The pore-forming haemolysins of Bacillus cereus: A review

Toxins

Volumn 5, Issue 6, 2013, Pages 7492-7502

  Ramarao, Nalini ^a   Sanchis, Vincent ^a  

^a AGROPARISTECH   (France)

Author keywords

B. cereus; Cereolysin O; Cytotoxin K; Haemolysin II; Haemolysin III; Haemolysins; PlcR

Indexed keywords

ALPHA TOXIN; BETA TOXIN; CEREOLYSIN O; CLOSTRIDIUM PERFRINGENS TOXIN; CYTOLYSIN; ENDOTOXIN; HAEMOLYSIN II; HAEMOLYSIN III; HAEMOLYSIN IV; HEMOLYSIN; INTERMEDILYSIN; LISTERIOLYSIN O; UNCLASSIFIED DRUG; BACTERIAL TOXIN;

ALO GENE; BACILLUS CEREUS; BACTERIAL GENOME; BACTERIAL VIRULENCE; CDC GENE; CLO GENE; CLOSTRIDIUM PERFRINGENS; GENE CONTROL; GENE FUNCTION; GENE IDENTIFICATION; GENOME ANALYSIS; HEMOLYSIS; ILY GENE; LISTERIA MONOCYTOGENES; NONHUMAN; OLIGOMERIZATION; PFO GENE; REVIEW; SPECIES COMPARISON; SPOROGENESIS; STAPHYLOCOCCUS AUREUS; STRUCTURAL GENOMICS; TLO GENE; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION;

BACILLUS CEREUS; CLOSTRIDIUM PERFRINGENS; LISTERIA MONOCYTOGENES; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

BACILLUS CEREUS; BACTERIAL TOXINS; HEMOLYSIN PROTEINS; PROTEIN CONFORMATION;

EID: 84891611455     PISSN: 20726651     EISSN: None     Source Type: Journal    
DOI: 10.3390/toxins5061119     Document Type: Review

References (103)

