A Review on the Synthesis and Bioactivity Aspects of Beauvericin, a Fusarium Mycotoxin
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
30515098
PubMed Central
PMC6256083
DOI
10.3389/fphar.2018.01338
Knihovny.cz E-zdroje
- Klíčová slova
- Fusarium, anticancer, beauvericin, bioactivity, biosynthesis,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Beauvericin (BEA) is an emerging Fusarium mycotoxin that contaminates food and feeds globally. BEA biosynthesis is rapidly catalyzed by BEA synthetase through a nonribosomal, thiol-templated mechanism. This mycotoxin has cytotoxicity and is capable of increasing oxidative stress to induce cell apoptosis. Recently, large evidence further shows that this mycotoxin has a variety of biological activities and is being considered a potential candidate for medicinal and pesticide research. It is noteworthy that BEA is a potential anticancer agent since it can increase the intracellular Ca2+ levels and induce the cancer cell death through oxidative stress and apoptosis. BEA has exhibited effective antibacterial activities against both pathogenic Gram-positive and Gram-negative bacteria. Importantly, BEA exhibits an effective capacity to inhibit the human immunodeficiency virus type-1 integrase. Moreover, BEA can simultaneously target drug resistance and morphogenesis which provides a promising strategy to combat life-threatening fungal infections. Thus, in this review, the synthesis and the biological activities of BEA, as well as, the underlying mechanisms, are fully analyzed. The risk assessment of BEA in food and feed are also discussed. We hope this review will help to further understand the biological activities of BEA and cast some new light on drug discovery.
Biomedical Research Centre University Hospital Hradec Kralove Czechia
College of Life Science Yangtze University Jingzhou China
Department of Chemistry Faculty of Science University of Hradec Kralove Hradec Kralove Czechia
Zobrazit více v PubMed
Albonico M., Schutz L. F., Caloni F., Cortinovis C., Spicer L. J. (2017). In vitro effects of the Fusarium mycotoxins fumonisin B1 and beauvericin on bovine granulosa cell proliferation and steroid production. Toxicon. 128, 38–45. 10.1016/j.toxicon.2017.01.019 PubMed DOI
Beccari G., Senatore M. T., Tini F., Sulyok M., Covarelli L. (2018). Fungal community, Fusarium head blight complex and secondary metabolites associated with malting barley grains harvested in Umbria, central Italy. Int. J. Food Microbiol. 273, 33–42. 10.1016/j.ijfoodmicro.2018.03.005 PubMed DOI
Bertero A., Moretti A., Spicer L. J., Caloni F. (2018). Fusarium molds and mycotoxins: potential species-specific effects. Toxins 10:E244. 10.3390/toxins10060244 PubMed DOI PMC
Blesa J., Marín R., Lino C. M., Mañes J. (2012). Evaluation of enniatins A, A1, B, B1 and beauvericin in Portuguese cereal-based foods. Food Addit. Contam. A 29, 1727–1735. 10.1080/19440049.2012.702929 PubMed DOI
Carballo D., Font G., Ferrer E., Berrada H. (2018). Evaluation of mycotoxin residues on ready-to-eat food by chromatographic methods coupled to mass spectrometry in tandem. Toxins 10:E243. 10.3390/toxins10060243 PubMed DOI PMC
Castlebury L. A., Sutherland J. B., Tanner L. A., Henderson A. L., Cerniglia C. E. (1999). Use of a bioassay to evaluate the toxicity of beauvericin to bacteria. World J. Microb. Biot. 15, 119–121. 10.1023/A:1008895421989 DOI
Celik M., Aksoy H., Yilmaz S. (2010). Evaluation of beauvericin genotoxicity with the chromosomal aberrations, sister-chromatid exchanges and micronucleus assays. Ecotoxicol. Environ. Saf. 73, 1553–1557. 10.1016/j.ecoenv.2010.07.036 PubMed DOI
