An engineered chymotrypsin/cathepsin G site in domain I renders Bacillus thuringiensis Cry3A active against western corn rootworm larvae

Applied and Environmental Microbiology

Volumn 74, Issue 2, 2008, Pages 367-374

  Walters, Frederick S ^a   Stacy, Cheryl M ^a   Mi, Kyong Lee ^a   Palekar, Narendra ^a   Chen, Jeng S ^a  

^a SYNGENTA BIOTECHNOLOGY INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MIDGUT CELLS; ROOTWORM LARVAE;

BINDING SITES; CELLS; ENZYMES; PESTICIDES;

BACTERIA;

CATHEPSIN G; CHYMOTRYPSIN; CRY3A TOXIN; FUNGAL PROTEIN; PESTICIDE; PROTEIN MCRY3A; UNCLASSIFIED DRUG;

BACTERIUM; BEETLE; ENZYME; LARVA; MAIZE; PEST CONTROL; PEST SPECIES; TOXIN;

ALPHA HELIX; ARTICLE; BACILLUS THURINGIENSIS; BRUSH BORDER; CARBOXY TERMINAL SEQUENCE; COLEOPTERA; CORN; CRY3A GENE; ENZYME ACTIVE SITE; ENZYME ENGINEERING; FUNGAL GENE; IN VITRO STUDY; IN VIVO STUDY; LARVAL DEVELOPMENT; NONHUMAN; POINT MUTATION; PROTEIN DOMAIN; PROTEIN MODIFICATION; SENSITIVITY ANALYSIS; STRAIN IDENTIFICATION; UNITED STATES; WESTERN CORN ROOTWORM;

AMINO ACID SEQUENCE; ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BEETLES; CATHEPSINS; CHYMOTRYPSIN; CLONING, MOLECULAR; ENDOTOXINS; LARVA; MICROVILLI; MOLECULAR SEQUENCE DATA; MUTATION; PEST CONTROL, BIOLOGICAL; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; SERINE ENDOPEPTIDASES; ZEA MAYS;

NORTH AMERICA; UNITED STATES;

BACILLUS THURINGIENSIS; COLEOPTERA; DIABROTICA VIRGIFERA VIRGIFERA; ZEA MAYS;

EID: 38349116495     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02165-07     Document Type: Article

References (58)

