Inter-laboratory comparison of Cry1Ab toxin quantification in MON 810 maize by enzyme-immunoassay

Food and Agricultural Immunology

Volumn 23, Issue 2, 2012, Pages 99-121

  Székács, András ^a   Weiss, Gabriele ^b   Quist, David ^c   Takács, Eszter ^a   Darvas, Béla ^a   Meier, Matthias ^b   Swain, Trilochan ^c   Hilbeck, Angelika ^b,d  

^a PLANT PROTECTION INSTITUTE   (Hungary)

^b Ecostrat GmbH   (Germany)

^c Genøk Center for Biosafety   (Norway)

^d ETH ZURICH   (Switzerland)

Author keywords

Bacillus thuringiensis; Cry1Ab toxin; ELISA; GM plants; MON 810

Indexed keywords

BACILLUS THURINGIENSIS; ZEA MAYS;

EID: 84861212362     PISSN: 09540105     EISSN: 14653443     Source Type: Journal    
DOI: 10.1080/09540105.2011.604773     Document Type: Article

References (82)

1. Adamczyk, J.J. Jr, Adam, L.C. and Hardee, D.D. 2001. Field efficacy and seasonal expression profiles for terminal leaves of single and double Bacillus thuringiensis toxin cotton genotypes. Journal of Economic Entomology, 94: 1589-1593.
2. Andrews, R.E., Bibilos, M.M. and Bulla, L.A. 1985. Protease activation of the entomocidal protoxin of Bacillus thuringiensis subsp kurstaki. Applied and Environmental Microbioliology, 50: 737-742.
3. Barton, K.A., & Miller, M.J. 1998. Expression of genes in plants. U.S. Patent 2001/0003849, 17 April 1998.
4. Baumgarte, S. and Tebbe, C.C. 2005. Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810) and its effect on bacterial communities in the maize rhizosphere. Molecular Ecology, 14: 2539-2551.
5. Bietlot, H., Carey, P.R., Choma, C., Kaplan, H., Lessard, T. and Pozsgay, M. 1989. Facile preparation and characterization of the toxin from Bacillus thuringiensis var. kurstaki. Biochemical Jornal, 260: 87-91.
6. Bravo, A., Gill, S.S. and Soberón, M. 2007. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon, 49: 423-435.
7. Bravo, A., Sanchez, J., Kouskoura, T. and Crickmore, N. 2002. N-terminal activation is an essential early step in the mechanism of action of the Bacillus thuringiensis Cry1Ac insecticidal toxin. Journal of Biological Chemistry, 277: 23985-23987.
8. Bruns, H.A. and Abel, C.A. 2003. Nitrogen fertility effects on Bt delta-endotoxin and nitrogen concentrations of maize during-early growth. Agronomy Journal, 95: 207-211.
9. Chen, M., Ye, G., Liu, Z., Fang, Q., Hu, C.Peng, Y. 2009. Analysis of Cry1Ab toxin bioaccumulation in a food chain of Bt rice, an herbivore and a predator. Ecotoxicology, 18: 230-238.
10. Chilcutt, C.F. and Tabashnik, B.E. 2004. Contamination of refuges by Bacillus thuringiensis toxin genes from transgenic maize. Proceedings of the National Academy of Sciences of the United States of America, 101: 7526-7529.
11. Choma, C.J. and Kaplan, H. 1990. Folding and unfolding of protoxin from Bacillus thuringiensis: Evidence that the toxic moiety is present in an active confirmation. Biochemistry, 29: 10971-10977.
12. Choma, C.J. and Kaplan, H. 1991. The toxic moiety of Bacillus thuringiensis protein undergoes a conformational change upon activation. Biochemical and Biophysical Research Communications, 179: 1934-1938.
13. Crespo, A.L.B., Spencer, T.A., Nekl, E., Pusztai-Carey, M., Moar, W.J. and Siegfried, B.D. 2008. Comparison and validation of methods to quantify Cry1Ab toxin from Bacillus thuringiensis for standardization of insect bioassays. Applied and Environmental Microbioliology, 74: 130-135.
14. De Maagd, R.A., Bosch, D. and Stiekema, W. 1999. Bacillus thuringiensis toxin mediated insect resistance in plants. Trends in Plant Science, 4: 9-13.