Chen B. F., Tsai M. C., Jow G. M. (2006). Induction of calcium influx from extracellular fluid by beauvericin in human leukemia cells. Biochem. Biophys. Res. Commun. 340, 134–139. 10.1016/j.bbrc.2005.11.166 PubMed DOI
CONTAM Panel (2014). (EFSA Panel on Contaminants in the Food Chain). Scientific Opinion on the risks to human and animal health related to the presence of beauvericin and enniatins in food and feed. EFSA J, 12:3916 10.2903/j.efsa.2014.3916 DOI
Covarelli L., Beccari G., Prodi A., Generotti S., Etruschi F., Meca G., et al. . (2015). Biosynthesis of beauvericin and enniatins in vitro by wheat Fusarium species and natural grain contamination in an area of central Italy. Food Microbiol. 46, 618–626. 10.1016/j.fm.2014.09.009 PubMed DOI
Daniel J. F. S., Silva A. A., Nakagawa D. H., de Medeiros L. S., Carvalho M. G. (2017). Larvicidal activity of Beauveria bassiana extracts against Aedes aegypti and Identification of Beauvericins. J. Braz. Chem. Soc. 28, 1003–1013. 10.21577/0103-5053.20160253 DOI
Decleer M., Landschoot S., De Saeger S., Rajkovic A., Audenaert K. (2018). Impact of fungicides and weather on cyclodepsipeptide-producing Fusarium spp. and beauvericin and enniatin levels in wheat grains. J. Sci. Food Agric. [Epub ahead of print]. 10.1002/jsfa.9167. PubMed DOI
Dornetshuber R., Heffeter P., Lemmens-Gruber R., Elbling L., Marko D., Micksche M., et al. (2009). Oxidative stress and DNA interactions are not involved in Enniatin- and Beauvericin-mediated apoptosis induction. Mol. Nutr. Food Res. 53, 1112–1122. 10.1002/mnfr.200800571 PubMed DOI
Dzoyema J. P., Melong R., Tsamoc A. T., Maffoc T., Kapched D. G., Ngadjuic B. T., et al. (2017). Cytotoxicity, antioxidant and antibacterial activity of four compounds produced by an endophytic fungus Epicoccum nigrum associated with Entada abyssinica. Revista Brasileira de Farmacognosia. 27, 251–253. 10.1016/j.bjp.2016.08.011 DOI
Escrivá L., Jennen D., Caiment F., Manyes L. (2018). Transcriptomic study of the toxic mechanism triggered by beauvericin in Jurkat cells. Toxicol. Lett. 284, 213–221. 10.1016/j.toxlet.2017.11.035 PubMed DOI
Fernández-Blanco C., Frizzell C., Shannon M., Ruiz M. J., Connolly L. (2016). An in vitro investigation on the cytotoxic and nuclear receptor transcriptional activity of the mycotoxins fumonisin B1 and beauvericin. Toxicol. Lett. 57, 1–10. 10.1016/j.toxlet.2016.05.021 PubMed DOI
Ferrer E., Juan-García A., Font G., Ruiz M. J. (2009). Reactive oxygen species induced by beauvericin, patulin and zearalenone in CHO-K1 cells. Toxicol. In Vitro 23, 1504–1509. 10.1016/j.tiv.2009.07.009 PubMed DOI
Feudjio F. T., Dornetshuber R., Lemmens M., Hoffmann O., Lemmens-Gruber R., Berger W. (2010). Beauvericin and enniatin: emerging toxins and/or remedies? World Mycotoxin J. 3, 415–430. 10.3920/WMJ2010.1245 DOI
Fornelli F., Minervini F., Logrieco A. (2004). Cytotoxicity of fungal metabolites to lepidopteran (Spodoptera frugiperda) cell line (SF-9). J. Invertebrate Pathol. 85, 74–79. 10.1016/j.jip.2004.01.002 PubMed DOI
Fraeyman S., Croubels S., Devreese M., Antonissen G. (2017). Emerging Fusarium and alternaria mycotoxins: occurrence, toxicity and toxicokinetics. Toxins 9:E228. 10.3390/toxins9070228 PubMed DOI PMC
Fukuda K., Arai M., Yamaguchi Y., Masuma R. (2004). New beauvericins, potentiators of antifungal miconazole activity produced by Beauveria sp. FKI-1366. J. Antibiot. 57, 110–116. 10.7164/antibiotics.57.110 PubMed DOI
Ganessi S., Moretti A., Bonvicini Pagliai A. M., Logrieco A., Sabatini A. (2002). Effects of beauvericin on Schizaphis graminium (Aphididae). J. Invert. Pathol. 80, 90–96. 10.1016/S0022-2011(02)00125-8 PubMed DOI
