Cereulide and valinomycin, two important natural dodecadepsipeptides with ionophoretic activities

• Autorzy: Kroten M A , Bartoszewicz M. , Swiecicka I.
• Języki publikacji: EN

Abstrakty

EN

Cereulide produced by Bacillus cereus sensu stricto and valinomycin synthesized mainly by Streptomyces spp. are natural dodecadepsipeptide ionophores that act as potassium transporters. Moreover, they comprise three repetitions of similar tetrapeptide motifs synthesized by non-ribosomal peptide synthesis complexes. Resemblances in their structure find their reflections in the same way of action. The toxicity of valinomycin and cereulide is an effect of the disturbance of ionic equilibrium and transmembrane potential that may influence the whole organism and then cause fatal consequences. The vim and ces operons encoding valinomycin and cereulide are both composed of two large, similar synthetase genes, one thioestrase gene and four other ORFs with unknown activities. In spite of the characterization of valinomycin and cereulide, genetic determinants encoding their biosynthesis have not yet been clarified.

Słowa kluczowe

EN

cereulide; valinomycin; Bacillus cereus; ionophoretic activity; Streptomyces; natural dodecadepsipeptide; potassium transporter; toxicity; genetic determinant

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2010
• Tom: 59
• Numer: 1
• Opis fizyczny: p.3-10,fig.,ref.

Twórcy

autor

Kroten M A

• University of Bialystok, Swierkowa 20B, 15-950 Bialystok, Poland

autor

Bartoszewicz M.

autor

Swiecicka I.