1. Guinebretière, M.H.; Thompson, F.L.; Sorokin, A.; Normand, P.; Dawyndt, P.; Ehling-Schulz, M.; Svensson, B.; Sanchis, V.; Nguyen-The, C.; Heyndrickx, M.; et al. Ecological diversification in the Bacillus cereus Group. Environ. Microbiol. 2008, 10, 851-865.
2. Ivanova, N.; Sorokin, A.; Anderson, I.; Galleron, N.; Candelon, B.; Kapatral, V.; Bhattacharyya, A.; Reznik, G.; Mikhailova, N.; Lapidus, A.; et al. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 2003, 423, 87-91.
3. Rejasse, A.; Gilois, N.; Barbosa, I.; Huillet, E.; Bevilacqua, C.; Tran, S.; Ramarao, N.; Stenfors, A.L.P.; Sanchis, V. Temperature-dependent production of various PlcR-controlled virulence factors in Bacillus weihenstephanensis strain KBAB4. Appl. Environ. Microbiol. 2012, 78, 2553-2561.
4. Kolstø, A.B.; Tourasse, N.J.; Økstad, O.A. What sets Bacillus anthracis apart from other Bacillus species? Annu. Rev. Microbiol. 2009, 63, 451-476.
5. Anonymous. The community summary report on food-borne outbreaks in the European Union in 2007. EFSA J. 2009, doi:10.2903/j.efsa.2009.271r.
6. Hernaiz, C.; Picardo, A.; Alos, J.I.; Gomez-Garces, J.L. Nosocomial bacteremia and catheter infection by Bacillus cereus in an immunocompetent patient. Clin. Microbiol. Infect. 2003, 9, 973-975.
7. Kotiranta, A.; Lounatmaa, K.; Haapasalo, M. Epidemiology and pathogenesis of Bacillus cereus infections. Microbes Infect. 2000, 2, 189-198.
8. Lund, T.; de Buyser, M.L.; Granum, P.E. A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Mol. Microbiol. 2000, 38, 254-261.
9. Naranjo, M.; Denayer, S.; Botteldoorn, N.; Delbrassinne, L.; Veys, J.; Waegenaere, J.; Sirtaine, N.; Driesen, R.B.; Sipido, K.R.; Mahillon, J.; et al. Sudden death of a young adult associated with Bacillus cereus food poisoning. J. Clin. Microbiol. 2011, 49, 4379-4381.
10. Mahler, H.; Pasi, A.; Kramer, J.M.; Schulte, P.; Scoging, A.C.; Bär, W.; Krähenbühl, S. Fulminant liver failure in association with the emetic toxin of Bacillus cereus. N. Engl. J. Med. 1997, 336, 1142-1148.
11. Dierick, K.; van Coillie, E.; Swiecicka, I.; Meyfroidt, G.; Devlieger, H.; Meulemans, A.; Hoedemaekers, G.; Fourie, L.; Heyndrickx, M.; Mahillon, J. Fatal family outbreak of Bacillus cereus-associated food poisoning. J. Clin. Microbiol. 2005, 43, 4277-4279.
12. Ehling-Schulz, M.; Fricker, M.; Scherer, S. Bacillus cereus, the causative agent of an emetic type of food-borne illness. Mol. Nutr. Food Res. 2004, 48, 479-487.
13. Stenfors, A.L.P.; Fagerlund, A.; Granum, P.E. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 2008, 32, 579-606.
14. Ramarao, N. Bacillus cereus: Caractéristiques et pathogénicité. EMC Biol. Méd. 2012, 7, 1-11.
15. Cadot, C.; Tran, S.L.; Vignaud, M.L.; de Buyser, M.L.; Kolstø, A.B.; Brisabois, A.; Nguyen-Thé, C.; Lereclus, D.; Guinebretière, M.H.; Ramarao, N. InhA1, NprA and HlyII as candidates to differentiate pathogenic from non-pathogenic Bacillus cereus strains. J. Clin. Microbiol. 2010, 48, 1358-1365.
16. Bottone, E.J. Bacillus cereus, a volatile human pathogen. Clin. Microbiol. Rev. 2010, 23, 382-398.
17. Callegan, M.C.; Kane, S.T.; Cochran, D.C.; Novosad, B.; Gilmore, M.S.; Gominet, M.; Lereclus, D. Bacillus endophthalmitis: Roles of bacterial toxins and motility during infection. Invest. Ophthalmol. Vis. Sci. 2005, 46, 3233-3238.
18. Gray, J.; George, R.H.; Durbin, G.M.; Ewer, A.K.; Hocking, M.D.; Morgan, M.E. An outbreak of Bacillus cereus respiratory tract infections on a neonatal unit due to contaminated ventilator circuits. J. Hosp. Infect. 1999, 41, 19-22.
