446
Views
15
CrossRef citations to date
0
Altmetric
Articles

Assessment of cytotoxic and genotoxic effects of enniatin-A in vitro

, , , &
Pages 1633-1644 | Received 13 Mar 2018, Accepted 30 May 2018, Published online: 16 Jul 2018

References

  • Aksoy H, Yılmaz S, Çelik M, Yüzbaşıoğlu D, Ünal F. 2008-II. Moniliformin Mikotoksininin in vitro Genotoksik Etkileri. SAÜ Fen Bil Der. 10(2):1–14.
  • Alakoc C, Eroğlu HE. 2011. Determining mitotic index in peripheral lymphocytes of welders exposed to metal arc welding fumes. Turk J Biol. 35:325–330.
  • Ataseven N, Yüzbaşıoğlu D, Keskin AÇ, Ünal F. 2016. Genotoxicity of monosodium glutamate. Food Chem Toxicol. 91:8–18.
  • Azqueta A, Collins A. 2013. The essential comet assay: a comprehensive guide to measuring DNA damage and repair. Arch Toxicol. 87:949–968.
  • Bausinger J, Speit G. 2016. The impact of lymphocyte isolation on induced DNA damage in human blood samples measured by the comet assay. Mutagenesis. 00:1–6.
  • Behm C, Degen GH, Föllmann W. 2009. The Fusarium toxin enniatin B exerts no genotoxic activity, but pronounced cytotoxicity in vitro. Mol Nutr Food Res Special Issue: Food-Borne Mycotoxins. 53(4):423–430.
  • Bennett JW, Klich M. 2003. Mycotoxins. Clin Microbiol Rev. 16:497–516.
  • Bourais I, Amine A. 2006. Aflatoxines: toxiques redoutables dans nos aliments. Les Technologies De Laboratoire. 1:4–8.
  • Çelik M, Aksoy H, Yılmaz S. 2010. Evaluation of beauvericin genotoxicity with the chromosomal aberrations, sister-chromatid exchanges and micronucleus assays. Ecotox Environ Safe. 73:1553–1557.
  • Chen Y, Ma J, Wang F, Hu J, Cui A, Wei C, Yang Q, Li F. 2013. Amygdalin induces apoptosis in human cervical cancer cell line HeLa cells. Immunopharmacol Immunotoxicol. 35(1):43–51.
  • [EC] European Commission. 2006. Commission Recommendation 2006b/576/EC of 17 August 2006 on the presence of Deoxynivalenol, Zearalenone, Ochratoxin A, T-2 and HT-2 and Fumonisins in products intended for animal feeding. [accessed 2016 Nov 03]. http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32006H0576&from=EN.
  • [EC] European Commission. 2013. Commission Recommendation 2013/165/EU of 27 March 2013 on the presence of T-2 and HT-2 toxin in cereals and cereal products text with EEA relevance.[accessed 2016 Nov 03]. http://eur-lex.europa.eu/legalcontent/EN/TXT/PDF/?uri=CELEX:32013H0165& from=EN
  • Dabrowski M, Obremski K, Gajecka M, Gajecki MT, Zielonka L. 2016. Changes in the subpopulations of porcine peripheral blood lymphocytes induced by exposure to low doses of Zearalenone (ZEN) and deoxynivalenol (DON). Molecules. 21:557.
  • De Lorenzi L, De Giovanni A, Malagutti L, Molteni L, Sciaraffia F, Tamburini A, Zannotti M. 2005. Genotoxic activity of the Fumonisin B1 mycotoxin in cultures of bovine lymphocytes. Ital J Anim Sci. 4:395–402.
  • Desjardins AE, Proctor RH. 2007. Molecular biology of Fusarium mycotoxins. Int J Food Microbiol. 119(1–2):47–50.
  • Doebler JA. 2000. Effects of neutral ionophores on membrane electrical characteristics of NG108-15 cells. Toxicol Lett. 114:27–38.