Bibliografia

• Agata N., M. Ohta, M. Mori and M. Isobe. 1995. A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus.FEMS Microbiol. Lett. 129: 17-20.
• Agata N., M. Mori, M. Ohta, S. Suwan, L Ohtani and M. Isobe. 1994. A novel dodecadepsipeptide, cereulide, isolated from Bacillus cereus causes vacuole formation in Hep-2 cells. FEMS Microbiol. Lett. 121: 31-34.
• Andersson M.A., P. Hakulinen, U. Honkalampi-Hämäläinen, D. Hoornstra, J.-C. Lhuguenot, J. Mäki-Paakkanen, M. Savo-lainen, I. Severin, A.-L. Stammati, L. Turco and others. 2007. Toxicological profile of cereulide, the Bacillus cereus emetic toxin, in functional assays with human, animal and bacterial cells. Toxicon 49: 351-367.
• Bartoszewicz M., I. Święcicka, and J. Buczek. 2006. Cereulide and enterotoxins of Bacillus cereus sensu lato. Med. Weter. 62: 28-31.
• Bartoszewicz M., B.M. Hansen and I. Święcicka. 2008. The members of the Bacillus cereus group are commonly present contaminants of fresh and heat-treated milk. Food Microbiol. 25: 588-596.
• Beart J. 2006. DDT and human health. Sei, Total Environ. 355: 78-89.
• Bethal V. 2006. Mode of action of microbial bioactive metabolites. Folia Microbiol. 51: 359-369.
• Booth I. 1988. Bacterial transport energetics and mechanisms, p. 377-428. In: Anthony C. (ed.), Bacterial energy transduction. Academic Press, London, United Kingdom.
• Briley R.T., J.H. Teel and J.P. Fowler. 2001. Nontypical Bacillus cereus outbreak in a child care center. J. Environ. Health 63: 9-11.
• Brockmann H. and G. Schmidt-Kastner. 1955. Valinomycin I, XXVII. Mitteil, über Antibiotica aus Actinomyceten. Chem. Ber. 88: 57-61.
• Cheng Y.-Q. 2006. Deciphering the biosynthetic codes for the potent anti-SARS-CoV cyclodepsipeptide valinomycin in Streptomyces tsusimaensis ATCC 15141. Chem. Bio. Chem. 7: 471-477.
• Dierick K., E. Van Coillie, I. Święcicka, G, Meyfroidt, H. Devlieger, A. Meulemans, G. Hoedemaekers, L. Fourie, M. Heyndrickx and J. Mahillon. 2005. Fatal family outbreak of Bacillus cereus-associated food poisoning. J. Clin. Microbiol. 43: 4277-4279.
• Drobniewski F. 1993. Bacillus cereus and relatives. Clin. Microbiol. Rev. 6: 324-338.
• Duax W.L., J.F. Griffin, D.A. Langs, GD. Smith, P. Grochulski, V. Pletnev and V. Ivanov. 1996. Molecular structure and mechanisms of action of cyclic and linear ion transport antibiotics. Biopolymers 40: 141-155.
• Ehling-Schulz M., M. Fricker and S. Scherer. 2004a. Bacillus cereus, the causative agent of an emetic type food-borne illness. Mol. Nutr. Food Res. 48: 479-187.
• Ehling-Schulz M., M. Fricker and S. Scherer. 2004b. Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. FEMS Microbiol. Lett. 232: 189-195.
• Ehling-Schulz M., B. Svensson, M.-H. Guinebretiere, T. Lindback, M. Andersson, A. Schulz, M. Fricker, A. Christiansson, P.E. Granum, E. Martlbauer and others. 2005. Emetic toxin formation is restricted to a single evolutionary lineage of closely related strains. Microbiology 151: 183-197.
• Ehling-Schulz M., M. Fricker, H. Grallert, P. Rieck, M. Wagner and S. Scherer. 2006. Cereulide synthetase gene cluster from emetic Bacillus cereus: Structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXOl. BMC Microbiol. 6:20.
• Finlay W.J.J., N.A. Logan and A.D. Sutherland. 2000. Bacillus cereus produces most emetic toxin at lower temperatures. Lett. Appl. Microbiol. 31: 385-389.
• Finlay W.J.J., N.A. Logan and A.D. Sutherland. 2002. Bacillus cereus emetic toxin production in cooked rice. Food Microbiol. 19: 431-439.
• Fricker M., U. Messelhausser, U. Busch, S. Scheres and M. Ehling-Schulz. 2007. Diagnostic real-time PCR assays for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Appl. Environ. Microbiol. 73: 1892-1898.
• Granum P.E. and T. Lund. 1997. Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Lett. 157: 223-228.
• Goodfellow M., E.V. Ferguson and J.-J. Sanglier. 1992. Numerical classification and identification of Streptomyces species - a review. Gene 115: 225-232.
• Guinebretiere M.H., H. Girardin, C. Dargaignaratz, F. Carlin and C. Nguyen-The. 2006. Contamination flows of Bacillus cereus and spore-forming aerobic bacteria in a cooked, pasteurized and chilled zucchini puree processing line. înt. J. Food Microbiol. 82: 223-232.
• Hansen B.M. and N.B. Hendriksen. 2001. Detection of entero-toxic Bacillus cereus and Bacillus thuringiensis strains by PCR analysis. Appl. Environ. Microbiol. 67: 185-189.