1. Arantes, O., and D. Lereclus. 1991. Construction of cloning vectors for Bacillus thuringiensis. Gene 108:115-119.
2. Barrett, A. J., N. D. Rawlings, and J. F. Woessner. 1998. Handbook of proteolytic enzymes. Academic Press, New York, NY.
3. Bauer, L. S. 1990. Response of the cottonwood leaf beetle (Coleoptera: Chrysomelidae) to Bacillus thuringiensis var. san diego. Environ. Entomol. 19:428-431.
4. Baum, J. A., C.-R. Chu, M. Rupar, G. R. Brown, W. P. Donovan, J. E. Huesing, O. Ilagan, T. M. Malvar, M. Pleau, M. Walters, and T. Vaughn. 2004. Binary toxins from Bacillus thuringiensis active against the western corn rootworm, Diabrotica virgifera virgifera LeConte. Appl. Environ. Microbiol. 70:4889-4898.
5. 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.
6. Bown, D. P., H. S. Wilkinson, M. A. Jongsma, and J. A. Gatehouse. 2004. Characterisation of cysteine proteinases responsible for digestive proteolysis in guts of larval western corn rootworm (Diabrotica virgifera) by expression in the yeast Pichia pastoris. Insect Biochem. Mol. Biol. 34:305-320.
7. Carroll, J., D. Convents, J. Van Damme, A. Boets, J. Van Rie, and D. J. Ellar. 1997. Intramolecular proteolytic cleavage of Bacillus thuringiensis Cry3A δ-endotoxin may facilitate its coleopteran toxicity. J. Invertebr. Pathol. 70:41-49.
8. Carroll, J., J. Li, and D. J. Ellar. 1989. Proteolytic processing of a coleopteran-specific δ-endotoxin produced by Bacillus thuringiensis var. tenebrionis. Biochem. J. 261:99-105.
9. Chen, E., and C. Stacy. April 2006. Modified Cry3A toxins and nucleic acid sequences coding therefor. U.S. patent 7,030,295.
10. Christeller, J. T., B. D. Shaw, S. E. Gardiner, and J. Dymock. 1989. Partial purification and characterization of the major midgut proteases of grass grub larvae (Costelytra zealandica, Coleoptera: Scarabaeidae). Insect Biochem. 19:221-231.
11. Colepicolo-Neto, P., E. J. H. Bechara, C. Ferreira, and W. R. Terra. 1987. Digestive enzymes in close and distant genera of a same family: properties of midgut hydrolases from luminescent Pyrophorus divergens (Coleoptera: Elateridae) larvae. Comp. Biochem. Physiol. 87:755-759.
12. Coombs, J. J., D. S. Douches, W. B. Li, E. J. Grafius, and W. L. Pett. 2003. Field evaluation of natural, engineered, and combined resistance mechanisms in potato for control of Colorado potato beetle. J. Am. Soc. Hortic. Sci. 128:219-224.
13. Donovan, W. P., J. M. Gonzalez, Jr., M. P. Gilbert, and C. Dankocsik. 1988. Isolation and characterization of EG2158, a new strain of Bacillus thuringiensis toxic to coleopteran larvae, and nucleotide sequence of the toxin gene. Mol. Gen. Genet. 214:365-372.
14. Fabrick, J., C. Behnke, T. Czapla, K. Bala, A. G. Rao, K. J. Kramer, and G. R. Reeck. 2002. Effects of a potato cysteine proteinase inhibitor on midgut proteolytic enzyme activity and growth of the southern corn rootworm, Diabrotica undecempunctata howardi (Coleoptera: Chrysomelidae). Insect Biochem. Mol. Biol. 32:405-415.
15. Finney, D. J. 1971. Probit analysis. Cambridge University Press, Cambridge, England.
16. Génissel, A., J.-C. Leplé, N. Millet, S. Augustin, L. Jouanin, and G. Pilate. 2003. High tolerance against Chrsomela tremulae of transgenic poplar plants expressing a synthetic cry3Aa gene from Bacillus thuringiensis ssp. tenebrionis. Mol. Breed. 11:103-110.
17. Gillikin, J. W., S. Bevilacqua, and J. S. Graham. 1992. Partial characterization of digestive tract proteinases from western corn rootworm larvae, Diabrotica virgifera. Arch. Insect Biochem. Physiol. 19:285-298.
18. Godfrey, L. D., L. J. Meinke, and R. J. Wright. 1993. Field corn vegetative and reproductive biomass accumulation: response to western corn rootworm (Coleoptera: Chrysomelidae) root injury. J. Econ. Entomol. 86:1557-1573.
19. Hernández, C. A., M. Pujol, J. Alfonso-Rubí, R. Armas, Y. Coll, M. Pérez, A. González, M. Ruiz, P. Castañera, and F. Ortego. 2003. Proteolytic gut activities in the rice water weevil, Lissorhoptrus brevirostris Suffrian (Coleoptera: Curculionidae). Arch. Insect Biochem. Physiol. 53:19-29.
20. Herrnstadt, C., G. G. Soares, E. R. Wilcox, and D. L. Edwards. 1986. A new strain of Bacillus thuringiensis with activity against coleopteran insects. Bio/Technology 4:305-308.
21. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