Grove J. F., Pople M. (1980). The insecticidal activity of beauvericin and the enniatin complex. Mycopathologia 70, 103–105. 10.1007/BF00443075 DOI
Guo Z. Q., Pfohl K., Karlovsky P., Dehne H. W., Altincicek B. (2016). Fumonisin B-1 and beauvericin accumulation in wheat kernels after seed-borne infection with Fusarium proliferatum. Agric. Food Sci. 25, 138–145. 10.23986/afsci.55539 DOI
Hamill R. L., Higgens C. E., Boaz H. E., Gorman M. (1969). The structure op beauvericin, a new depsipeptide antibiotic toxic to Artemia salina. Tetrahedron. Lett. 10, 4255–4258. 10.1016/S0040-4039(01)88668-8 DOI
Heilos D., Rodríguez-Carrasco Y., Englinger B., Timelthaler G., van Schoonhoven S., Sulyok M., et al. . (2017). The natural fungal metabolite beauvericin exerts anticancer activity in vivo: a pre-clinical pilot study. Toxins 9:E258. 10.3390/toxins9090258 PubMed DOI PMC
Hietaniemi V., Rämö S., Yli-Mattila T., Jestoi M., Peltonen S., Kartio M., et al. . (2016). Updated survey of Fusarium species and toxins in Finnish cereal grains. Food Addit. Contam. A 33, 831–848. 10.1080/19440049.2016.1162112 PubMed DOI
Hu L., Rychlik M. (2014). Occurrence of enniatins and beauvericin in 60 Chinese medicinal herbs. Food Addit. Contam. A 31, 1240–1245. 10.1080/19440049.2014.913813 PubMed DOI
Jestoi M., Rokka M., Yli-Marrila T., Parikka P., Rizzo A., Peltonen K. (2004). Presence and concentrations of the Fusarium-related mycotoxins beauvericin, enniatins and moniliformin in Finnish grain samples. Food Add. Contam. 21, 794–802. 10.1080/02652030410001713906 PubMed DOI
Jow G. M., Chou C. J., Chen B. F., Tsai J. H. (2004). Beauvericin induces cytotoxic effects in human acute lymphoblastic leukemia cells through cytochrome c release, caspase 3 activation: the causative role of calcium. Cancer Lett. 216, 165–173. 10.1016/j.canlet.2004.06.005 PubMed DOI
Juan C., Mañes J., Raiola A., Ritieni A. (2013a). Evaluation of beauvericin and enniatins in Italian cereal products and multicereal food by liquid chromatography coupled to triple quadrupole mass spectrometry. Food Chem. 140, 755–762. 10.1016/j.foodchem.2012.08.021 PubMed DOI
Juan C., Raiola A., Manes J., Ritieni A. (2014). Presence of mycotoxin in commercial infant formulas and baby foods from Italian market. Food Cont. 39, 227–236. 10.1016/j.foodcont.2013.10.036 DOI
Juan C., Ritieni A., Mañes J. (2013b). Occurrence of Fusarium mycotoxins in Italian cereal and cereal products from organic farming. Food Chem. 141, 1747–1755. 10.1016/j.foodchem.2013.04.061 PubMed DOI
Jurjevic Z., Solfrizzo M., Cvjetkovic B., De Girolamo A., Visconti A. (2002). Occurrence of beauvericin in corn from Croatia. Food Technol. Biotechnol. 40, 91–94.
Kepenekci I., Saglam H. D., Oksal E., Yanar D., Yanar Y. (2017). Nematicidal activity of Beauveria bassiana (Bals.-Criv.) Vuill. against root-knot nematodes on tomato grown under natural conditions. Egyptian J. Biol. Pest Control 27:117.
Kim J., Sung G. H. (2018). Beauvericin synthetase contains a calmodulin binding motif in the entomopathogenic fungus Beauveria bassiana. J. Gen. Appl. Microbiol. 64, 145–147. 10.2323/jgam.2017.09.003 PubMed DOI
Kopp F., Marahiel M. A. (2007). Macrocyclization strategies in polyketide and nonribosomal peptide biosynthesis. Nat. Prod. Rep. 24, 735–749. 10.1039/b613652b PubMed DOI
Kostecki M., Szczesna J., Chelkowski J., Wisniewska H. (1995). Beauvericin and moniliformin production by Polish isolates of Fusarium subglutinans and natural co-occurrence of both mycotoxins in maize samples. Microbiol. Aliments Nutr. 13, 67–70.
