Food safety knowledge on the Bt mutant protein Cry8Ka5 employed in the development of coleopteran-resistant transgenic cotton plants

References

• Sanahuja G, Banakar R, Twyman RM, Capell T, Christou P. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotech J 2011; 9:283-300; http://dx.doi.org/10.1111/j.1467-7652.2011.00595.x
   PubMed Web of Science ®Google Scholar
• Vachon V, Laprade R, Schwartz JL. Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J Invertebr Pathol 2012; 111:1-12; PMID:22617276; http://dx.doi.org/10.1016/j.jip.2012.05.001
   PubMed Web of Science ®Google Scholar
• Bravo A, Gill SS, Soberón M. Mode of action of Bacillus thuringiensis: Cry and Cyt toxins and their potential for insect control. Toxicon 2007; 49:423-35; PMID:17198720; http://dx.doi.org/10.1016/j.toxicon.2006.11.022
   PubMed Web of Science ®Google Scholar
• Soberón M, Fernández LE, Pérez C, Gill SS, Bravo A. Mode of action of mosquitocidal Bacillus thuringiensis toxins. Toxicon v. 49, n. 5, p. 2007; 597-600; http://dx.doi.org/10.1016/j.toxicon.2006.11.008
   PubMed Web of Science ®Google Scholar
• Kumar S, Chandra A, Pandey KC. Bacillus thuringiensis (Bt) transgenic crop: an environment friendly insect-pest management strategy. J Environ Biol 2008; 29:641-53; PMID:19295059
   PubMed Web of Science ®Google Scholar
• Mendelsohn M, Kough J, Vaituzis Z, Matthews K. Are Bt crops safe? Nat Biotechnol 2003; 21:1003-9; PMID:12949561; http://dx.doi.org/10.1038/nbt0903-1003
   PubMed Web of Science ®Google Scholar
• Gatehouse AM, Ferry N, Edwards MG, Bell HA. Insect-resistant biotech crops and their impacts on beneficial arthropods. Philos Trans R Soc Lond B Biol Sci 2011; 12:1438-52; http://dx.doi.org/10.1098/rstb.2010.0330
   Web of Science ®Google Scholar
• Tabashnik BE. Evolution of resistance to Bacillus thuringiensis. Annu Rev Entomol 1994; 39:47-79; http://dx.doi.org/10.1146/annurev.en.39.010194.000403
   Web of Science ®Google Scholar
• Gould F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Ann Rev Entomol 1998; 43:701-26; http://dx.doi.org/10.1146/annurev.ento.43.1.701
   PubMed Web of Science ®Google Scholar
• Bagla P. Hardy cotton-munching pests are latest blow to GM crops. Science 2010; 327:14-39
   Web of Science ®Google Scholar
• Carriere Y, Crowder DW, Tabashnik BE. Evolutionary ecology of insect adaptation to Bt crops. Evol Appl 2010; 3:561-73; PMID:25567947; http://dx.doi.org/10.1111/j.1752-4571.2010.00129.x
   PubMed Web of Science ®Google Scholar
• Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, Bing JW, Huckaba RM. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 2010; 103:1031-8; PMID:20857709; http://dx.doi.org/10.1603/EC10040
   PubMed Web of Science ®Google Scholar
• Alcantara E, Estrada A, Alpuerto V, Head G. Monitoring Cry1Ab susceptibility in Asian corn borer (Lepidoptera: Crambidae) on Bt corn in the Philippines. Crop Prot 2011; 30:554-9; http://dx.doi.org/10.1016/j.cropro.2010.12.019
   Web of Science ®Google Scholar
• Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW. Field evolved resistance to Bt maize by western corn rootworm. PLoS One 2011; 6:e22629; PMID:21829470; http://dx.doi.org/10.1371/journal.pone.0022629
   PubMed Web of Science ®Google Scholar
• Zhang H, Yin W, Zhao J, Jin L, Yang Y, Wu S, Tabashnik BE, Wu Y. Early warning of cotton bollworm resistance associated with intensive planting of Bt cotton in China. PLoS One 2011; 6:e22874; PMID:21857961; http://dx.doi.org/10.1371/journal.pone.0022874
   PubMed Web of Science ®Google Scholar
• Wan P, Huang Y, Wu H, Huang M, Cong S, Tabashnik BE, Wu K. Increased frequency of pink bollworm resistance to Bt toxin Cry1Ac in China. PLoS ONE 2012; 7:e29975; PMID:22238687; http://dx.doi.org/10.1371/journal.pone.0029975
   PubMed Web of Science ®Google Scholar
• Tabashnik BE, Wu K, Wu Y. Early detection of field-evolved resistance to Bt cotton in China: cotton bollworm and pink bollworm. J Invertebr Pathol 2012; 110:301-6; PMID:22537835; http://dx.doi.org/10.1016/j.jip.2012.04.008
   PubMed Web of Science ®Google Scholar