• Häggblom M.M., C. Apetroaic, M.A. Andersson and M.S. Salkinoja-Salonen. 2002. Quantitative analysis of cereulide, the emetic toxin of Bacillus cereus, produced under various conditions. Appl. Environ. Microbiol. 68: 2479-2483.
• Helgason E., D.A. Caugant, I. Olsen and A.-B. Kolsto. 2000. Genetic structure of population of Bacillus cereus and Bacillus thuringiensis isolates associated with periodontitis and other human infections. J. Clin. Microbiol. 38: 1615-1622.
• Hoton F.M., L. Andrup, I. Święcicka and J. Mahillon. 2005. The cereulide genetic determinants of emetic Bacillus cereus are plasmid-borne. Microbiology 151: 2121-2124.
• Horwood P.F., G.W. Burgess and H.J. Oakey. 2004. Evidence for nonribosomal peptide synthetase production of cereulide (the emetic toxin) in Bacillus cereus. FEMS Microbiol. Lett. 232: 319-324.
• Jääskeläinen E.L., M.M. Häggblom, M.A. Andersson, L. Vanne and M.S. Salkinoja-Salonen. 2003a. Potential of Bacillus cereus for producing emetic toxin, cereulide, in bakery products: quantitative analysis by chemical and biological methods. J. Food Prot. 66: 1047-1054.
• Jääskeläinen E.L., V. Teplova, M.A. Andersson, L.C. Andersson, P. Tammela, M.C. Andersson, T.I. Pirhonen, N.E. Saris, P. Vuorela and M.S. Salkinoja-Salonen. 2003b. In vitro assay for human toxicity of cereulide, the emetic mitochondrial toxin produced by food poisoning Bacillus cereus. Toxicol, in vitro 1 7: 737-744.
• Jääskeläinen EX., M.M. Häggblom, M.A. Andersson and M.S. Salkinoja-Salonen. 2004. Atmospheric oxygen and other conditions affecting the production if cereulide by Bacillus cereus in food. Int. J. Food Microbiol. 96: 75-83. Jensen G.B., B.M. Hansen, J. Eilenberg and J. Mahillon. 2003. The hidden lifestyles of Bacillus cereus and relatives. Environ. Microbiol. 5: 631-640.
• Lucking G., M.K. Dommel, S. Scherer, A. Fouet and M. Ehling-Schulz. 2009. Cereulide synthesis in emetic Bacillus cereus is controlled by the transition state regulator AbrB, but not by the virulence regulator PlcR. Microbiology 155: 922-931.
• Mahler H., A. Pasi, J.N. Kramer, P. Schulte, A.C. Scoging, W. Bär and S. Krähenbühl. 1997. Fulminant liver failure in association with the emetic toxin of Bacillus cereus. N. Engl. J. Med. 336: 1173-1174.
• Maianski N.A., D. Roos and T.W. Kuijpers. 2003. Tumor necrosis factor alpha induces a caspase-independent death pathway in human neutrophiles. Blood 101: 1987-1995.
• Marahiel M.A., T. Stachelhaus and H.D. Mootz. 1997. Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97: 2651-2673.
• Michelet N., P.E. Granum and J. Mahillon. 2006. Bacillus cereus enterotoxins, bi- and tri- component cytolysins and other haemolysins. In: Alouf J., Popoff M.R. (Eds.) The comprehensive sourcebook of bacterial toxins. Academic Press, London, pp. 779-790.
• Mikkola R., N.-E.L. Saris, P.A. Grigoriev, M.A. Andersson and M.S. Salkinoja-Salonen. 1999. Ionophoretic properties and mitochondrial effects of cereulide. Eur J. Biochem. 263: 112-117.
• Omura S., H. Ikeda, J. Ishikawa, A. Hanamoto, C. Takahashi, M. Shinose, Y. Takahashi, H. Horikawa, H. Nakazawa, T. Osnoe and others. 2001. Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc. Natl. Acad. Sei. USA 98: 12215-12220.
• Paananen A., R. Mikkola, T. Sareneva, S. Matikainen, M. Andersson, I. Julkunen, M.S. Salkinoja-Salonen and T. Timonen. 2000. Inhibition of human NK cell function by valinomycin, a toxin from Streptomyces griseus in indoor air. Infect. Immun. 68: 165-169.
• Paananen A., R. Mikkola, T. Sareneva, S. Matikainen, M. Hess, M. Andersson, I. Julkunen, M.S. Salkinoja-Salonen and T. Timonen. 2002. Inhibition of human natural killer cell activity by cereulide, an emetic toxin from Bacillus cereus. Clin. Exp. Immunol. 129: 420-428.
• Paananen A., K. Jarvinen, T. Sareneva, M.S. Salkinoja-Salonen, T. Timonen and E. Hölttä. 2005. Valinomycin-induced apoptosis of human NK cells is predominantly caspase independent. Toxicology 212: 37-45.
• Park C.N., J.M. Lee, D. Lee and B.S. Kim. 2008 Antifungal activity of valinomycin, a peptide antibiotic produced by Streptomyces sp. strain M10 antagonistic to Botrytis cinerea. J. Microbiol. Biotechnol. 18: 880-884.
• Perkins J.B., S. K. Guterman, C.L. Howitt, V.E. Williams and J. Pero. 1990. Streptomyces genes involved in biosynthesis of the peptide antibiotic valinomycin. J. Bacteriol. 172: 3108-3116.
• Pettit G.R., R. Tan, N. Melody, J.M. Kielty, R.K. Pettit, D.L. Herald, B.E. Tucker, L.P. Mallavia, D.L. Doubek and J.M. Schmidt. 1999. Antineoplastic agents. Part 409: Isolation and structure of montanastatin from a terrestrial actinomycete. Bioorgan. Med. Chem. 7: 895-899.