15. Dhillon, M.K. and Sharma, H.C. 2009. Effects of Bacillus thuringiensis delta-endotoxins Cry1Ab and Cry1Ac on the coccinellid beetle, Cheilomenes sexmaculatus (Coleoptera, Coccinellidae) under direct and indirect exposure conditions. Biocontrol Science and Technology, 19: 407-420.
16. Díaz-Mendoza, M., Farinós, G.P., Castañera, P., Hernández-Crespoand, P. and Ortego, F. 2007. Proteolytic processing of native Cry1Ab toxin by midgut extracts and purified trypsins from the Mediterranean corn borer Sesamia nonagrioides. Journal of Insect Physiology, 53: 428-435.
17. Dively, G.P., Rose, R., Sears, M.K., Hellmich, R.L., Stanley-Horn, D.E.Calvin, D.D. 2004. Effects on Monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Cry1Ab-expressing corn during anthesis. Environmental Entomology, 33: 1116-1125.
18. Douville, M., Gagne, F., Masson, L., McKay, J. and Blaise, C. 2005. Tracking the source of Bacillus thuringiensis Cry1Ab endotoxin in the environment. Biochemical Systematics and Ecology, 33: 219-232.
19. Ermolli, M., Fantozzi, A., Marini, M., Scotti, D., Balla, B.Hoffmann, S. 2006a. Food safety: screening tests used to detect and quantify GMO proteins. Accreditation and Quality Assurance, 11: 55-57.
20. Ermolli, M., Prospero, A., Balla, B., Querci, M., Mazzeo, A. and Van Den Eede, G. 2006b. Development of an innovative immunoassay for CP4EPSPS and Cry1AB genetically modified protein detection and quantification. Food Additives and Contaminants, 23: 876-882.
21. Ezequiel, M., Reggiardo, M.I., Vallejos, R.H. and Permingeat, H.R. 2006. Detection of BT transgenic maize in foodstuffs. Food Research International, 39: 250-255.
22. Fantozzi, A., Ermolli, M., Marini, M., Scotti, D., Balla, B.Querci, M. 2007. First application of a microsphere-based immunoassay to the detection of genetically modified organisms (GMOs): Quantification of Cry1Ab protein in genetically modified maize. Journal of Agricultural and Food Chemistry, 55: 1071-1076.
23. Gao, Y., Fancil, K.J., Xu, X., Schwedler, D.A., Gilbert, J.R. and Herman, R.A. 2006. Purification and characterization of a chimeric Cry1F delta-endotoxin expressed in transgenic cotton plants. Journal of Agricultural and Food Chemistry, 54: 829-835.
24. Gao, Y., Schafer, B.W., Collins, R.A., Herman, R.A., Xu, X.Gilbert, J.R. 2004. Characterization of Cry 34Ab1 and Cry35Ab1 insectcidal crystal proteins expressed in transgenic corn plants and Pseudomonas fluorescens. Journal of Agricultural and Food Chemistry, 52: 8057-8065.
25. Gill, S.S., Cowles, E.A. and Pietrantonio, P.V. 1992. The mode of action of Bacillus thuringiensis endotoxins. Annual Review of Entomology, 37: 615-636.
26. Gould, F. 1998. Sustainability of transgenic insecticidal cultivars: Integrating pest genetics and ecology. Annual Review of Entomology, 43: 701-726.
27. Gould, F. 2000. Testing Bt refuge strategies in the field. Nature Biotechnology, 18: 266-267.
28. Grothaus, G.D., Bandla, M., Currier, T., Giroux, R., Jenkins, G.R.Lipp, M. 2006. Immunoassay as an analytical tool in agricultural biotechnology. Journal of AOAC International, 89: 913-928.
29. Harwood, J.D., Wallin, W.G. and Obrycki, J.J. 2005. Uptake of Bt endotoxins by nontarget herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem. Molecular Ecology, 14(9): 2815-2823.
30. Hellmich, R.L., Siegfried, B.D., Sears, M.K., Stanley-Horn, D.E., Mattila, H.R.Spencer, T. 2001. Monarch larvae sensitivity to Bacillus thuringiensis purified proteins and pollen. Proceedings of the National Academy of Sciences of the United States of America, 98: 11925-11930.
31. Hilbeck, A., Baumgartner, M., Fried, P.M. and Bigler, F. 1998a. Effects of transgenic Bt corn-fed prey on immature development of Chrysoperla carnea (Neuroptera: Chrysopidae). Environmental Entomology, 27: 480-487.