19. Miller, J.M.; Hair, J.G.; Hebert, M.; Hebert, L.; Roberts, F.J., Jr; Weyant, R.S. Fulminating bacteremia and pneumonia due to Bacillus cereus. J. Clin. Microbiol. 1997, 35, 504-507.
20. Bouillaut, L.; Ramarao, N.; Buisson, C.; Gilois, N.; Gohar, M.; Lereclus, D.; Nielsen-Leroux, C. FlhA influences Bacillus thuringiensis PlcR-regulated gene transcription, protein production, and virulence. Appl. Environ. Microbiol. 2005, 71, 8903-8910.
21. Tran, S.L.; Guillemet, E.; Gohar, M.; Lereclus, D.; Ramarao, N. CwpFM (EntFM) is a Bacillus cereus potential cell wall peptidase implicated in adhesion, biofilm formation and virulence. J. Bacteriol. 2010, 192, 2638-2642.
22. Gilois, N.; Ramarao, N.; Bouillaut, L.; Perchat, S.; Aymerich, S.; Nielsen-Leroux, C.; Lereclus, D.; Gohar M. Growth-related variations in the Bacillus cereus secretome. Proteomics 2007, 7, 1719-1728.
23. Brillard, J.; Susanna, K.; Michaud, C.; Dargaignaratz, C.; Gohar, M.; Nielsen-Leroux, C.; Ramarao, N.; Kolstø, A.B.; Nguyenthe, C.; Lereclus, D.; Broussolle, V. The YvfTU two-component system is involved in plcR expression in Bacillus cereus. BMC Microbiol. 2008, doi:10.1186/1471-2180-8-183.
24. Ramarao, N.; Lereclus, D. Adhesion and cytotoxicity of Bacillus cereus and Bacillus thuringiensis to epithelial cells are FlhA and PlcR dependent, respectively. Microbes Infect. 2006, 8, 1483-1491.
25. Auger, S.; Ramarao, N.; Faille, C.; Fouet, A.; Aymerich, S.; Gohar, M. Biofilm formation and cell surface properties among pathogenic and non pathogenic strains of the Bacillus cereus group. Appl. Environ. Microbiol. 2009, 75, 6616-6618.
26. Guillemet, E.; Cadot, C.; Tran, S.L.; Guinebretière, M.H.; Lereclus, D.; Ramarao, N. The InhA metalloproteases of Bacillus cereus contribute concomitantly to virulence. J. Bacteriol. 2010, 192, 286-294.
27. Lindbäck, T.; Okstad, O.A.; Rishovd, A.L.; Kolstø, A.B. Insertional inactivation of hblC encoding the L2 component of Bacillus cereus ATCC 14579 haemolysin BL strongly reduces enterotoxigenic activity, but not the haemolytic activity against human erythrocytes. Microbiology 1999, 145, 3139-3146.
28. Fagerlund, A.; Lindbäck, T.; Storset, A.K.; Granum, P.E.; Hardy, S.P. Bacillus cereus Nhe is a pore forming toxin with structural and functional properties similar to ClyA (HlyE, SheA) family of haemolysins, able to induce osmotic lysis in epithelia. Microbiology 2008, 154, 693-704.
29. Senesi, S.; Ghelardi, E. Production, secretion and biological activity of Bacillus cereus enterotoxins. Toxins 2010, 2, 1690-1703.
30. Gilmore, M.S.; Cruz-Rodz, A.L.; Leimeister-Wächter, M.; Kreft, J.; Goebel, W. A Bacillus cereus cytolitic determinant, cereolysin AB, which comprises the phospholipase C and sphingomyelinase genes: Nucleotide sequence and genetic linkage. J. Bacteriol. 1989, 171, 744-753.
31. Vilas-Boas, G.; Sanchis, V.; Lereclus, D.; Lemos, M.V.; Bourguet, D. Genetic differentiation between sympatric populations of Bacillus cereus and Bacillus thuringiensis. Appl. Environ. Microbiol. 2002, 68, 1414-1424.
32. Bernheimer, A.W.; Grushoff, P. Cereolysin: Production, purification and partial characterization. J. Gen. Microbiol. 1967, 46, 143-150.
33. Shannon, J.G.; Ross, C.L.; Koehler, T.M.; Rest, R.F. Characterization of anthrolysin O, the Bacillus anthracis cholesterol-dependent cytolysin. Infect. Immun. 2003, 71, 3183-3189.
34. Johnson, M.K.; Geoffroy, C.; Alouf, J.E. Binding of cholesterol by sulfhydryl-activated cytolysins. Infect. Immun. 1980, 27, 97-101.
35. Bernheimer, A.W.; Grushoff, P. Extracellular hemolysins of aerobic sporogenic Bacilli. J. Bacteriol.1967, 93, 1541-1543.