Kouri K., Lemmens M., Lemmens-Gruber R. (2003). Beauvericin-induced channels in ventricular myocytes and liposomes. Biochim. Biophys. Acta 1609, 203–210. 10.1016/S0005-2736(02)00689-2 PubMed DOI
Lee K. E., Kim B. H., Lee C. (2010). Occurrence of Fusarium mycotoxin beauvericin in animal feeds in Korea. Anim. Feed Sci. Tech. 157, 190–194. 10.1016/j.anifeedsci.2010.03.003 DOI
Leland J. E., McGuire M. R., Grace J. A., Jaronski S. T., Ulloa M., Park Y. H., et al. (2005). Strain selection of a fungal entomopathogen, Beauveria bassiana, for control of plant bugs (Lygus spp.)(Heteroptera: Miridae). Biol. Control 35, 104–114. 10.1016/j.biocontrol.2005.06.005 DOI
Lemmens-Gruber R., Rachoy B., Steininger E., Kouri K., Saleh P., Krska P., et al. . (2000). The effect of the Fusarium metabolite beauvericin on electromechanical and -physiological properties in isolated smooth and heart muscle preparations of guinea pigs. Mycopathologia 149, 5–12. 10.1023/A:1007293812007 PubMed DOI
Lin H. I., Lee Y. J., Chen B. F., Tsai M. C., Lu J. L., Chou C. J., et al. (2005). Involvement of Bcl-2 family, cytochrom c and caspase 3 in induction of apoptosis by beauvericin in human non-small cell lung cancer cells. Cancer Lett. 230, 248–259. 10.1016/j.canlet.2004.12.044 PubMed DOI
Lindblad M., Gidlund A., Sulyok M., Borjesson T., Krska R., Olsen M., et al. . (2013). Deoxynivalenol and other selected Fusarium toxins in Swedish wheat—occurrence and correlation to specific Fusarium species. Int. J. Food Microbiol. 167, 284–291. 10.1016/j.ijfoodmicro.2013.07.002 PubMed DOI
Liu T., Wang L., Duan Y. X., Wang X. (2008). Nematicidal activity of culture filtrate of Beauveria bassiana against Meloidogyne hapla. World J. Microbiol. Biotechnol. 24, 113–118. 10.1007/s11274-007-9446-z DOI
Logrieco A., Moretti A., Castella G., Kostecki M., Golinski P., Ritieni A., et al. . (1998). Beauvericin production by Fusarium species. Appl. Environ. Microbiol. 64, 3084–3088. PubMed PMC
Logrieco A., Moretti A., Ritieni A., Caiaffa M. F., Macchia L. (2002). Beauvericin: chemistry, biology and significance, in Advances in Microbial Toxin Research and Its Biotechnological Exploitation, eds Upadhyay, Rajeev K. (Boston, MA: Springer Verlag; ), 23–30. 10.1007/978-1-4757-4439-2_2 DOI
Lu C. L., Lin H. I., Chen B. F., Jow G. M. (2016). Beauvericin-induced cell apoptosis through the mitogen-activated protein kinase pathway in human nonsmall cell lung cancer A549 cells. J. Toxicol. Sci. 41, 429–437. 10.2131/jts.41.429 PubMed DOI
Mahnine N., Meca G., Elabidi A., Fekhaoui M., Saoiabi A., Font G., et al. (2011). Further data on the levels of emerging Fusarium mycotoxins enniatins (A, A1, B, B1), beauvericin and fusaproliferin in breakfast and infant cereals from Morocco. Food Chem. 124, 481–485. 10.1016/j.foodchem.2010.06.058 DOI
Mallebrera B., Juan-Garcia A., Font G., Ruiz M. J. (2016). Mechanisms of beauvericin toxicity and antioxidant cellular defense. Toxicol. Lett. 246, 28–34. 10.1016/j.toxlet.2016.01.013 PubMed DOI
Mallebrera B., Prosperini A., Font G., Ruiz M. J. (2018). In vitro mechanisms of Beauvericin toxicity: a review. Food Chem. Toxicol. 111, 537–545. 10.1016/j.fct.2017.11.019 PubMed DOI
Manizan A. L., Oplatowska-Stachowiak M., Piro-Metayer I., Campbell K., Koffi-Nevry R., Elliott C., et al. (2018). Multi-mycotoxin determination in rice, maize and peanut products most consumed in Cote d'Ivoire by UHPLC-MS/MS. Food Control 87, 22–30. 10.1016/j.foodcont.2017.11.032 DOI
Manyes L., Escrivá L., Ruiz M. J., Juan-García A. (2018). Beauvericin and enniatin B effects on a human lymphoblastoid Jurkat T-cell model. Food Chem. Toxicol. 115, 127–135. 10.1016/j.fct.2018.03.008 PubMed DOI
