Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 810490, 14 pages
http://dx.doi.org/10.1155/2014/810490
Research Article

Evaluation of Cytotoxic and Antimicrobial Effects of Two Bt Cry Proteins on a GMO Safety Perspective

1Graduate Program in Biochemistry, Federal University of Ceará, 60440-900 Fortaleza, CE, Brazil
2Graduate Program in Bioprocess Engineering and Biotechnology, Federal University of Paraná, P.O. Box 19011, 81531-98 Curitiba, PR, Brazil
3National Center of Genetic Resources (Embrapa-Cenargen), Parque Estação Biológica-PqEB-Avenida, W5 Norte (Final), P.O. Box 02372, 70770-917 Brasília, DF, Brazil
4Graduate Program in Pharmacology, Federal University of Ceará, 60430-270 Fortaleza, CE, Brazil
5Graduate Program in Gemonics Sciences and Biotechnology, Catholic University of Brasília, SGAN Quadra 916, Módulo B, W5 Norte, Asa Norte, 70790-160 Brasília, DF, Brazil

Received 18 April 2014; Accepted 1 July 2014; Published 23 July 2014

Academic Editor: Atanas Atanassov

Copyright © 2014 Davi Felipe Farias et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. L. Prieto-Samsonov, R. I. Vázquez-Padrón, C. Ayra-Pardo, J. González-Cabrera, and G.A. de la Riva, “Bacillus thuringiensis: from biodiversity to biotechnology,” Journal of Industrial Microbiology and Biotechnology, vol. 19, pp. 202–219, 1997. View at Publisher · View at Google Scholar
  2. J. Mendelsohn and J. Baselga, “Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer,” Journal of Clinical Oncology, vol. 21, no. 14, pp. 2787–2799, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. J. Romeis, M. Meissle, and F. Bigler, “Transgenic crops expressing Bacillus thuringiensis toxins and biological control,” Nature Biotechnology, vol. 24, no. 1, pp. 63–71, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. A. M. R. Gatehouse, N. Ferry, M. G. Edwards, and H. A. Bell, “Insect-resistant biotech crops and their impacts on beneficial arthropods,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 366, no. 1569, pp. 1438–1452, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. G. Sanahuja, R. Banakar, R. M. Twyman, T. Capell, and P. Christou, “Bacillus thuringiensis: a century of research, development and commercial applications,” Plant Biotechnology Journal, vol. 9, no. 3, pp. 283–300, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. G. R. Oliveira, M. C. Silva, W. A. Lucena et al., “Improving Cry8Ka toxin activity towards the cotton boll weevil (Anthonomus grandis),” BMC Biotechnology, vol. 11, article 85, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Delaney, J. D. Astwood, H. Cunny et al., “Evaluation of protein safety in the context of agricultural biotechnology,” Food and Chemical Toxicology, vol. 46, pp. S71–S97, 2008. View at Google Scholar
  8. M. O'Callaghan, T. R. Glare, E. P. J. Burgess, and L. A. Malone, “Effects of plants genetically modified for insect resistance on nontarget organisms,” Annual Review of Entomology, vol. 50, pp. 271–292, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Yu, Y. Li, and K. Wu, “Risk assessment and ecological effects of transgenic Bacillus thuringiensis crops on non-target organisms,” Journal of Integrative Plant Biology, vol. 53, no. 7, pp. 520–538, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. H. P. J. M. Noteborn, M. E. Bienenmann-Ploum, J. H. J. van den Berg et al., “Safety assessment of the Bacillus thuringiensis insecticidal crystal protein CRYIA(b) expressed in tomato,” in Genetically Modified Foods: Safety Issues, G. R. Takeoko, R. Teranishi, and K. H. Engel, Eds., pp. 23–26, American Chemical Society, Washington, DC, USA, 1996. View at Google Scholar