32. Hilbeck, A., Moar, W., Pusztai-Carey, M., Filipini, A. and Bigler, F. 1998b. Toxicity of Bacillus thuringiensis Cry1Ab toxin to the predator Chrysoperla carnea (Neuroptera: Chrysopidae). Environmental Entomology, 27: 1255-1263.
33. Hilbeck, A., Moar, W., Pusztai-Carey, M., Filipini, A. and Bigler, F. 1999. Prey-mediated effects of Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysoperla carnea (Neuroptera: Chrysopidae). Entomologia Experimentalis et Applicata, 91: 305-316.
34. Hilbeck, A. and Schmidt, J.E.U. 2006. Another view on Bt proteins-How specific are they and what else might they do?. Biopesticides International, 2: 1-50.
35. Höfte, H. and Whiteley, H. 1989. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiological Reviews, 53: 242-255.
36. Huber-Lukac, M., Luthy, P. and Braun, D.G. 1983. Specificities of monoclonal antibodies against the activated delta-endotoxin of Bacillus thuringiensis var. thuringiensis. Infection and Immunity, 40: 608-612.
37. Icoz, I., Andow, D., Zwahlen, C. and Stotzky, G. 2009. Is the Cry1Ab protein from Bacillus thuringiensis (Bt) taken up by plants from soils previously planted with Bt corn and by carrot from hydroponic culture?. Bulletin of Environmental Contamination and Toxicology, 83: 48-58.
38. International Organization for Standardization. 1994. ISO 5725-4:1994 Accuracy (trueness and precision) of measurement methods and results. Part 4: Basic methods for the determination of the trueness of a standard measurement method (http://www.iso.org/iso/home.htm).
39. Kruger, M., van Rensburg, J.B.J. and van den Berg, J. 2009. Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa. Crop Protection, 28: 684-689.
40. Lambert, B., Buysse, L., Decock, C., Jansens, S., Piens, C.Saey, B. 1996. A Bacillus thuringiensis insecticidal crystal protein with a high activity against members of the family Noctuidae. Applied and Environmental Microbioliology, 62: 80-86.
41. Lang, A., Brunzel, S., Dolek, M., Otto, M. and Theißen, B. 2011. Modelling in the light of uncertainty of key parameters: a call to exercise caution in field predictions of Bt-maize effects. Proceedings of the Royal Society B, 278: 980-981.
42. Lipp, M., Anklam, E. and Stave, J.W. 2000. Validation of an immunoassay for detection and quantitation of genetically modified soybean in food and food fractions using reference materials: Interlaboratory study. Journal of AOAC International, 83: 919-927.
43. Liu, C.-M. and Tzeng, Y.M. 2001. Quantitative analysis of parasporal crystal protein from Bacillus thuringiensis by capillary electrophoresis. Journal of Food and Drug Analysis, 9: 79-83.
44. Lung, J.H.T., Male, K.B., Mazza, A., Masson, L. and Broussau, R. 2004. Analysis of insecticidal proteins from Bacillus thuringiensis and recombinant Escherichia coli by capillary electrokinetic chromatography. Electrophoresis, 25: 3292-3299.
45. Margarit, E., Reggiardo, M.I., Vallejos, R.H. and Permingeat, H.R. 2006. Detection of BT transgenic maize in foodstuffs. Food Research International, 39: 250-255.
46. Masson, L., Erlandson, M., Pusztai-Carey, M., Brousseau, R., Juarez-Perez, V. and Frutos, R. 1998. A holistic approach for determining the entomopathogenic potential of Bacillus thuringiensis strains. Applied and Environmental Microbioliology, 64: 4782-4788.
47. McGaughey, W.H., Gould, F. and Gelernter, W. 1998. Bt resistance management. Nature Biotechnology, 16: 144-146.
48. Mendelsohn, M., Kough, J., Zigfridais, V. and Matthewsm, K. 2003. Are Bt-crops safe?. Nature Biotechnology, 21: 1003-1009.