36. Alouf, J.E.; Billington, S.J.; Jost, B.H. Repertoire and General Features of the Family of Cholesterol-Dependent Cytolysins. In The Comprehensive Sourcebook of Bacterial Protein Toxins, 3rd ed.; Alouf, J.E., Popoff, M.R., Eds.; Academic Press: London, UK, 2005; pp. 643-658.
37. Palmer, M. The family of thiol-activated, cholesterol-binding cytolysins. Toxicon 2001, 39, 1681-1689.
38. Shatursky, O.; Heuck, A.P.; Shepard, L.A.; Rossjohn, J.; Parker, M.W.; Johnson, A.E.; Tweten, R.K. The mechanism of membrane insertion for a cholesterol-dependent cytolysin: A novel paradigm for pore-forming toxins. Cell 1999, 99, 293-299.
39. Jacobs, T.; Cima-Cabal, M.D.; Darji, A.; Méndez, F.J.; Vázquez, F.; Jacobs, A.A.; Shimada, Y.; Ohno-Iwashita, Y.; Weiss, S.; de los Toyos, J.R. The conserved undecapeptide shared by thiol-activated cytolysins is involved in membrane binding. FEBS Lett. 1999, 459, 463-466.
40. Rossjohn, J.; Feil, S.C.; McKinstry, W.J.; Tweten, R.K.; Parker, M.W. Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell 1997, 89, 685-692.
41. Polekhina, G.; Giddings, K.S.; Tweten, R.K.; Parker, M.W. Insights into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin. Proc. Natl. Acad. Sci. USA 2005, 102, 600-605.
42. Bourdeau, R.W.; Malito, E.; Chenal, A.; Bishop, B.L.; Musch, M.W.; Villereal, M.L.; Chang, E.B.; Mosser, E.M.; Rest, R.F.; Tang, W.J. Cellular functions and X-ray structure of anthrolysin O, a cholesterol-dependent cytolysin secreted by Bacillus anthracis. J. Biol. Chem. 2009, 284, 14645-14656
43. Soltani, C.E.; Hotze, E.M.; Johnson, A.E.; Tweten, R.K. Specific protein-membrane contacts are required for prepore and pore assembly by a cholesterol-dependent cytolysin. J. Biol. Chem. 2007, 282, 15709-15716.
44. Dang, T.X.; Hotze, E.M.; Rouiller, I.; Tweten, R.K.; Wilson-Kubalek, E.M. Prepore to pore transition of a cholesterol-dependent cytolysin visualized by electron microscopy. J. Struct. Biol. 2005, 150, 100-108.
45. Vazquez-Boland, J.A.; Kuhn, M.; Berche, P.; Chakraborty, T.; Domínguez-Bernal, G.; Goebel, W.; González-Zorn, B.; Wehland, J.; Kreft, J. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 2001. 14, 584-640.
46. Mosser, E.M.; Rest, R.F. The Bacillus anthracis cholesterol-dependent cytolysin, Anthrolysin O, kills human neutrophils, monocytes and macrophages. BMC Microbiol. 2006, doi:10.1186/1471-2180-6-56.
47. Beecher, D.J.; Olsen, T.W.; Somers, E.B.; Wong, A.C. Evidence for contribution of tripartite hemolysin BL, phosphatidylcholine-preferring phospholipase C, and collagenase to virulence of Bacillus cereus endophthalmitis. Infect. Immun. 2000, 68, 5269-5276.
48. Agaisse, H.; Gominet, M.; Okstad, O.A.; Kolstø, A.B.; Lereclus, D. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol. Microbiol. 1999, 32, 1043-1053.
49. Gohar, M.; Økstad, O.A.; Gilois, N.; Sanchis, V.; Kolstø, A.B.; Lereclus, D. Two-dimensional electrophoresis analysis of the extracellular proteome of Bacillus cereus reveals the importance of the PlcR regulon. Proteomics 2002, 2, 784-791.
50. Lereclus, D.; Agaisse, H.; Gominet, M.; Salamitou, S.; Sanchis, V. Identification of a Bacillus thuringiensis gene that positively regulates transcription of the phosphatidylinositol-specific phospholipase C gene at the onset of the stationary phase. J. Bacteriol. 1996, 178, 2749-2756.
51. Gominet, M.; Slamti, L.; Gilois, N.; Rose, M.; Lereclus, D. Oligopeptide permease is required for expression of the Bacillus thuringiensis plcR regulon and for virulence. Mol. Microbiol. 2001, 40, 963-975.