  • Dornetshuber R, Heffeter P, Kamyar MR, Peterbauer T, Berger W, Lemmens-Gruber R. 2007. Enniatin exerts p53-dependent cytostatic and p53-independent cytotoxic activities against human cancer cells. Chem Res Toxicol. 20:465–473.
  • Ergene S, Çelik A, Çavaş T, Kaya F. 2007. Genotoxic biomonitoring study of population residing in pesticide contaminated regions in Göksu Delta: micronucleus, chromosomal aberrations and sister chromatid exchanges. Environ Int. 33:877–885.
  • Escriva L, Font G, Manyes L. 2015. In vivo toxicity studies of fusarium mycotoxins in the last decade: a review. Food Chem Toxicol. 78:185–206.
  • Evans HJ. 1984. Human peripheral blood lymphocytes for the analysis of chromosome aberrations in mutagentests in mutagen tests. In: Kilbey BJ, Legator M, Nichols W, Ramel C, editors. Handbook of mutagenicity test procedures. Amsterdam: Elsevier Science Publishers; p. 405–427.
  • Fenech M. 2000. The in vitro micronucleus technique. Mutat Res. 455(1–2):81–95.
  • Firakova S, Proksa B, Sturdikova M. 2007. Biosynthesis and biological activities of enniatins. Pharmazie. 62:563–568.
  • Fornelli F, Minervini F, Logrieco A. 2004. Cytotoxicity of fungal metabolites to lepidopteran (Spodoptera frugiperda) cell line (SF 9). J Inv Pathol. 85:74–79.
  • Gaumann E, Roth S, Ettlinger L, Plattner PA, Nager U. 1947. Enniatin, ein neues gegen Mykobakterien wirksames Antibiotikum. Experimentia. 3:202.
  • Goyary D, Chattopadhyay P, Giri S, Aher V, Upadhyay A, Veer V. 2014. Ochratoxin A induces cytotoxicity, DNA damage and apoptosis in rat hepatocyte primary cell culture at nanomolar concentration. World Mycotoxin J. 7:379–386.
  • Hartmann A, Agurell E, Beevers C, Brendler-Schwaab S, Burlinson B, Clay P, Collins A, Smith A, Speit G, Thybaud V, et al. 2003. Recommendations for conducting the in vivo alkaline comet assay. Mutagenesis. 18(1):45–51.
  • Holland NT, Duramad P, Rothman N, Figgs LW, Blair A, Hubbard A, Smith MT. 2002. Micronucleus frequency and proliferation in human lymphocytes after exposure to herbicide 2,4-dichlorophenoxyacetic acid in vitro and in vivo. Mutat Res. 521:165–178.
  • Ivanova L, Skjerve E, Eriksen GS, Uhling S. 2006. Cytotoxicity of enniatins A, A1, B, B1, B2 and B3 from Fusarium avenaceum. Toxicon. 47:868–876.
  • Jain AK, Andsorbhoy RK. 1988. Cytogenetical studies on the effects of some chlorinated pesticides. III. Concluding remarks. Cytologia. 53:427–436.
  • Jestoi M. 2008. Emerging Fusarium-mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin – a review. Crit Rev Food Sci Nutr. 48:21–49.
  • Juan C, Manes J, Raiola A, Ritieni A. 2013b. 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.
  • Juan C, Manyes L, Font G, Juan-Garcia A. 2014. Evaluation of immunologic effect of Enniatin A and quantitative determination in feces, urine and serum on treated Wistar rats. Toxicon. 87:45–53.
  • Juan C, Ritieni A, Manes J. 2013a. Occurrence of Fusarium mycotoxins in Italian cereal and cereal products from organic farming. Food Chem. 141:1747–1755.
  • Kamyar M, Rawnduzi P, Studenik CR, Kouri K, Lemmens-Gruber R. 2004. Investigation of the electrophysiological properties of enniatins. Arch Biochem Biophys. 429:215–223.