• Priest F.G. 1993. Systematics and Ecology of Bacillus. In: Sonenshein A.L., Hoch J.A., Losick R. (eds.), Bacillus subtilis and other gram-positive bacteria. Biochemistry, Physiology, and Molecular Genetics. ASM, Washington.
• Radko L., W. Cybulski, J. Wessely-Szponder and W. Rzeski. 2006. Studies on cytotoxicity monensin and narasin in rat hepato-cyte cell line culture. Med. Weter. 62: 834-836.
• Rajkovic A., M. Uyttendaele, W. Deley, A. Van Soom and J. Rijsselaere. 2006. Dynamics of boar semen motility inhibition as a semi-quantitative measurement of Bacillus cereus emetic toxic (Cereulide). J. Microbiol. Meth. 65: 525-534.
• Rajkovic A, M. Uyttendaele, A. Vermeulen, M. Andjelkovic, I. Fitz-James, P. in 't Veld, Q. Denon, R. Verhe and J. Debevere. 2008. Heat resistance of Bacillus cereus emetic toxin, cereulide. Lett, Appl. Microbiol. 46: 536-41.
• Rasko D.A., J. Ravel, O.A. Okstad, E. Helgason, R.Z. Cer, L. Jiang, K.A. Shores, D.E. Fouts, N.J. Tourasse, S.V. Anqiuoli and others. 2004. The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO 1. Nucleic Acid Res. 32: 977-988.
• Rasko D.A., M.J. Rosowitz, O.A. Okstad, D.E. Fouts, L. Jiang, R.Z. Cer, A.-B. Kolsto, S.R. Gill and J. Ravel. 2007. Complete sequence analysis of novel plasmids from emetic and periodontal Bacillus cereus isolates reveals a common evolutionary history among the B. cereus-gxovip plasmids, including Bacillus anthracis pXOl. J. Bacteriol. 189: 52-64.
• Salkinoja-Salonen M.S., M.A. Andersson, R. Mikkola, A. Paananen, J. Peltola, H. Mussalo-Rauhamaa, R. Vuorio, N.-E. Saris, P. Grigorjev, J. Helin and others. 1998. Toxigenic microbes in indoor environment: identification, structure and biological effects of the aerosolising toxins. In: Johanning E. (ed.) 3rd Int Conf on Bioaerosols, Fungi and Mycotoxins. Saratoga Springs, New York.
• Shinagawa K., H. Konuma, H. Sekita and S. Rugii. 1995. Ernesis of rhesus monkeys induced by intragastric administration with the HEp-2 vacuolation factor (cereulide) produced by Bacillus cereus. FEMS Microbiol. Lett. 130: 87-90.
• Siebier S.A. and M.A. Marahiel. 2003. Learning from nature's drug factories: nonribosomal synthesis of macrocyclic peptides. J. Bacteriol. 185: 7036-7043.
• Święcicka I. and J. Mahillon. 2006. Diversity of commensal Bacillus cereus sensu lato isolated from the common sow bug (Porcelio scaber, Isopoda). FEMS Microbiol. Ecol. 56: 132-140.
• Święcicka I., G.A. Van der Auvera and J. Mahillon. 2006. Hemolytic and nonhemolytic enterotoxin genes are broadly distributed among Bacillus thuringiensis isolated from wild mammals. Microbial. Ecol. 52: 544-551.
• Święcicka L, D.K. Bideshi and B.A. Federici. 2008. Novel isolate of Bacillus thuringiensis subsp. thuringiensis that produces a quasiquboidal crystal of Cry l Ab 21 toxic to larvae of Tricho-plusiani. Appl. Environ. Microbiol. 74: 923-930.
• Thorsen L., B.M. Hansen, K.F. Nielsen, N.B. Hendriksen, R.K. Phipps and B.B. Budde. 2006. Characterization of emetic Bacillus weihenstephanensis, a new cereulide-producing bacterium. Appl. Environ. Microbiol. 12: 5118-5121.
• Turnbull P.C., J.M. Kramer, K. Jørgensen, R.J. Gilbert and J. Melling. 1979. Properties and production characteristic of vomiting, diarrheal, and necrotizing toxins of Bacillus cereus. Am, J. Clin. Nutr. 32: 219-228.
• Van der Auwera G.A., L. Andrup and J. Mahillon. 2005. Conjugative plasmid pAW63 brings new insights into the genesis of the Bacillus anthracis virulence plasmid pX02 and of the Bacillus thuringiensis plasmid pBT9727. BMG Genomics 6: 103.
• Van der Auwera G.A., S. Timmery, F. Hoton and J. Mahillon. 2007. Plasmid exchanges among members of the Bacillus cereus group in foodstuffs. Int. J. Food Microbiol. 113: 164-172.
• Van der Auwera G.A., S. Timmery and J. Mahillon. 2008. Self-transfer and mobilisation capabilities of the pX02-like plasmid pBT9727 from Bacillus thuringiensis subsp. konkukian 97-27. Plasmid 59: 134-138.
• Wilcks A., B.M. Hansen, N.B. Hendriksen and T.R. Licht. 2006. Persistence of Bacillus thuringiensis bioinsecticides in the gut of human-flora-associated rats. FEMS Immunol. Med. Microbiol. 48: 410-418.
• Wulff E.G., CM. Mguni, K. Mansfeld-Giesc, J. Fels, M. Lubeck and J. Hockenhull. 2002. Biochemical and molecular characterization of Bacillus ainyloliquefaciens, B. subtilis and B. pumilus isolates with distinct antagonistic potential against Xanthomonas campestris pv. campestris. Plant Pathol. 5 1: 574-584.