Massini P., Näf U. (1980). Ca2+ ionophores and the activation of human blood platelets. The effects of ionomycin, beauvericin, lysocellin, virginiamycin S, lasalocid-derivatives and McN 4308. Biochim. Biophys. Acta 598, 575–587. 10.1016/0005-2736(80)90037-1 PubMed DOI
McElhinney C., Danaher M., Elliott C. T., O'Kiely P. (2015). Mycotoxins in farm silages – a 2-year Irish national survey. Grass Forage Sci. 71, 339–352. 10.1111/gfs.12191 DOI
Meca G., Sospedra I., Soriano J. M., Ritieni A., Moretti A., Manes J. (2010). Antibacterial effect of the bioactive compound beauvericin produced by Fusarium proliferatum on solid medium of wheat. Toxicon 56, 349–354. 10.1016/j.toxicon.2010.03.022 PubMed DOI
Mei L., Zhang L., Dai R. (2009). An inhibition study of beauvericin on human and rat cytochrome P450 enzymes and its pharmacokinetics in rats. J. Enzyme Inhib. Med. Chem. 24, 753–762. 10.1080/14756360802362041 PubMed DOI
Mizukami M., Otsuka H., Yokota T. (2018). Global existence and boundedness in a chemotaxis-haptotaxis system with signal-dependent sensitivity. J. Math. Anal. Appl. 464, 354–369. 10.1016/j.jmaa.2018.04.002 DOI
Nilanonta C., Isaka M., Kittakoop P., Palittapongarnpim P., Kamchonwongpaisan S., Pittayakhajonwut D., et al. . (2000). Antimycobacterial and antiplasmodial cyclodepsipeptides from the insect pathogenic fungus Paecilomyces tenuipes BCC 1614. Planta Med. 66, 756–758. 10.1055/s-2000-9776 PubMed DOI
Nilanonta C., Isaka M., Kittakoop P., Trakulnaleamsai S. (2002). Precursordirected biosynthesis of beauvericin analogs by the insect pathogenic fungus Paecilomyces tenuipes BCC 1614. Tetrahedron 58, 3355–3360. 10.1016/S0040-4020(02)00294-6 DOI
Patocka J. (2016). Bioactive metabolites of entomopathogenic fungi Beauveria bassiana. Mil. Med. Sci. Lett. 85, 80–88. 10.31482/mmsl.2016.015 DOI
Peczynska-Czoch W., Urbanczyk M. J., Bałazy S. (1991). Formation of beauvericin by selected strains of Beauveria bassiana. Arch. Immunol. Ther. Exp. 139, 175–179. PubMed
Peeters H., Zocher R., Kleinkauf H. (1988). Synthesis of beauvericin by a multifunctional enzyme. J Antibiotics 41, 352–359. 10.7164/antibiotics.41.352 PubMed DOI
Prince R. C., Crofts A. R., Steinrauf L. K. (1974). A comparison of beauvericin, enniatin and valinomycin as calcium transporting agents in liposomes and chromatophores. Biochem. Biophys. Res. Commun. 59, 697–703. 10.1016/S0006-291X(74)80036-7 PubMed DOI
Prosperini A., Juan-García A., Font G., Ruiz M. J. (2013). Beauvericin-induced cytotoxicity via ROS production and mitochondrial damage in Caco-2 cells. Toxicol. Lett. 22, 204–211. 10.1016/j.toxlet.2013.07.005 PubMed DOI
Qadri S. M., Kucherenko Y., Lang F. (2011). Beauvericin induced erythrocyte cell membrane scrambling. Toxicology 283, 24–31. 10.1016/j.tox.2011.01.023 PubMed DOI
Quiles J. M., Saladino F., Mañes J., Fernández-Franzón M., Meca G. (2016). Occurrence of mycotoxins in refrigerated pizza dough and risk assessment of exposure for the Spanish population. Food Chem. Toxicol. 94, 19–24. 10.1016/j.fct.2016.05.011 PubMed DOI
Santini A., Meca G., Uhlig S., Ritieni A. (2012). Fusaproliferin, beauvericin and enniatins: occurrence in food-a review. World Mycotoxin J. 5, 71–81. 10.3920/WMJ2011.1331 DOI
Schenzel J., Hungerbühler K., Bucheli T. D. (2012). Mycotoxins in the environment: II. Occurrence and origin in Swiss river waters. Environ. Sci. Technol. 46, 13076–13084. 10.1021/es301558v PubMed DOI