  11. M. Gill and D. Ellar, “Transgenic Drosophila reveals a functional in vivo receptor for the Bacillus thuringiensis toxin Cry1Ac1,” Insect Molecular Biology, vol. 11, no. 6, pp. 619–625, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. N. A. Broderick, K. F. Raffa, and J. Handelsman, “Midgut bacteria required for Bacillus thuringiensis insecticidal activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 41, pp. 15196–15199, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. H.-S.. Kim, S. Yamashita, T. Akao et al., “In vitro cytotoxicity of non-Cyt inclusion proteins of a Bacillus thuringiensis isolate against human cells, including cancer cells,” Journal of Applied Microbiology, vol. 89, no. 1, pp. 16–23, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Mesnage, E. Clair, S. Gress, C. Then, A. Székács, and G.-E. Séralini, “Cytotoxicity on human cells of Cry1Ab and Cry1Ac Bt insecticidal toxins alone or with a glyphosate-based herbicide,” Journal of Applied Toxicology, vol. 33, no. 7, pp. 695–699, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. T. G. Yudina, A. V. Konukhova, L. P. Revina, L. I. Kostina, I. A. Zalunin, and G. G. Chestukhina, “Antibacterial activity of Cry- and Cyt-proteins from Bacillus thuringiensis ssp. israelensis,” Canadian Journal of Microbiology, vol. 49, no. 1, pp. 37–44, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. L. P. Revina, L. I. Kostina, M. A. Dronina et al., “Novel antibacterial proteins from entomocidal crystals of Bacillus thuringiensis ssp. israelensis,” Canadian Journal of Microbiology, vol. 51, no. 2, pp. 141–148, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. T. G. Yudina, A. L. Brioukhanov, I. A. Zalunin et al., “Antimicrobial activity of different proteins and their fragments from Bacillus thuringiensis parasporal crystals against clostridia and archaea,” Anaerobe, vol. 13, no. 1, pp. 6–13, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Bondzio, F. Stumpff, J. Schön, H. Martens, and R. Einspanier, “Impact of Bacillus thuringiensis toxin Cry1Ab on rumen epithelial cells (REC)—a new in vitro model for safety assessment of recombinant food compounds,” Food and Chemical Toxicology, vol. 46, no. 6, pp. 1976–1984, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Bondzio, U. Lodemann, C. Weise, and R. Einspanier, “Cry1Ab treatment has no effects on viability of cultured porcine intestinal cells, but triggers Hsp70 expression,” PLoS ONE, vol. 8, no. 7, Article ID e67079, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  21. U. K. Laemmli, “Cleavage of structural proteins during the assembly of the head of bacteriophage T4,” Nature, vol. 227, no. 5259, pp. 680–685, 1970. View at Publisher · View at Google Scholar · View at Scopus
  22. M. F. Grossi-de-Sa, M. Q. de Magalhães, M. S. Silva et al., “Susceptibility of Anthonomus grandis (cotton boll weevil) and Spodoptera frugiperda (fall armyworm) to a Cry1Ia-type toxin from a Brazilian Bacillus thuringiensis strain,” Journal of Biochemistry and Molecular Biology, vol. 40, no. 5, pp. 773–782, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Edman, “Determination of amino acid sequences in protein,” Thrombosis et Diathesis Haemorrhagica, supplement 13, pp. 17–20, 1964. View at Google Scholar
  24. R. V. Burim, R. Canalle, J. L. C. Lopes, W. Vichnewski, and C. S. Takahashi, “Genotoxic action of the sesquiterpene lactone centratherin on mammalian cells in vitro and in vivo,” Teratogenesis, Carcinogenesis, and Mutagenesis, vol. 21, no. 6, pp. 383–393, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Mosmann, “Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays,” Journal of Immunological Methods, vol. 65, no. 1-2, pp. 55–63, 1983. View at Publisher · View at Google Scholar · View at Scopus
  26. T. M. Souza, D. F. Farias, B. M. Soares et al., “Toxicity of Brazilian plant seed extracts to two strains of Aedes aegypti (Diptera: Culicidae) and nontarget animals,” Journal of Medical Entomology, vol. 48, no. 4, pp. 846–851, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. P. D. L. Lima, D. S. Leite, M. C. Vasconcellos et al., “Genotoxic effects of aluminum chloride in cultured human lymphocytes treated in different phases of cell cycle,” Food and Chemical Toxicology, vol. 45, no. 7, pp. 1154–1159, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. M. P. Merker and L. Levine, “A protein from the marine mollusc Aplysia californica that is hemolytic and stimulates arachidonic acid metabolism in cultured mammalian cells,” Toxicon, vol. 24, no. 5, pp. 451–465, 1986. View at Publisher · View at Google Scholar · View at Scopus
