Binding sites for Bacillus thuringiensis Cry2Ae toxin on heliothine brush border membrane vesicles are not shared with Cry1A, Cry1F, or Vip3A toxin

Applied and Environmental Microbiology

Volumn 77, Issue 10, 2011, Pages 3182-3188

  Gouffon, C ^a   Van Vliet, A ^b   Van Rie, J ^b   Jansens, S ^b   Jurat Fuentes, J L ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b Bayer sa nv Belgium   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS THURINGIENSIS; BRUSH BORDER MEMBRANE VESICLES; BT TOXIN; CHROMATOGRAPHIC PURIFICATION; DATA SUPPORT; EFFICIENT STRATEGY; HELICOVERPA ARMIGERA; HELIOTHIS VIRESCENS; INDEPENDENT MODE; INSECT COLONIES; INSECT RESISTANCE; REDUCING CONDITIONS; SPECIFIC BINDING; TARGET INSECT; TOXIN BINDING;

BACILLI; BACTERIOLOGY; BRUSHES; CELL MEMBRANES; CHROMATOGRAPHIC ANALYSIS; INSECT CONTROL; METABOLITES; POSITIVE IONS; TOXIC MATERIALS;

BINDING SITES;

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS;

BACTERIUM; BIOASSAY; CHROMATOGRAPHY; DATA SET; LABORATORY METHOD; LARVA; MEMBRANE; MOTH; PEST CONTROL; TOXIN;

ANIMAL; ARTICLE; BINDING SITE; DRUG EFFECT; LEPIDOPTERA; METABOLISM; MICROVILLUS; PROTEIN BINDING; TRANSPORT VESICLE;

ANIMALS; BACTERIAL PROTEINS; BINDING SITES; ENDOTOXINS; HEMOLYSIN PROTEINS; LEPIDOPTERA; MICROVILLI; PROTEIN BINDING; TRANSPORT VESICLES;

BACILLUS THURINGIENSIS; HELICOVERPA ARMIGERA; HELICOVERPA ZEA; HELIOTHIS VIRESCENS; HEXAPODA;

EID: 79958196767     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02791-10     Document Type: Article

References (48)