Schoevers E. J., Santos R. R., Fink-Gremmels J., Roelen B. A. (2016). Toxicity of beauvericin on porcine oocyte maturation and preimplantation embryo development. Reprod. Toxicol. 65, 159–169. 10.1016/j.reprotox.2016.07.017 PubMed DOI
Serrano A. B., Font G., Mañes J., Ferrer E. (2013). Emerging Fusarium mycotoxins in organic and conventional pasta collected in Spain. Food Chem. Toxicol. 51, 259–266. 10.1016/j.fct.2012.09.034 PubMed DOI
Serrano A. B., Font G., Ruiz M. J., Ferrer E. (2012). Co-occurrence and risk assessment of mycotoxins in food and diet from Mediterranean area. Food Chem. 135, 423–429. 10.1016/j.foodchem.2012.03.064 PubMed DOI
Sewram V., Nieuwoudt T. W., Marasas W. F., Shephard G. S., Ritieni A. (1999). Determination of Fusarium mycotoxins, fusaproliferin and beauvericin by high-perfomance liquid chromatography-electrospray ionization mass spectrometry. J. Chromatogr. A. 858, 175–185. 10.1016/S0021-9673(99)00814-6 PubMed DOI
Shao M., Li L., Gu Z., Yao M., Xu D., Fan W., et al. . (2018). Mycotoxins in commercial dry pet food in China. Food Addit. Contam. Part B Surveill. 11, 237–245. 10.1080/19393210.2018.1475425 PubMed DOI
Shekhar-Guturja T., Gunaherath G. M., Wijeratne E. M., Lambert J. P., Averette A. F., Lee S. C., et al. . (2016a). Dual action antifungal small molecule modulates multidrug efflux and TOR signaling. Nat. Chem. Biol. 12, 867–875. 10.1038/nchembio.2165 PubMed DOI PMC
Shekhar-Guturja T., Tebung W. A., Mount H., Liu N., Köhler J. R., Whiteway M., et al. . (2016b). Beauvericin potentiates azole activity via inhibition of multidrug efflux, blocks Candida albicans morphogenesis, and is effluxed via Yor1 and circuitry controlled by Zcf29. Antimicrob. Agents Chemother. 60, 7468–7480. 10.1128/AAC.01959-16 PubMed DOI PMC
Shimada A., Fujioka S., Koshino H., Kimura Y. (2010). Nematicidal activity of beauvericin produced by the fungus Fusarium bulbicola. Z. Naturforsch. C. J Biosci. 65, 207–210. 10.1515/znc-2010-3-407 PubMed DOI
Shin C. G., An D. G., Song H. H., Lee C. (2009). Beauvericin and enniatins H, I and MK1688 are new potent inhibitors of human immunodeficiency virus type-1 integrase. J. Antibiot. 62, 687–690. 10.1038/ja.2009.102 PubMed DOI
Sifou A., Meca G., Serrano A. B., Mahnine N., El Abidi A., Mañes J., et al. (2011). First report on the presence of emerging Fusarium mycotoxins enniatins (A, A1, B, B1), beauvericin and fusaproliferin in rice on the Moroccan retail markets. Food Control 22, 1826–1830. 10.1016/j.foodcont.2011.04.019 DOI
Srobarova A., Moretti A., Ferracane R., Ritieni A., Logrieco A. (2002). Toxigenic Fusarium species of liseola section in pre-harvest maize ear rot and associated mycotoxins in Slovakia. Eur. J. Plant Pathol. 108, 299–306. 10.1023/A:1015645813231 DOI
Stanciu O., Juan C., Miere D., Loghin F., Mañes J. (2017). Presence of enniatins and beauvericin in romanian wheat samples: from raw material to products for direct human consumption. Toxins 9:E189. 10.3390/toxins9060189 PubMed DOI PMC
Steiniger C., Hoffmann S., Mainz A., Kaiser M., Voigt K., Meyer V., et al. . (2017). Harnessing fungal nonribosomal cyclodepsipeptide synthetases for mechanistic insights and tailored engineering. Chem. Sci. 8, 7834–7843. 10.1039/C7SC03093B PubMed DOI PMC
Sumikova T., Chrpova J., Dzuman Z., Salava J., Sterbova L., Palicova J., et al. (2017). Mycotoxins content and its association with changing patterns of Fusarium pathogens in wheat in the Czech Republic. World Mycotoxin J. 10, 143–151. 10.3920/WMJ2016.2133 DOI