52. Bouillaut, L.; Perchat, S.; Arold, S.; Zorrilla, S.; Slamti, L.; Henry, C.; Gohar, M.; Declerck, N.; Lereclus, D. Molecular basis for group-specific activation of the virulence regulator PlcR by PapR heptapeptides. Nucleic Acids Res. 2008, 36, 3791-3801.
53. Lereclus, D.; Agaisse, H. Toxin and Virulence Gene Expression in Bacillus thuringiensis. In Entomopathogenic Bacteria: From Laboratory to Field Application; Charles, J.F., Delécluse, A., Nielsen-Leroux, C., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2000; pp. 127-142.
54. Slamti, L.; Lereclus, D. A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J. 2002, 21, 4550-4559.
55. Gohar, M.; Faegri, K.; Perchat, S.; Ravnum, S.; Økstad, O.A.; Gominet, M.; Kolstø, A.B.; Lereclus, D. The PlcR virulence regulon of Bacillus cereus. PLoS One 2008, 3, e2793.
56. Coolbaugh, J.C.; Williams, R.P. Production and characterization of two hemolysins of Bacillus cereus. Can. J. Microbiol. 1978, 24, 1289-1295.
57. Sinev, M.A.; Budarina, Z.I.; Gavrilenko, I.V.; Tomashevskiǐ, A.I.; Kuzmin, N.P. Evidence of the existence of hemolysin II from Bacillus cereus: Cloning the genetic determinant of hemolysin II. Mol. Biol. 1993, 27, 1218-1229.
58. Baida, G.; Budarina, Z.I.; Kuzmin, N.P.; Solonin, A.S. Complete nucleotide sequence and molecular characterization of hemolysin II gene from Bacillus cereus. FEMS Microbiol. Lett. 1999, 180, 7-14.
59. Andreeva, Z.; Nesterenko, V.F.; Yurkov, I.S.; Budarina, Z.I.; Sineva, E.V.; Solonin, A.S. Purification and cytotoxic properties of Bacillus cereus hemolysin II. Prot. Express. Purif. 2006, 47, 186-193.
60. Andreeva, Z.I.; Nesterenko, V.F.; Fomkina, M.G.; Ternovsky, V.I.; Suzina, N.E.; Bakulina, A.Y.; Solonin, A.S.; Sineva, E.V. The properties of Bacillus cereus hemolysin II pores depend on environmental conditions. Biochem. Biophys. Acta 2007, 1768, 253-263.
61. Andreeva-Kovalevskaya, Z.I.; Solonin, A.S.; Sineva, E.V.; Ternovsky, V.I. Pore-forming proteins and adaptation of living organisms to environmental conditions. Biochemistry 2008, 73, 1473-1492.
62. Miles, G.; Bayley, H.; Cheley, S. Properties of Bacillus cereus hemolysin II: A heptameric transmembrane pore. Protein Sci. 2006, 11, 1813-1824.
63. Tran, S.L.; Guillemet, E.; Ngo-Camus, M.; Clybouw, C.; Puhar, A.; Moris, A.; Gohar, M.; Lereclus, D.; Ramarao, N. Hemolysin II is a Bacillus cereus virulence factor that induces apoptosis of macrophages. Cell. Microbiol. 2011, 13, 92-108.
64. Tran, S.L.; Puhar, A.; Ngo-Camus, M.; Ramarao, N. Trypan blue dye enters viable cells incubated with the pore-forming toxin HlyII of Bacillus cereus. PLoS One 2011, 6, e22876.
65. Valeva, A.; Hellmann, N.; Walev, I.; Strand, D.; Plate, M.; Boukhallouk, F.; Brack, A.; Hanada, K.; Decker, H.; Bhakdi, S. Evidence that clustered phosphocholine head groups serve as sites for binding and assembly of an oligomeric protein pore. J. Biol. Chem. 2006, 281, 26014-26021.
66. Liang, X.; Ji, Y. Involvment of alpha5beta1 integrin and TNF alpha in Staphylococcus aureus alpha toxin induced death of epithelial cells. Cell. Microbiol. 2007, 9, 1809-1821.
67. Nagahama, M.; Hayashhi, S.; Morimitsu, S.; Sakurai, J. Biological activities and pore formation of Clostridium perfringens beta toxin in HL 60 cells. J. Biol. Chem. 2003, 278, 36934-36941.
68. Granum, P.E. Clostridium perfringens toxins involved in food poisoning. Int. J. Food. Microbiol. 1990, 10, 101-111.
69. Clair, G.; Roussi, S.; Armengaud, J.; Duport, C. Expanding the known repertoire of virulence factors produced by Bacillus cereus through early secretome profiling in three redox conditions. Mol. Cell. Proteomics 2010, 9, 1486-1498.