1. Ali, M. I., and R. G. Luttrell. 2007. Susceptibility of bollworm and tobacco budworm (Lepidoptera: Noctuidae) to Cry2Ab2 insecticidal protein. J. Econ. Entomol. 100:921-931.
2. Betz, F. S., B. G. Hammond, and R. L. Fuchs. 2000. Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. Regul. Toxicol. Pharmacol. 32:156-173.
3. Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
4. Caccia, S., et al. 2010. Binding site alteration is responsible for field-isolated resistance to Bacillus thuringiensis Cry2A insecticidal proteins in two Helicoverpa species. PLoS One 5:e9975.
5. Chitkowski, R. L., S. G. Turnipseed, M. J. Sullivan, and W. C. Bridges, Jr. 2003. Field and laboratory evaluations of transgenic cottons expressing one or two Bacillus thuringiensis var. kurstaki Berliner proteins for management of noctuid (Lepidoptera) pests. J. Econ. Entomol. 96:755-762.
6. Clive, J. 2009. Global status of commercialized biotech/GM crops: 2009. ISAAA brief no. 41. ISAAA, Ithaca, NY.
7. Convents, D., C. Houssier, I. Lasters, and M. Lauwereys. 1990. The Bacillus thuringiensis d-endotoxin: evidence for a two domain structure of the minimal toxic fragment. J. Biol. Chem. 265:1369-1375.
8. Crickmore, N., and D. J. Ellar. 1992. Involvement of a possible chaperonin in the efficient expression of a cloned CryIIA delta-endotoxin gene in Bacillus thuringiensis. Mol. Microbiol. 6:1533-1537.
9. Crickmore, N., et al. 2010. Bacillus thuringiensis toxin nomenclature. http://www.lifesci.sussex.ac.uk/Home/Neil_Crickmore/Bt/. Accessed 24 November 2010.
10. Dankocsik, C., W. P. Donovan, and C. S. Jany. 1990. Activation of a cryptic crystal protein gene of Bacillus thuringiensis subspecies kurstaki by gene fusion and determination of the crystal protein insecticidal specificity. Mol. Microbiol. 4:2087-2094.
11. de Maagd, R. A., M. Weemen-Hendriks, W. Stiekema, and D. Bosch. 2000. Bacillus thuringiensis delta-endotoxin Cry1C domain III can function as a specificity determinant for Spodoptera exigua in different, but not all, Cry1-Cry1C hybrids. Appl. Environ. Microbiol. 66:1559-1563.
12. English, L., et al. 1994. Mode of action of CryIIA: a Bacillus thuringiensis delta-endotoxin. Insect Biochem. Mol. Biol. 24:1025-1035.
13. Estela, A., B. Escriche, and J. Ferre. 2004. Interaction of Bacillus thuringiensis toxins with larval midgut binding sites of Helicoverpa armigera (Lepidoptera: Noctuidae). Appl. Environ. Microbiol. 70:1378-1384.
14. Estruch, J. J., et al. 1996. Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. Proc. Natl. Acad. Sci. U. S. A. 93:5389-5394.
15. Ferre, J., and J. Van Rie. 2002. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 47:501-533.
16. Garczynski, S. F., J. W. Crim, and M. J. Adang. 1991. Identification of putative insect brush border membrane-binding molecules specific to Bacillus thuringiensis delta-endotoxin by protein blot analysis. Appl. Environ. Microbiol. 57:2816-2820.
17. Hernandez, C. S., and J. Ferre. 2005. Common receptor for Bacillus thuringiensis toxins Cry1Ac, Cry1Fa, and Cry1Ja in Helicoverpa armigera, Helicoverpa zea, and Spodoptera exigua. Appl. Environ. Microbiol. 71:5627-5629.
18. Hernandez-Rodriguez, C. S., A. Van Vliet, N. Bautsoens, J. Van Rie, and J. Ferre. 2008. Specific binding of Bacillus thuringiensis Cry2A insecticidal proteins to a common site in the midgut of Helicoverpa species. Appl. Environ. Microbiol. 74:7654-7659.
19. Hofmann, C., et al. 1988. Specificity of Bacillus thuringiensis δ-endotoxins is correlated with the presence of high-affinity binding sites in the brush border membrane of target insect midguts. Proc. Natl. Acad. Sci. U. S. A. 85:7844-7848.
20. Hunter, W., and F. Greenwood. 1962. Preparation of iodine-131 labelled human growth hormone of high specific activity. Nature 194:495-496.
21. Jackson, R. E., M. A. Marcus, F. Gould, J. R. Bradley, Jr., and J. W. Van Duyn. 2007. Cross-resistance responses of Cry1Ac-selected Heliothis virescens (Lepidoptera: Noctuidae) to the Bacillus thuringiensis protein Vip3A. J. Econ. Entomol. 100:180-186.
22. Jimenez-Juarez, N., et al. 2007. Bacillus thuringiensis Cry1Ab mutants affecting oligomer formation are non-toxic to Manduca sexta larvae. J. Biol. Chem. 282:21222-21229.
23. Jurat-Fuentes, J. L., and M. J. Adang. 2004. Characterization of a Cry1Acreceptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. Eur. J. Biochem. 271:3127-3135.
24. Jurat-Fuentes, J. L., and M. J. Adang. 2001. Importance of Cry1 deltaendotoxin domain II loops for binding specificity in Heliothis virescens (L.). Appl. Environ. Microbiol. 67:323-329.
25. Jurat-Fuentes, J. L., F. L. Gould, and M. J. Adang. 2003. Dual resistance to Bacillus thuringiensis Cry1Ac and Cry2Aa toxins in Heliothis virescens suggests multiple mechanisms of resistance. Appl. Environ. Microbiol. 69:5898-5906.
