patterns and karyotype evolution in three pig kidney cell strains. Chromosoma (Berl.) 45:138 -149.
42. Bøyum A. 1968. Isolation of leucocytes from human blood: further observations on methylcellulose, dextran, and Ficoll as erythrocyteaggregating agents. Scand. J. Clin. Lab. Invest. Suppl. 97:31-50.
43. Valmu L, Hilden TJ, van Willigen G, Gahmberg CG. 1999. Characterization of 2 (CD18) integrin phosphorylation in phorbol ester-activated T lymphocytes. Biochem. J. 339:119 -125.
44. Ihanus E, Uotila L, Toivanen A, Stefanidakis M, Bailly P, Cartron Gahmberg J-PCG. 2003. Characterization of ICAM-4 binding to the I domains of the CD11a/CD18 and CD11b/CD18 leukocyte integrins. Eur. J. Biochem. 270:1710 -1723.
45. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106:761-771.
46. Miyazaki J, Araki K, Yamato E, Ikegami H, Asano T, Shibasaki Y, Oka Y, Yamamura K. 1990. Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127:126 -132.
47. Hoornstra D, Andersson MA, Mikkola R, Salkinoja-Salonen MS. 2003. A new method for in vitro detection of microbially produced mitochondrial toxins. Toxicol. In Vitro 17:745-751.
48. Andersson MA, Hakulinen P, Honkalampi-Hämäläinen U, Hoornstra D, Lhuguenot JC, Mäki-Paakkanen J, Savolainen M, Severin I, Stammati AL, Turco L, Weber A, von Wright A, Zucco F, Salkinoja-Salonen M. 2007. Toxicological profile of cereulide, the Bacillus cereus emetic toxin, in functional assays with human, animal, and bacterial cells. Toxicon 49:351-367.
49. Kruglov AG, Andersson MA, Mikkola R, Roivainen M, Kredics L, Saris NEL, Salkinoja-Salonen MS. 2009. Novel mycotoxin from Acremonium exuviarum is a powerful inhibitor of the mitochondrial respiratory chain complex III. Chem. Res. Toxicol. 22:565-573.
50. Apetroaie C, Andersson MA, Spröer C, Tsitko I, Shaheen R, Jääskeläinen EL, Wijnands LM, Heikkilä R, Salkinoja-Salonen MS. 2005. Cereulide-producing strains of Bacillus cereus show diversity. Arch. Microbiol. 184:141-151.
51. Apetroaie-Constantin C, Shaheen R, Andrup L, Smidt L, Rita H, Salkinoja-Salonen MS. 2008. Environment driven cereulide production by emetic strains of Bacillus cereus. Int. J. Food Microbiol. 127:60-67.
52. Carlin F, Fricker M, Pielaat A, Heisterkamp S, Shaheen R, Salkinoja-Salonen M, Svensson B, Nguyen TH, Ehling-Schulz CM. 2006. Emetic toxin-producing strains of Bacillus cereus show distinct characteristics within the Bacillus cereus group. Int. J. Food Microbiol. 109:132-138.
53. Häggblom MM, Apetroaie C, Andersson MA, Salkinoja-Salonen MS. 2002. Quantitative analysis of cereulide, the emetic toxin of Bacillus cereus, produced under various conditions. Appl. Environ. Microbiol. 68:2479- 2483.
54. Shaheen R. 2009. Bacillus cereus spores and cereulide in food-borne illness. Ph.D thesis. University of Helsinki, Department of Applied Chemistry and Microbiology, Helsinki, Finland.
55. oC. EN-ISO standard 7932, 3rd ed. International Organisation for Standardization, Geneva, Switzerland.56.
56. Tallent SM, Rhodehamel J, Harmon SM, Bennett R. 2012. Bacillus cereus in Food and Drug Administration bacteriological analytical manual, 8th ed, revision A. AOAC International, Gaithersburg, MD. http://www.fda.gov/Food /ScienceResearch/LaboratoryMethods/BacteriologicalAnalyticalManualBA M/ucm070875.htm.