49. Milne, R. and Kaplan, H. 1993. Purification and characterization of a trypsin-like digestive enzyme from spruce budworm (Choristoneura fumiferana) responsible for the activation of Δ-endotoxin from Bacillus thuringiensis. Insect Biochemistry and Molecular Biology, 23: 663-673.
50. Miranda, R., Zamudio, F.Z. and Bravo, A. 2001. Processing of Cry1Ab delta endotoxin from Bacillus thuringiensis by Manduca sexta and Spodoptera frugiperda midgut proteases: Role in protoxin activation and toxin inactivation. Insect Biochemistry and Molecular Biology, 31: 1155-1163.
51. Mohan, M. and Gujar, G.T. 2003. Characterization and comparison of midgut proteases of Bacillus thuringiensis susceptible and resistant diamondback moth (Plutellidae: Lepidoptera). Journal of Invertebrate Pathology, 82: 1-11.
52. Monsanto. 2002. Safety assessment of YieldGard insect-protected event MON810. Published by agbios.com as Product Safety Description. Retrieved March 17, 2009, from http://agbios.com/docroot/decdocs/02-269-010.pdf
53. Nguyen, H.T., Hunfeld, H., Meissle, M., Miethling-Graff, R., Pagel-Wieder, S.Rauschen, S. 2008. Round robin quantitation of Cry3Bb1 using the qualitative PathoScreen ELISA. IOBC/WPRS Bulletin, 33: 59-66.
54. Nguyen, T.H. and Jehle, J.A. 2007. Quantitative analysis of the seasonal and tissue-specific expression of Cry1Ab in transgenic maize MON 810. Journal of Plant Diseases and Protection, 114: 82-87.
55. Nguyen, J. and Russel, S.C. 2010. Targeted proteomics approach to species-level identification of Bacillus thuringiensis spores by AP-MALDI-MS. Journal of the American Society for Mass Spectrometry, 21: 993-1001.
56. Oppert, B. 1999. Protease interactions with Bacillus thuringiensis insecticidal toxins. Archives of Insect Biochemistry and Physiology, 42: 1-12.
57. Park, H.W., Bideshi, D.K. and Federici, B.A. 2000. Molecular genetic manipulation of truncated Cry1C protein synthesis in Bacillus thuringiensis to improve stability and yield. Applied and Environmental Microbioliology, 66: 4449-4455.
58. Perry, J.N., Devos, Y., Arpaia, S., Bartsch, D., Gathmann, A.Hails, R.S. 2010. A mathematical model of exposure of nontarget Lepidoptera to Bt-maize pollen expressing Cry1Ab within Europe. Proceedings of the Royal Society B, 277: 1417-1425.
59. Pigott, C.R. and Ellar, D.J. 2007. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiology and Molecular Biology Reviews, 71: 255-281.
60. Ranasinghe, C. and Akhurst, J.R. 2002. Matrix assisted laser desorption ionisation time of flight mass spectrometry (MALDI-TOF MS) for detecting novel Bt toxins. Journal of Invertebrate Pathology, 79: 51-58.
61. Romeis, J., Meissle, M., Raybould, A. and Hellmich, R.L. 2009. "Impact of insect-resistant genetically modified crops on non-target arthropods". In Environmental impact of genetically modified crops, Edited by: Ferry, N. and Gatehouse, A.M.R. 165-198. Wallingford: CABI.
62. Schmidt, J.E.U., Braun, C.U., Whitehouse, L.P. and Hilbeck, A. 2008. Effects of activated Bt transgene products (Cry1Ab, Cry3Bb) on immature stages of the ladybird Adalia bipunctata in laboratory ecotoxicity testing. Archives of Environmental Contamination and Toxicology, 56: 221-228.
63. Schnepf, E., Crickmore, N., Van Rie, J., Lereclus, D., Baum, J.Feitelson, J. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiology and Molecular Biology Reviews, 62: 775-806.
64. Shao, Z., Cui, Y., Liu, X., Yi, H., Ji, J. and Yu, Z. 1998. Processing of delta-endotoxin of Bacillus thuringiensis subsp. kurstaki HD-1 in Heliothis armigera midgut juice and the effects of protease inhibitors. Journal of Invertebrate Pathology, 72: 73-81.
65. Shapiro, S.S. and Wilk, M.B. 1965. An analysis of variance test for normality. Biometrika, 52: 591-599.