70. Hernandez, E.; Ramisse, F.; Ducoureau, J.P.; Cruel, T.; Cavallo, J.D. Bacillus thuringiensis subsp. konkukian (serotype H34) superinfection: case report and experimental evidence of pathogenicity in immunosuppressed mice. J. Clin. Microbiol. 1998, 36, 2138-2139.
71. Ramarao, N.; Lereclus, D. The InhA1 metalloprotease allows spores of the B. cereus group to escape macrophages. Cell. Microbiol. 2005, 7, 1357-1364.
72. Sineva, E.; Andreeva-Kovalevskaya, Z.I.; Shadrin, A.M.; Gerasimov, Y.L.; Ternovsky, V.I.; Teplova, V.V.; Yurkova, T.V.; Solonin, A.S. Expression of Bacillus cereus hemolysin II in Bacillus subtilis renders the bacteria pathogenic for the crustacean Daphnia magna. FEMS Microbiol. Lett. 2009, 299, 110-119.
73. Budarina, Z.I.; Sinev, M.A.; Mayorov, S.G.; Tomashevski, A.Y.; Shmelev, I.V.; Kuzmin, N.P. Hemolysin II is more characteristic of Bacillus thuringiensis than Bacillus cereus. Arch. Microbiol. 1994, 161, 252-257.
74. Budarina, Z.I.; Nikitin, D.V.; Zenkin, N.; Zakharova, M.; Semenova, E.; Shlyapnikov, M.G.; Rodikova, E.A.; Masyukova, S.; Ogarkov, O.; Baida, G.E.; et al. A new Bacillus cereus DNA-binding protein, HlyIIR, negatively regulates expression of B. cereus haemolysin II. Microbiology 2004, 150, 3691-3701.
75. Guillemet, E.; Tran, S.L.; Cadot, C.; Rognan, D.; Lereclus, D.; Ramarao, N. Glucose 6P binds and activates HlyIIR to repress Bacillus cereus haemolysin hlyII gene expression. PLoS One 2013, 8, e55085.
76. Sineva, E.; Shadrin, A.; Rodikova, E.A.; Andreeva-Kovalevskaya, Z.I.; Protsenko, A.S.; Mayorov, S.G.; Galaktionova, D.Y.; Magelky, E.; Solonin, A.S. Iron regulates expression of Bacillus cereus hemolysin II via global regulator Fur. J. Bacteriol. 2012, 194, 3327-3335.
77. Tran, S.; Guillemet, E.; Lereclus, D.; Ramarao, N. Iron regulates Bacillus thuringiensis haemolysin hlyII gene expression during insect infection. J. Invert. Pathol. 2013, 113, 205-208.
78. Rodikova, E.A.; Kovalevskiy, O.V.; Mayorov, S.G.; Budarina, Z.I.; Marchenkov, V.V.; Melnik, B.S.; Leech, A.P.; Nikitin, D.V.; Shlyapnikov, M.G.; Solonin, A.S. Two HlyIIR dimers bind to a long perfect inverted repeat in the operator of the hemolysin II gene from Bacillus cereus. FEBS Lett. 2007, 581, 1190-1196.
79. Kovalevskiy, O.V.; Lebedev, A.A.; Surin, A.K.; Solonin, A.S.; Antson, A.A. Crystal structure of Bacillus cereus HlyIIR, a transcriptional regulator of the gene for pore-forming toxin hemolysin II. J. Mol. Biol. 2007, 365, 825-834.
80. Deutscher, J. The mechanisms of carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 2008, 11, 87-93.
81. Harvie, D.R.; Vílchez, S.; Steggles, J.R.; Ellar, D.J. Bacillus cereus Fur regulates iron metabolism and is required for full virulence. Microbiology 2005, 151, 569-577.
82. Ratledge, C.; Dover, L.G. Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. 2000, 54, 881-941.
83. Weinberg, E.D. Iron availability and infection. Biochim. Biophys. Acta 2009, 1790, 600-605.
84. Baida, G.E.; Kuzmin, N.P. Cloning and primary structure of a new hemolysin gene from Bacillus cereus. Biochim. Biophys. Acta 1995, 1264, 151-154.
85. Hofmann, K.; Stoffel, W. TMbase-A database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 1993, 374, 166.
86. Baida, G.E.; Kuzmin, N.P. Mechanism of action of hemolysin III from Bacillus cereus. Biochim. Biophys. Acta 1996, 1284, 122-124.
87. Beecher, D.J.; Wong, A.C. Cooperative, synergistic and antagonistic haemolytic interactions between haemolysin BL, phosphatidylcholine phospholipase C and sphingomyelinase from Bacillus cereus. Microbiology 2000, 146, 3033-3039.