• Brévault T, Prudent P, Vaissayre M, Carrière Y. Susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to Cry1Ac and Cry2Ab2 insecticidal proteins in four countries of the West African cotton belt. J Econ Entomol 2009; 102:2301-9; http://dx.doi.org/10.1603/029.102.0636
   PubMed Web of Science ®Google Scholar
• An J, Gao Y, Wu K, Gould F, Gao J, Shen Z, Lei C. Vip3Aa tolerance response of Helicoverpa armigera populations from a Cry1Ac cotton planting region. J Econ Entomol 2010; 103:2169-73; PMID:21309241; http://dx.doi.org/10.1603/EC10105
   PubMed Web of Science ®Google Scholar
• Marquez AM, Dias JM, Ribeiro BM. Screening and characterization of Bacillus thuringiensis isolates from Brazil for the presence of coleoptera-specific cry genes. Microbiol Res 2000; 154:355-62; PMID:10772158; http://dx.doi.org/10.1016/S0944-5013(00)80010-5
   PubMed Web of Science ®Google Scholar
• Grossi-de-Sa MF, Quezado de Magalhaes M, Silva MS, Silva SM, Dias SC, Nakasu EY, Brunetta PS, Oliveira GR, Neto OB, Sampaio de Oliveira R 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. J Biochem Mol Biol 2007; 30:773-82; http://dx.doi.org/10.5483/BMBRep.2007.40.5.773
   Google Scholar
• Martins EL, Praça LB, Dumas VF, Silva-Werneck JO, Sone EH, Waga IC, Berry C, Monnerat RG. Characterization of Bacillus thuringiensis isolates toxic to cotton boll weevil (Anthonomus grandis). Biol Control 2007: 40:65-68; http://dx.doi.org/10.1016/j.biocontrol.2006.09.009
   Web of Science ®Google Scholar
• Martins ES, Aguiar RW, Martins NF, Melatti VM, Falcão R, Gomes AC, Ribeiro BM, Monnerat RG. Recombinant Cry1Ia protein is highly toxic to cotton boll weevil (Anthonomus grandis Boheman) and fall armyworm (Spodoptera frugiperda). J Appl Microbiol 2008; 104:1363-71; PMID:18248369; http://dx.doi.org/10.1111/j.1365-2672.2007.03665.x
   PubMed Web of Science ®Google Scholar
• Nakasu EY, Firmino AA, Dias SC, Rocha TL, Ramos HB, Oliveira GR, Lucena W, Carlini CR, Grossi-de-Sá MF. Analysis of Cry8Ka5-binding proteins from Anthonomus grandis (Coleoptera: Curculionidae) midgut. J Invertebr Pathol 2010; 104:227-30; PMID:20144614; http://dx.doi.org/10.1016/j.jip.2010.01.012
   PubMed Web of Science ®Google Scholar
• Lucena WA, Pelegrini PB, Martins-de-Sa D, Fonseca FC, Gomes JE, Jr, de Macedo LL, da Silva MC, Oliveira RS, Grossi-de-Sa MF. Molecular approaches to improve the insecticidal activity of Bacillus thuringiensis Cry toxins. Toxins (Basel) 2014; 6:2393-423; PMID:25123558; http://dx.doi.org/10.3390/toxins6082393
   PubMed Web of Science ®Google Scholar
• Oliveira GR, Silva MC, Lucena WA, Nakasu EY, Firmino AA, Beneventi MA, Souza DS, Gomes JE, Jr, de Souza JD Jr, Rigden DJ et al. Improving Cry8Ka toxin activity towards the cotton boll weevil (Anthonomus grandis). BMC Biotechnol 2011; 9:85; http://dx.doi.org/10.1186/1472-6750-11-85
   Web of Science ®Google Scholar
• Oliveira GR. In vitro evolution of Cry molecules active against Anthonomus grandis and Spodoptera frugiperda [dissertation in Portuguese]. [Porto Alegre]: Federal University of Rio Grande do Sul; 2008. 97p
   Google Scholar
• Lira J, Beringer J, Burton S, Griffin S, Sheets J, Tan SY, Woosley A, Worden S, Narva KE. Insecticidal activity of Bacillus thuringiensis Cry1Bh1 against Ostrinia nubilalis (Hubner) (Lepidoptera: Crambidae) and other lepidopteran pests. Appl Environ Microbiol 2013; 79:7590-7; PMID:24077715; http://dx.doi.org/10.1128/AEM.01979-13
   PubMed Web of Science ®Google Scholar
• Palma L, Muñoz D, Berry C, Murillo J, de Escudero IR, Caballero P. Molecular and insecticidal characterization of a novel Cry-related protein from Bacillus thuringiensis toxic against Myzus persicae. Toxins (Basel) 2014; 6:3144-56; PMID:25384108; http://dx.doi.org/10.3390/toxins6113144
   PubMed Web of Science ®Google Scholar
• Zhao C, Jurat-Fuentes JL, Abdelgaffar HM, Pan H, Song F, Zhang J. Identification of a new cry1I-type gene as a candidate for gene Pyramiding in corn to control Ostrinia species larvae. Appl Environ Microbiol 2015: 81:3699-705; PMID:25795679; http://dx.doi.org/10.1128/AEM.00379-15