26. Karim, S., and D. H. Dean. 2000. Pesticidal and receptor binding properties of Bacillus thuringiensis Cry1Ab and Cry1Ac delta-endotoxin mutants to Pectinophora gossypiella and Helicoverpa zea. Curr. Microbiol. 41:430-440.
27. Karim, S., S. Riazzudin, F. Gould, and D. H. Dean. 2000. Determination of receptor binding properties of Bacillus thuringiensis delta-endotoxins to cotton bollworm (Helicoverpa zea) and pink bollworm (Pectinophora gossypiella) midgut brush border membrane vesicles. Pestic. Biochem. Physiol. 67:198-216.
28. Koziel, M. G., et al. 1993. Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Bio/ Technology 11:194-200.
29. Lee, M. K., P. Miles, and J. S. Chen. 2006. Brush border membrane binding properties of Bacillus thuringiensis Vip3A toxin to Heliothis virescens and Helicoverpa zea midguts. Biochem. Biophys. Res. Commun. 339:1043-1047.
30. Liang, Y., S. S. Patel, and D. H. Dean. 1995. Irreversible binding kinetics of Bacillus thuringiensis CryIA delta-endotoxins to gypsy moth brush border membrane vesicles is directly correlated to toxicity. J. Biol. Chem. 270: 24719-24724.
31. Luo, K., and M. J. Adang. 1994. Removal of adsorbed toxin fragments that modify Bacillus thuringiensis CryIC d-endotoxin iodination and binding by sodium dodecyl sulfate treatment and renaturation. Appl. Environ. Microbiol. 60:2905-2910.
32. Pardo-Lopez, L., et al. 2006. Structural changes of the Cry1Ac oligomeric pre-pore from Bacillus thuringiensis induced by N-acetylgalactosamine facilitates toxin membrane insertion. Biochemistry 45:10329-10336.
33. Perlak, F. J., et al. 2001. Development and commercial use of Bollgard cotton in the U. S. A.-early promises versus today's reality. Plant J. 27:489-501.
34. Roush, R. T. 1998. Two-toxins strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Philos. Trans. R. Soc. Lond. B. Biol. Sci. 353:1777-1786.
35. Sena, J. A., C. S. Hernandez-Rodriguez, and J. Ferre. 2009. Interaction of Bacillus thuringiensis Cry1 and Vip3A proteins with Spodoptera frugiperda midgut binding sites. Appl. Environ. Microbiol. 75:2236-2237.
36. Siqueira, H. A., D. Moellenbeck, T. Spencer, and B. D. Siegfried. 2004. Cross-resistance of Cry1Ab-selected Ostrinia nubilalis (Lepidoptera: Crambidae) to Bacillus thuringiensis delta-endotoxins. J. Econ. Entomol. 97:1049-1057.
37. Sivasupramaniam, S., et al. 2008. Toxicity and characterization of cotton expressing Bacillus thuringiensis Cry1Ac and Cry2Ab2 proteins for control of lepidopteran pests. J. Econ. Entomol. 101:546-554.
38. Soberon, M., S. S. Gill, and A. Bravo. 2009. Signaling versus punching hole: how do Bacillus thuringiensis toxins kill insect midgut cells? Cell. Mol. Life Sci. 66:1337-1349.
39. Stewart, S. D., J. J. Adamczyk, Jr., K. S. Knighten, and F. M. Davis. 2001. Impact of Bt cottons expressing one or two insecticidal proteins of Bacillus thuringiensis Berliner on growth and survival of noctuid (Lepidoptera) larvae. J. Econ. Entomol. 94:752-760.
40. Tabashnik, B. E., et al. 2002. Control of resistant pink bollworm (Pectinophora gossypiella) by transgenic cotton that produces Bacillus thuringiensis toxin Cry2Ab. Appl. Environ. Microbiol. 68:3790-3794.
41. Terra, W. R., and C. Ferreira. 1994. Insect digestive enzymes: properties, compartmentalization and function. Comp. Biochem. Physiol. 109B:1-62.
42. Vanderzant, E. S., S. W. Fort, and C. D. Richardson. 1962. Rearing of bollworm on artificial diet. J. Econ. Entomol. 55:140.
43. Van Rie, J., S. Jansens, H. Hofte, D. Degheele, and H. Van Mellaert. 1990. Receptors on the brush border membrane of the insect midgut as determinants of the specificity of Bacillus thuringiensis delta-endotoxins. Appl. Environ. Microbiol. 56:1378-1385.
44. Van Rie, J., S. Jansens, H. Höfte, D. Degheele, and H. Van Mellaert. 1989. Specificity of Bacillus thuringiensis delta-endotoxins. Importance of specific receptors on the brush border membrane of the mid-gut of target insects. Eur. J. Biochem. 186:239-247.
45. Wolfersberger, M. G., et al. 1987. Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly (Pieris brassicae). Comp. Biochem. Physiol. 86A:301-308.
46. Wu, S.-J., and D. H. Dean. 1996. Functional significance of loops in the receptor binding domain of Bacillus thuringiensis CryIIIA d-endotoxin. J. Mol. Biol. 255:628-640.
47. Zhang, X., M. Candas, N. B. Griko, R. Taussig, and L. A. Bulla, Jr. 2006. A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc. Natl. Acad. Sci. U. S. A. 103:9897-9902.
48. Zhao, J. Z., et al. 2003. Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat. Biotechnol. 21:1493-1497.