88. Guinebretiere, M.H.; Auger, S.; Galleron, N.; Contzen, M.; de Sarrau, B.; Debuyser, M.L.; Lamberet, G.; Fagerlund, A.; Granum, P.E.; Lereclus, D.; et al. Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus group occasionally associated with food poisoning. Int. J. Syst. Evol. Microbiol. 2013, 63, 31-40.
89. Song, L.H.; Hobaugh, M.R.; Shustak, C.; Cheley, S.; Bayley, H.; Gouaux, J.E. Structure of staphylococcal alpha hemolysin, a heptameric transmembrane pore. Science 1996, 274, 1859-1866.
90. Menestrina, G.; Serra, M.D.; Prevost, G. Mode of action of beta-barrel pore-forming toxins of the staphylococcal alpha-hemolysin family. Toxicon 2001, 39, 1661-1672.
91. Fagerlund, A.; Ween, O.; Lund, T.; Hardy, S.P.; Granum, P.E. Genetic and functional analysis of the cytK family genes in Bacillus cereus. Microbiology 2004, 150, 2689-2697.
92. Guinebretiere, M.H.; Fagerlund, A.; Granum, P.E.; Nguyen-The, C. Rapid discrimination of cytK-1 and cytK-2 genes in Bacillus cereus strains by a novel duplex PCR system. FEMS Microbiol. Lett. 2006, 259, 74-80.
93. Fagerlund, A.; Lindback, T.; Granum, P.E. Bacillus cereus cytotoxins Hbl, Nhe and CytK are secreted via the Sec translocation pathway. BMC Microbiol. 2010, doi:10.1186/1471-2180-10-304.
94. Hardy, S.P.; Lund, T.; Granum, P.E. CytK toxin of Bacillus cereus forms pores in planar lipid bilayers and is cytotoxic to intestinal epithelia. FEMS Microbiol. Lett. 2001, 197, 47-51.
95. Ceuppens, S.; Rajkovic, A.; Heyndrickx, M.; Tsilia, V.; van de Wiele, T.; Boon, N.; Uyttendaele, M. Regulation of toxin production by Bacillus cereus and its food safety implications. Crit. Rev. Microbiol. 2011, 37, 188-213.
96. Kamar, R.; Gohar, M.; Jéhanno, I.; Réjasse, A.; Kallassy, M.; Lereclus, D.; Sanchis, V.; Ramarao, N. Pathogenic potential of B. cereus strains as revealed by phenotypic analysis. J. Clin. Microbiol. 2013, 51, 320-323.
97. Guinebretière, M.H.; Broussolle, V.; Nguyen-The, C. Enterotoxigenic profiles of food-poisoning and food-borne Bacillus cereus strains. J. Clin. Microbiol. 2002. 40, 3053-3056.
98. Wijnands, L.M.; Dufrenne, J.B.; Rombouts, F.M.; Veld, P.H.; van Leusden, F.M. Prevalence of potentially pathogenic Bacillus cereus in food commodities in The Netherlands. J. Food Prot. 2006, 69, 2587-2594.
99. Ngamwongsatit, P.; Buasri, W.; Pianariyanon, P.; Pulsrikarn, C.; Ohba, M.; Assavanig, A.; Panbangred, W. Broad distribution of enterotoxin genes (hblCDA, nheABC, cytK, and entFM) among Bacillus thuringiensis and Bacillus cereus as shown by novel primers. Int. J. Food Microbiol. 2008, 121, 352-356.
100. Guinebretiere, M.H.; Velge, P.; Couvert, O.; Carlin, F.; Debuyser, M.L.; Nguyen-The, C. Ability of Bacillus cereus group strains to cause food poisoning varies according to phylogenetic affiliation (groups I to VII) rather than species affiliation. J. Clin. Microbiol. 2010, 48, 3388-3391.
101. Brillard, J.; Lereclus, D. Comparison of cytotoxin cytK promoters from Bacillus cereus strain ATCC 14579 and from a B. cereus food-poisoning strain. Microbiology 2004, 150, 2699-2705.
102. Fagerlund, A.; Brillard, J.; Fürst, R.; Guinebretière, M.H.; Granum, P.E. Toxin production in a rare and genetically remote cluster of strains of the Bacillus cereus group. BMC Microbiol. 2007, doi:10.1186/1471-2180-7-43.
103. Ceuppens, S.; Timmery, S.; Mahillon, J.; Uyttendaele, M.; Boon, N. Small Bacillus cereus ATCC 14579 subpopulations are responsible for cytotoxin K production. J. Appl. Microbiol. 2013, 114, 899-906.