Svingen T., Lund Hansen N., Taxvig C., Vinggaard A. M., Jensen U., Have Rasmussen P. (2017). Enniatin B and beauvericin are common in Danish cereals and show high hepatotoxicity on a high-content imaging platform. Environ. Toxicol. 32, 1658–1664. 10.1002/tox.22367 PubMed DOI
Taevernier L., Bracke N., Veryser L., Wynendaele E., Gevaert B., Peremans K., et al. . (2016a). Blood-brain barrier transport kinetics of the cyclic depsipeptide mycotoxins beauvericin and enniatins. Toxicol. Lett. 258, 175–184. 10.1016/j.toxlet.2016.06.1741 PubMed DOI
Taevernier L., Veryser L., Roche N., Peremans K., Burvenich C., Delesalle C., et al. . (2016b). Human skin permeation of emerging mycotoxins (beauvericin and enniatins). J. Expo. Sci. Environ. Epidemiol. 26, 277–287. 10.1038/jes.2015.10 PubMed DOI
Tang C. Y., Chen Y. W., Jow G. M., Chou C. J., Jeng C. J. (2005). Beauvericin activates Ca2+-activated Cl- currents and induces cell deaths in Xenopus oocytes via influx of extracellular Ca2+. Chem. Res. Toxicol. 18, 825–833. 10.1021/tx049733d PubMed DOI
Tansakul N., Jala P., Laopiem S., Tangmunkhong P., Limsuwan S. (2013). Co-occurrence of five Fusarium toxins in corn-dried distiller's grains with solubles in Thailand and comparison of ELISA and LC-MS/MS for fumonisin analysis. Mycotoxin Res. 29, 255–260. 10.1007/s12550-013-0173-z PubMed DOI
Tao Y. W., Lin Y. C., She Z. G., Lin M. T., Chen P. X., Zhang J. Y. (2015). Anticancer activity and mechanism investigation of beauvericin isolated from secondary metabolites of the mangrove endophytic fungi. Anticancer Agents Med. Chem. 15, 258–266. 10.2174/1871520614666140825112255 PubMed DOI
Toman E., Makrlík E., Vanura P. (2011). On the complexation of the sodium cation with beauvericin: experimental and theoretical study. Monatsh. Chem. 142, 779–782. 10.1007/s00706-011-0499-1 DOI
Tong Y., Liu M., Zhang Y., Liu X., Huang R., Song F., et al. . (2016). Beauvericin counteracted multi-drug resistant Candida albicans by blocking ABC transporters. Synth. Syst. Biotechnol. 1, 158–168. 10.1016/j.synbio.2016.10.001 PubMed DOI PMC
Tonshin A. A., Teplova V. V., Andersson M. A., Salkinoja-Salonen M. S. (2010). The Fusarium mycotoxins enniatins and beauvericin cause mitochondrial dysfunction by affecting the mitochondrial volume regulation, oxidative phosphorylation and ion homeostasis. Toxicology 276, 49–57. 10.1016/j.tox.2010.07.001 PubMed DOI
Uhlig S., Jestoi M., Parikka P. (2007). Fusarium avenaceum—the North European situation. Int. J. Food Microbiol. 119, 17–24. 10.1016/j.ijfoodmicro.2007.07.021 PubMed DOI
Uhlig S., Torp M., Heier B. T. (2006). Beauvericin and enniatins A, A1, B and B1 in Norwegian grain: a survey. Food Chem. 94, 193–201. 10.1016/j.foodchem.2004.11.004 DOI
Van der Fels-Klerx H. J., Kandhai M. C., Brynestad S., Dreyer M., Börjesson T., Martins H. M., et al. (2009). Development of a European system for identification of emerging mycotoxins in wheat supply chains. World Mycotoxin J. 2, 119–127. 10.3920/WMJ2008.1122 DOI
Wang Q., Xu L. (2012). Beauvericin, a bioactive compound produced by fungi: a short review. Molecules 17, 2367–2377. 10.3390/molecules17032367 PubMed DOI PMC
Wätjen W., Debbab A., Hohlfeld A., Chovolou Y., Proksch P. (2014). The mycotoxin beauvericin induces apoptotic cell death in H4IIE hepatoma cells accompanied by an inhibition of NF-κB-activity and modulation of MAP-kinases. Toxicol. Lett. 231, 9–16. 10.1016/j.toxlet.2014.08.021 PubMed DOI
Wu Q., Wang X., Nepovimova E., Miron A., Liu Q., Wang Y., et al. . (2017). Trichothecenes: immunomodulatory effects, mechanisms, and anti-cancer potential. Arch. Toxicol. 91, 3737–3785. 10.1007/s00204-017-2118-3 PubMed DOI