  • Kirsch-Volders M, Plas G, Elhajouji A, Lukamowicz M, Gonzalez L, Loock KV, Decordier I. 2011. The in vitro MN assay in 2011: origin and fate, biological significance protocols, high throughput methodologies and toxicological relevance. Arch Toxicol. 85(8):873–899.
  • Logrieco AF, Mulé G, Moretti A, Bottalico A. 2002. Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. Eur J Plant Pathol. 108:597–609.
  • Loi M, Fanelli F, Liuzzi VC, Logrieco AF, Mulè G. 2017. Mycotoxin biotransformation by native and commercial enzymes: present and future perspectives. Toxins. 9:111.
  • Lu H, Fernández-Franzón M, Font G, Ruiz MJ. 2013. Toxicity evaluation of individual and mixed enniatins using an in vitro method with CHO-K1 cells. Toxicol In Vitro. 27(2):672–680.
  • Lu Z, Chen H, Zheng XM, Chen ML. 2017. Experimental study on the apoptosis of cervical cancer Hela cells induced by juglone through c-Jun N-terminal kinase/c-Jun pathway. Asian Pac J Trop Med. 10(6):572–575.
  • Mamur S, Unal F, Altok K, Deger SM, Yuzbasioglu D. 2016. DNA damage in hemodialysis patients with chronic kidney disease; a test of the role of diabetes mellitus; a comet assay investigation. Mutat Res. 800:22–27.
  • Mamur S, Yüzbaşioğlu D, Unal F, Yilmaz S. 2010. Does potassium sorbate induce genotoxic or mutagenic effects in lymphocytes? Toxicol In Vitro. 24(3):790–794.
  • Manyes L, Escriva L, Serrano AB, Rodriguez-Carrasco Y, Tolosa J, Meca G, Font G. 2014. A preliminary study in Wistar rats with enniatin A contaminated feed. Toxicol Mech Methods. 24:179–190.
  • Meca G, Font G, Ruiz MJ. 2011. Comparative cytotoxicity study of enniatins A, A₁, A₂, B, B₁, B₄ and J₃ on Caco-2 cells, Hep-G₂ and HT-29. Food Chem Toxicol. 49(9):2464–2469.
  • Meca G, Ruiz MJ, Soriano JM, Ritieni A, Moretti A, Font G, Manes J. 2010. Isolation and purification of enniatins A, A1, B, B1, produced by Fusarium tricinctum in solid culture, and cytotoxicity effects on Caco-2 cells. Toxicon. 56:418–424.
  • Medina A, Rodríguez A, Magan N. 2015. Climate change and mycotoxigenic fungi: impacts on mycotoxin production. Curr Opin Food Sci. 5:99–104.
  • Meky FA, Hardie LJ, Evans SW, Wild CP. 2001. Deoxynivalenol induced immunomodulation of human lymphocyte proliferation and cytokine production. Food Chem Toxicol. 39:827–836.
  • Mossman T. 1983. Rapid colometric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 65:55–63.
  • Nguyen PA, Strub C, Fontana A, Schorr-Galindo S. 2017. Crop molds and mycotoxins: alternative management using biocontrol. Biol Control. 104:10–27.
  • Palus J, Rydzynski K, Dziubaltowska E, Wyszynska K, Natarajan AT, Nilsson R. 2003. Genotoxic effects of occupational exposure to lead and cadmium. Mutat Res. 540:19–28.
  • Perry PE, Thompson EJ. 1984. The methodology of sister chromatid exchanges. In: Kilbey BJ, Legator M, Nichols W, Ramel C, editors. Handbook of mutagenicity test procedures. Amsterdam: Elsevier Science Publishers; p. 495–529.
  • Rodriguez-Carrasco Y, Heilos D, Richter L, Sussmuth RD, Heffeter P, Sulyok M, Kenner L, Berger W, Dornetshuber-Fleiss R. 2016. Mouse tissue distribution and persistence of the food-born fusariotoxins Enniatin B and Beauvericin. Toxicol Lett. 247:35–44.