   PubMed Web of Science ®Google Scholar
• Codex Alimentarius. Foods derived from modern biotechnology [Internet]. Rome, Italy, Codex Alimentarius Commission, Joint FAO/WHO Food Standards Programme, Food and Agriculture Organization of the United Nations. Second Edition. 2009. [cited 2015 Jul 10] Available from: http://www.fao.org/docrep/011/a1554e/a1554e00.htm
   Google Scholar
• Goodman RE, Hefle SL, Taylor SL, van Ree R. Assessing genetically modified crops to minimize the risk of increased food allergy: a review. Int Arch Allergy Immunol 2005; 137:153-66; PMID:15947471; http://dx.doi.org/10.1159/000086314
   PubMed Web of Science ®Google Scholar
• Delaney B, Astwood JD, Cunny H, Conn RE, Herouet-Guicheney C, Macintosh S, Meyer LS, Privalle L, Gao Y, Mattsson J, et al. Evaluation of protein safety in the context of agricultural biotechnology. Food Chem Toxicol 2008; 46:S71-97; PMID:18348900; http://dx.doi.org/10.1016/j.fct.2008.01.045
   PubMed Web of Science ®Google Scholar
• Hammond BG, Koch MS. Bacillus thuringiensis biotechnology. 1st ed. Dordrecht: Springer; 2012. Chapter 16, A review of the food safety of Bt crops; p. 305-25
   Google Scholar
• Koch MS, Ward JM, Levine SL, Baum JA, Vicini JL, Hammond BG. The food and environmental safety of Bt crops. Front Plant Sci 2015; 6:283; PMID:25972882; http://dx.doi.org/10.3389/fpls.2015.00283
   PubMed Web of Science ®Google Scholar
• Martins WFS, Ayres CFJ, Lucena WA. Genetic diversity of Brazilian natural populations of Anthonomus grandis Boheman (Coleoptera: Curculionidae), the major cottonpest in the New World. Genet Mol Res 2007, 6:23-32; PMID:17299893
   PubMed Web of Science ®Google Scholar
• Farias DF, Viana MP, Oliveira GR, Santos VO, Pinto CE, Viana DA, Vasconcelos IM, Grossi-de-Sa MF, Carvalho AF. Food safety assessment of Cry8Ka5 mutant protein using Cry1Ac as a control Bt protein. Food Chem Toxicol 2015; 81:81-91; PMID:25890087; http://dx.doi.org/10.1016/j.fct.2015.04.008
   PubMed Web of Science ®Google Scholar
• Xu W, Cao S, He X, Luo Y, Guo X, Yuan Y, Huang K. Safety assessment of Cry1Ab/Ac fusion protein. Food Chem Toxicol 2009; 47:59-65
   Web of Science ®Google Scholar
• CAO S, He X, Xu W, Ran W, Liang L, Luo Y, Yuan Y, Zhang N, Zhou X, Huang K. Safety assessment of Cry1C protein from genetically modified rice according to the national standards of PR China for a new food resource. Regul Toxicol Pharmacol 2010; 58:474-81; PMID:20801181; http://dx.doi.org/10.1016/j.yrtph.2010.08.018
   PubMed Web of Science ®Google Scholar
• EPA. Biopesticide Registration Action Document. Bacillus thuringiensis Cry1A.105 and Cry2Ab2 Insecticidal Proteins and the Genetic Material Necessary for Their Production in Corn [PC Codes 006515 (Cry2Ab2), 006514 (Cry1A.105)]. Washington, DC: US. Environmental Protection Agency, Office of Pesticide Programs, Biopesticides and Pollution Prevention Division. 2010 [cited 2015 Jul 10]. Available from: http://www.epa.gov/oppbppd1/biopesticides/pips/mon-89034-brad.pdf
   Google Scholar
• Farias DF, Viana MP, de Oliveira GR, Beneventi MA, Soares BM, Pessoa C, Pessoa IP, Silva LP, Vasconcelos IM, de Sá MF et al. Evaluation of cytotoxic and antimicrobial effects of two Bt Cry proteins on a GMO safety perspective. Biomed Res Int. 2014; 2014:810490; PMID:25165717; http://dx.doi.org/10.1155/2014/810490
   PubMed Web of Science ®Google Scholar
• Grisolia CK, Oliveira R, Domingues I, Oliveira-Filho EC, Monerat RG, Soares AM. Genotoxic evaluation of different delta-endotoxins from Bacillus thuringiensis on zebrafish adults and development in early life stages. Mutat Res 2009; 31:119-23; http://dx.doi.org/10.1016/j.mrgentox.2008.10.017
   Web of Science ®Google Scholar
• Yudina TG, Brioukhanov AL, Zalunin IA, Revina LP, Shestakov AI, Voyushina NE, Chestukhina GG, Netrusov AI. Antimicrobial activity of different proteins and their fragments from Bacillus thuringiensis parasporal crystals against clostridia and archaea. Anaerobe 2007; 13:6-13; PMID:17126041; http://dx.doi.org/10.1016/j.anaerobe.2006.09.006
   PubMed Web of Science ®Google Scholar