Wu Q., Wang X., Nepovimova E., Wang Y., Yang H., Kuca K. (2018). Mechanism of cyclosporine A nephrotoxicity: oxidative stress, autophagy, and signalings. Food Chem. Toxicol. 118, 889–907. 10.1016/j.fct.2018.06.054 PubMed DOI
Wu X., Smith J. S. (2007). A gas chromatography-flame ionization detection method for detection of fusaproliferin in corn. J. Agric. Food Chem. 55, 3211–3216. 10.1021/jf063489+ PubMed DOI
Wu X. F., Xu R., Ouyang Z. J., Qian C., Shen Y., Wu X. D., et al. . (2013). Beauvericin ameliorates experimental colitis by inhibiting activated T cells via downregulation of the PI3K/Akt signaling pathway. PLoS ONE 8:e83013. 10.1371/journal.pone.0083013 PubMed DOI PMC
Xu L., Wang J., Zhao J., Li P., Shan T., Wang J., et al. . (2010). Beauvericin from the endophytic fungus, Fusarium redolens, isolated from Dioscorea zingiberensis and its antibacterial activity. Nat. Prod. Commun. 5, 811–814. 10.1016/j.jbiotec.2008.07.304 PubMed DOI
Xu Y., Orozco R., Wijeratne E. M., Gunatilaka A. A., Stock S. P., Molnár I. (2008). Biosynthesis of the cyclooligomer depsipeptide beauvericin, a virulence factor of the entomopathogenic fungus Beauveria bassiana. Chem. Biol. 15, 898–907. 10.1016/j.chembiol.2008.07.011 PubMed DOI
Yoo S., Kim M. Y., Cho J. Y. (2017). Beauvericin, a cyclic peptide, inhibits inflammatory responses in macrophages by inhibiting the NF-κB pathway. Korean J. Physiol. Pharmacol. 21, 449–456 10.4196/kjpp.2017.21.4.449 PubMed DOI PMC
Yoshinari T., Suzuki Y., Sugita-Konishi Y., Ohnishi T., Terajima J. (2016). Occurrence of beauvericin and enniatins in wheat flour and corn grits on the Japanese market, and their co-contamination with type B trichothecene mycotoxins. Food Addit. Contam. Part A 33, 1620–1626. 10.1080/19440049.2016.1228126 PubMed DOI
Zhan J., Burns A. M., Liu M. X., Faeth S. H., Gunatilaka A. A. (2007). Search for cell motility and angiogenesis inhibitors with potential anticancer activity: Beauvericin and other constituents of two endophytic strains of Fusarium oxysporum. J. Nat. Prod. 70, 227–232. 10.1021/np060394t PubMed DOI PMC
Zhang H., Ruan C., Bai X., Zhang M., Zhu S., Jiang Y. (2016). Isolation and identification of the antimicrobial agent beauvericin from the endophytic Fusarium oxysporum 5-19 with NMR and ESI-MS/MS. Biomed. Res. Int. 2016:1084670. 10.1155/2016/1084670 PubMed DOI PMC
Zhang L., Yan K., Zhang Y., Huang R., Bian J., Zheng C., et al. . (2007). High-throughput synergy screening identifies microbial metabolites as combination agents for the treatment of fungal infections. Proc. Nat. Acad. Sci. U. S. A. 104, 4606–4611. 10.1073/pnas.0609370104 PubMed DOI PMC
Zhao D., Liu B., Wang Y., Zhu X., Duan Y., Chen L. (2013). Screening for nematicidal activities of Beauveria bassiana and associated fungus using culture filtrate. African J. Microbiol. Res. 7, 974–978. 10.5897/AJMR12.2340 DOI
Zinedine A., Meca G., Mañes J., Font G. (2011). Further data on the occurrence of Fusarium emerging mycotoxins enniatins (A, A1, B, B1), fusaproliferin and beauvericin in raw cereals commercialized in Morocco. Food Control 22, 1–5. 10.1016/j.foodcont.2010.05.002 DOI
Zobel S., Boecker S., Kulke D., Heimbach D., Meyer V., Süssmuth R. D. (2016). Reprogramming the biosynthesis of cyclodepsipeptide synthetases to obtain new enniatins and beauvericins. Chembiochem 17, 283–287. 10.1002/cbic.201500649 PubMed DOI
Zuzek M. C., Grandi M., Strajn B. J., Frangez R. (2016). Beauvericin inhibits neuromuscular transmission and skeletal muscle contractility in mouse hemidiaphragm preparation. Toxicol. Sci. 150, 283–291. 10.1093/toxsci/kfv326 PubMed DOI