  • Scherkenbeck J, Jeschke P, Harder A. 2002. PF1022A and related cyclodepsipeptides-a novel class of anthelmintics. Curr Topics Med Chem. 2:759–777.
  • Schneider EL, Nakanishi Y, Lewis J, Sternberg H. 1981. Simultaneous examination of sister-chromatid exchanges and cell replication kinetics in tumor and normal cells in vivo. Cancer Res. 41:4973–4975.
  • Serrano AB, Meca G, Font G, Ferrer E. 2012. Risk assessment associated to the intake of the emerging Fusarium mycotoxins BEA, ENs and FUS present in infant formula of Spanish origin. Food Control. 28:178–183.
  • Singh NP, McCoy MT, Tice RR, Schneider EL. 1988. A simple technique forquantitation of low levels of DNA damage in individual cells. Exp Cell Res. 175:184–191.
  • Singh S, Banerjee S, Chattopadhyay PS, Borthakur K, Veer V. 2015. Deoxynivalenol induces cytotoxicity and genotoxicity in animal primary cell culture. Toxicol Mech Methods. 25(3):184–191.
  • Speit G, Houpter S. 1985. On the mechanism of differential Giemsa staining of Bromodeoxyuridine substitute chromosomes. II. Differences between the demonstration of sister chromatid differentiation and replication patterns. Hum Genet. 70:126–129.
  • Springler A, Vrubel GJ, Mayer E, Schatzmayr G, Novak B. 2016. Effect of Fusarium-derived metabolites on the barrier integrity of differentiated Intestinal Porcine Epithelial Cells (IPEC-J2). Toxins. 8:345.
  • Stanciu O, Juan C, Miere D, Loghin F, Manes J. 2017. Occurrence and co-occurrence of Fusarium mycotoxins in wheat grains and wheat flour from Romania. Food Control. 73:147–155.
  • Surrales J, Xamena N, Creus A, Catalan J, Norppa H, Marcos R. 1995. Induction of micronuclei by five pyrethroid insecticides in whole blood and isolated human lymphocytes cultures. Mutat Res. 341:169–184.
  • Uhlig S, Gutleb A, Thrane U, Flaoyen A. 2004. Identification of cytotoxic principles of Fusarium avenaceum using bioassay-guided fraction. Toxicon. 46:150–159.
  • Velickova N, Milev M. 2017. Micronucleus assay as genotoxicity method to determine the human health risk. Int J Curr Res Chem Pharm Sci. 4(5):31–35.
  • Ware LY, Durand N, Nikiema PA, Alter P, Fontana A, Montet D, Barro N. 2017. Occurrence of mycotoxins in commercial infant formulas locally produced in Ouagadougou (Burkina Faso). Food Control. 73:518–523.
  • Watjen W, Debbab A, Hohlfeld A, Chovolou Y, Kampkötter A, Edrada RA, Ebel R, Hakiki A, Mosaddak M, Totzke F, et al. 2009. Enniatins A1, B and B1 from an endophytic strain of Fusarium tricintum induce apoptotic cell death in H4IIE hepatoma cells accompanied by inhibition of ERK phosphorylation. Mol Nutr Food Res. 53:431–440.
  • Yılmaz E. 2014. Mutagenecity of Enniatin a1 and b1 mycotoxins in Ames Salmonella microsome test. Kafkas Univ Vet Fak Derg. 20(6):893–896.
  • Yılmaz S, Unal F, Yuzbasıoğlu D, Aksoy H. 2008. Clastogenic effects of food additive citric acid in human peripheral lymphocytes. Cytotechnology. 56:137–140.
  • Yüzbaşıoğlu D, Celik M, Yılmaz S, Unal F, Aksoy H. 2006. Clastogenicity of the fungicide afugan in cultured human lymphocytes. Mutat Res. 604:53–59.
  • Zengin N, Yuzbasıoğlu D, Unal F, Yılmaz S, Aksoy H. 2011. The evaluation of the genotoxicity of two food preservatives: sodium benzoate and potassium benzoate. Food Chem Toxicol. 49:763–769.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.