57. Essen R, de Ruyter C, de Wit M. 2000. Massive food poisoning in Kotterbos at Almere. Infect. Bull. 11:205-207. (In Dutch.)
58. Rajkovic A, Uyttendaele M, Courtens T, Heyndrickx M, Debevere J. 2006. Prevalence and characterization of Bacillus cereus in vacuum packed potato puree. Int. J. Food Sci. Technol. 41:878-884.
59. Saris NEL, Andersson MA, Mikkola M, Andersson LC, Teplova VV, Grigoriev PA, Salkinoja-Salonen MS. 2009. Microbial toxins affect on mitochondrial survival by increasing mitochondrial uptake of K_. Toxicol. Ind. Health 25:441- 446.
60. Ceccarini L, Masetti M, Cavalli A, Recanatini M. 2012. Ion conduction through the hERG potassium channel. PLoS One
61. Feske S, Skolnik EY, Prakriya M. 2012. Ion channels and transporters in lymphocyte function and immunity. Nat. Rev. Immunol. 12:532-547.
62. Petrilli V, Papin S, Dostert C, Mayor A, Martinon F, Tschopp J. 2007. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 14:1583-1589.
63. Qian J, Zhu L, Qiming L, Belevych N, Chen Q, Zhao F, Herness S, Quan N. 2012. Interleukin-1R3 mediates interleukin-1-induced potassium current increase through fast activation of Akt kinase. Proc. Natl. Acad. Sci. U. S. A. 109:12189 -12194.
64. Unwin RJ, Luft FC, Shirley DG. 2011. Pathophysiology and management of hypokalemia: a clinical perspective. Nat. Rev. Nephrol. 7:75- 84.
65. Jääskeläinen EL, Häggblom-Andersson MM, Vanne MA, Salkinoja-Salonen L. 2003. Potential of Bacillus cereus for producing an emetic toxin, cereulide, in bakery products: quantitative analysis by chemical and biological methods. J. Food Prot. 66:1047-1054.
66. Finlay WJJ, Logan NA, Sutherland AD. 1999. Semiautomated metabolic staining assay for Bacillus cereus emetic toxin. Appl. Environ. Microbiol. 65:1811-1812.
67. Agata N, Ohta M, Yokoyama K. 2002. Production of Bacillus cereus emetic toxin (cereulide) in various foods. Int. J. Food Microbiol. 73:23-25.
68. Pitchayawasin S, Isobe M, Kuse M, Franz T, Agata N, Ohta M. 2004. Molecular diversity of cereulide detected by means of nano-HPLC-ESIQ-TOF-MS. Int. J. Mass Spectrom. 235:123-129.
69. Cantley J, Grey ST, Maxwell PH, Withers DJ. 2010. The hypoxia response pathway and -cell function. Diabetes Obes. Metab. 2010(Suppl 2):159 -167.
70. Jitrapakdee S, Wutthisathapornchai A, Wallace JC, MacDonald MJ. 2010. Regulation of insulin secretion: role of mitochondrial signaling. Diabetologia 53:1019 -1032.
71. Virtanen SM, Roivainen M, Andersson MA, Ylipaasto P, Hoornstra D, Mikkola R, Salkinoja-Salonen MS. 2008. In vitro toxicity of cereulide on porcine pancreatic Langerhans islets. Toxicon 51:1029 -1037.
72. Virtanen SM, Takkinen H-M, Nevalainen J, Kronberg-Kippilä C, Salmenhaara M, Uusitalo L, Kenward MG, Erkkola M, Veijola R, Simell O, Ilonen J, Knip M. 2011. Early introduction of root vegetables in infant associated with advanced -cell autoimmunity in young children with human leukocyte antigen-conferred susceptibility to type 1 diabetes. Diabetic Med. 28:965-971.
73. Rajkovic A, Uyttendaele M, Mbregt S-A, Jääskeläinen E, Salkinoja-Salonen M, Debevere J. 2006. Influence of type of food on the kinetics and overall production of Bacillus cereus emetic toxin. J. Food Prot. 69:847-852.