66. Sims, S.R. and Berberich, S.A. 1996. Bacillus thuringiensis CryIA protein levels in raw and processed seed of transgenic cotton: Determination using insect bioassay and ELISA. Journal of Economic Entomology, 89: 247-251.
67. Soberón, A., Gill, S.S. and Bravo, A. 2009. Signaling versus punching hole: How do Bacillus thuringiensis toxins kill insect midgut cells?. Cellular and Molecular Life Sciences, 66: 1337-1349.
68. Stave, J.W. 1999. Detection of new or modified proteins in novel foods derived from GMO-future needs. Food Control, 10: 367-374.
69. Stave, J.W. 2002. Protein immunoassay methods or detection of biotech crops: Applications, limitations, and practical considerations. Journal of AOAC International, 85: 780-786.
70. Székács, A., Lauber, É., Juracsek, J. and Darvas, B. 2010a. Cry1Ab toxin production of MON 810 transgenic maize. Environmental Toxicology and Chemistry, 29: 182-190.
71. Székács, A., Lauber, É., Takács, E. and Darvas, B. 2010b. Detection of Cry1Ab toxin in the leaves of MON 810 transgenic maize. Analytical and Bioanalytical Chemistry, 396: 2203-2211.
72. Takahashi, Y., Hori, H., Furuno, H., Kawano, T., Takahashi, M. and Wada, Y. 1998. Enzyme-linked immunosorbent assays for rapid and quantitative detection of insecticidal crystal proteins of Bt pesticides. Journal of Pesticide Science, 23: 386-391.
73. Tapp, G. and Stotzky, G. 1995. Dot blot enzyme-linked immunosorbent assay for monitoring the fate of insecticidal toxins from Bacillus thuringiensis in soil. Applied and Environmental Microbioliology, 61: 602-609.
74. Then, C. 2010. Risk assessment of toxins derived from Bacillus thuringiensis-synergism, efficacy, and selectivity. Environmental Science and Pollution Research, 17: 791-797.
75. Then, C. and Lorch, A. 2008. "A simple question in a complex environment: How much Bt toxin do genetically engineered MON810 maize plants actually produce?". In Implications of GM-crop cultivation at large spatial scales. Theorie in der Ökologie: Vol. 14, Edited by: Breckling, B., Reuter, H. and Verhoeven, R. 17-21. Frankfurt: Peter Lang.
76. Volpe, G., Ammid, N.H., Moscone, D., Occhigrossi, L. and Palleschi, G. 2006. Development of an immunomagnetic electrochemical sensor for detection of BT-CRY1AB/CRY1AC proteins in genetically modified corn samples. Analytical Letters, 39: 1599-1609.
77. Walschus, U., Witt, S. and Wittmann, C. 2002. Development of monoclonal antibodies against Cry1Ab protein from Bacillus thuringiensis and their application in an ELISA for detection of transgenic Bt-maize. Food and Agricultural Immunology, 14: 231-240.
78. Wang, S., Guo, A.Y., Zheng, W.J., Zhang, Y., Qiao, H. and Kennedy, I.R. 2007. Development of ELISA for the determination of transgenic Bt-cottons using antibodies against Cry1Ac protein from Bacillus thuringiensis HD-73. Engineering in Life Sciences, 7: 149-154.
79. Wu, Z.P., Xu, B.J. and Chen, Z.Y. 2001. Separation and purification of Bacillus thuringiensis (Bt) toxic protein Cry1Ab from transgenic rice by ion-exchange chromatography. Chromatogarphia, 53: 571-573.
80. Xie, X. and Shu, Q. 2001. Studies on rapid quantitative analysis of Bt toxin by using Envirologix kits in transgenic rice. Scientia Agricultura Sinica, 34: 465-468.
81. Yamamoto, T. 1983. Identification of entomocidal toxins of Bacillus thuringiensis by high performance liquid chromatography. Journal of General Microbiology, 129: 2595-2603.
82. Zwahlen, C., Hilbeck, A., Gugerli, P. and Nentwig, W. 2003. Degradation of the Cry1Ab protein within transgenic Bacillus thuringiensis corn tissue in the fields. Molecular Ecology, 12: 765-775.