  29. A. W. Bernheimer, “Assay of hemolytic toxins,” Methods in Enzymology, vol. 165, pp. 213–217, 1988. View at Publisher · View at Google Scholar · View at Scopus
  30. L. V. Costa-Lotufo, M. T. Khan, A. Ather et al., “Studies of the anticancer potential of plants used in Bangladeshi folk medicine,” Journal of Ethnopharmacology, vol. 13, pp. 21–30, 2005. View at Google Scholar
  31. D. J. Finney, Probit Analysis, Cambridge University Press, Cambridge, UK, 3rd edition, 1971. View at MathSciNet
  32. D. C. Hissa, I. M. Vasconcelos, A. F. U. Carvalho et al., “Novel surfactant proteins are involved in the structure and stability of foam nests from the frog Leptodactylus vastus,” Journal of Experimental Biology, vol. 211, no. 16, pp. 2707–2711, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. S. F. F. Ribeiro, A. P. Agizzioa, O. L. T. Machado et al., “A new peptide of melon seeds which shows sequence homology with vicilin: partial characterization and antifungal activity,” Scientia Horticulturae, vol. 111, pp. 399–405, 2007. View at Google Scholar
  34. G. C. G. Militão, I. N. F. Dantas, P. M. P. Ferreira et al., “In vitro and in vivo anticancer properties of cucurbitacin isolated from Cayaponia racemosa,” Pharmaceutical Biology, vol. 50, no. 12, pp. 1479–1487, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Shimada, Y. S. Kim, K. Miyamoto, M. Yoshioka, and H. Murata, “Effects of Bacillus thuringiensis Cry1Ab toxin on mammalian cells,” Journal of Veterinary Medical Science, vol. 65, no. 2, pp. 187–191, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. R. F. T. Corrêa, D. M. P. Ardisson-Araújo, R. G. Monnerat, and B. M. Ribeiro, “Cytotoxicity analysis of three Bacillus thuringiensis subsp. israelensisδ-endotoxins towards insect and mammalian cells,” PLoS ONE, vol. 7, no. 9, Article ID e46121, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. C. K. Grisolia, R. Oliveira, I. Domingues, E. C. Oliveira-Filho, R. G. Monerat, and A. M. V. M. Soares, “Genotoxic evaluation of different δ-endotoxins from Bacillus thuringiensis on zebrafish adults and development in early life stages,” Mutation Research, vol. 672, no. 2, pp. 119–123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Bravo, S. S. Gill, and M. Soberón, “Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control,” Toxicon, vol. 49, no. 4, pp. 423–435, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. G. D. Brand, J. R. S. A. Leite, L. P. Silva et al., “Dermaseptins from Phyllomedusa oreades and Phyllomedusa distincta: anti-Trypanosoma cruzi activity without cytotoxicity to mammalian cells,” The Journal of Biological Chemistry, vol. 277, no. 51, pp. 49332–49340, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. R. A. Acey, S. Bailey, P. Healy, C. Jo, T. F. Unger, and R. A. Hudson, “A butyrylcholinesterase in the early development of the brine shrimp (Artemia salina) larvae: a target for phthalate ester embryotoxicity?” Biochemical and Biophysical Research Communications, vol. 299, no. 4, pp. 659–662, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Favilla, L. Macchia, A. Gallo, and C. Altomare, “Toxicity assessment of metabolites of fungal biocontrol agents using two different (Artemia salina and Daphnia magna) invertebrate bioassays,” Food and Chemical Toxicology, vol. 44, no. 11, pp. 1922–1931, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. Z. A. Mohamed, “First report of toxic Cylindrospermopsis raciborskii and Raphidiopsis mediterranea (Cyanoprokaryota) in Egyptian fresh waters,” FEMS Microbiology Ecology, vol. 59, no. 3, pp. 749–761, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. K. R. Prihoda and J. R. Coats, “Aquatic fate and effects of Bacillus thuringiensis Cry3Bb1 protein: toward risk assessment,” Environmental Toxicology and Chemistry, vol. 27, no. 4, pp. 793–798, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. K. R. Prihoda and J. R. Coats, “Fate of Bacillus thuringiensis (Bt) Cry3Bb1 protein in a soil microcosm,” Chemosphere, vol. 73, no. 7, pp. 1102–1107, 2008. View at Publisher · View at Google Scholar · View at Scopus