22. Koller, C. N., L. S. Bauer, and R. M. Hollingworth. 1992. Characterization of the pH-mediated solubility of Bacillus thuringiensis var. san diego native δ-endotoxin crystals. Biochem. Biophys. Res. Commun. 184:692-699.
23. Krieg, V. A., A. M. Huger, G. A. Langenbruch, and W. Schnetter. 1984. New results on Bacillus thuringiensis var. tenebrionis with special regard to its effect on the Colorado beetle. Anz. Schaedlkd. Pflanzenschutz Umweltschutz 57:145-150.
24. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
25. Lee, M. K., R. E. Milne, A. Z. Ge, and D. H. Dean. 1992. Location of a Bombyx mori receptor binding region on a Bacillus thuringiensis δ-endotoxin. J. Biol. Chem. 267:3115-3121.
26. Li, J., J. Caroll, and D. J. Ellar. 1991. Crystal structure of insecticidal δ-endotoxin from Bacillus thuringiensis at 2.5 Å resolution. Nature 353:815-821.
27. Lightwood, D. J., D. J. Ellar, and P. Jarrett. 2000. Role of proteolysis in determining potency of Bacillus thuringiensis Cry1Ac δ-endotoxin. Appl. Environ. Microbiol. 66:5174-5181.
28. Loseva, O., M. Ibrahim, M. Candas, C. N. Koller, L. S. Bauer, and L. A. Bulla, Jr. 2002. Changes in protease activity and Cry3Aa toxin binding in the Colorado potato beetle: implications for insect resistance to Bacillus thuringiensis toxins. Insect Biochem. Mol. Biol. 32:567-577.
29. Macaluso, A., and A. M. Mettus. 1991. Efficient transformation of Bacillus thuringiensis requires nonmethylated plasmid DNA. J. Bacteriol. 173:1353-1356.
30. MacIntosh, S. C., T. B. Stone, S. R. Sims, P. L. Hunst, J. T. Greenplate, P. G. Marrone, F. J. Perlak, D. A. Fischoff, and R. L. Fuchs. 1990. Specificity and efficacy of purified Bacillus thuringiensis proteins against agronomically important insects. J. Invertebr. Pathol. 56:258-266.
31. Marrone, P. G., F. D. Ferri, T. R. Mosley, and L. J. Meinke. 1985. Improvements in laboratory rearing of the southern corn rootworm, Diabrotica undecimpuncta howardi Barber (Coleoptera: Chrysomelidae), on an artificial diet and corn. J. Econ. Entomol. 78:290-293.
32. Martin, M. M., and J. S. Martin. 1984. Surfactants: their role in preventing the precipitation of proteins by tannins in insect guts. Oecologia 61:342-345.
33. Martinez-Ramirez, A. C., and M. D. Real. 1996. Proteolytic processing of Bacillus thuringiensis CryIIIA toxin and specific binding to brush-border membrane vesicles of Leptinotarsa decemlineata (Colorado potato beetle). Pestic. Biochem. Physiol. 54:115-122.
34. McPherson, S. A., F. J. Perlak, R. L. Fuchs, P. G. Marrone, P. B. Lavrik, and D. Fischoff. 1988. Characterization of the coleopteran-specific protein gene of Bacillus thuringiensis var. tenebrionis. Bio/Technology 6:61-66.
35. Metcalf, R. L. 1986. Foreword, p. vii-xv. In J. L. Krysan and T. A. Miller (ed.), Methods for the study of the pest Diabrotica. Springer-Verlag, New York, NY.
36. Moellenbeck, D. J., M. L. Peters, J. W. Bing, J. R. Rouse, L. S. Higgins, L. Sims, T. Nevshemal, L. Marshall, R. T. Ellis, P. G. Bystrak, B. A. Lang, J. L. Stewart, K. Kouba, V. Sondag, V. Gustafson, K. Nour, D. Xu, J. Swenson, J. Zhang, T. Czapla, G. Schwab, S. Jayne, B. A. Stockhoff, K. Narva, H. E. Schnepf, S. J. Stelman, C. Poutre, M. Koziel, and N. Duck. 2001. Insecticidal proteins from Bacillus thuringiensis protect corn from corn rootworms. Nat. Biotechnol. 19:668-672.
37. Mullis, K. B., and F. A. Faloona. 1987. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 155:335-350.
38. Murdock, L. L., G. Brookhart, P. E. Dunn, D. E. Foard, S. Kelley, L. Kitch, R. E. Shade, R. H. Shukle, and J. L. Wolfson. 1987. Cysteine digestive proteinases in Coleoptera. Comp. Biochem. Physiol. 87B:783-787.
39. Murray, E. E., J. Lotzer, and M. Eberle. 1989. Codon usage in plant genes. Nucleic Acids Res. 17:477-498.
40. Novillo, C., P. Castañera, and F. Ortego. 1997. Characterization and distribution of chymotrypsin-like and other digestive proteases in Colorado potato beetle larvae. Arch. Insect Biochem. Physiol. 36:181-201.
41. Oehme, F. W., and J. A. Pickerell. 2003. Genetically engineered corn rootworm resistance: potential for reduction of human health effects from pesticides. Biomed. Environ. Sci. 16:17-28.
42. Oppert, B. 1999. Protease interactions with Bacillus thuringiensis insecticidal toxins. Arch. Insect Biochem. Physiol. 42:1-12.
43. Oppert, B., K. Hartzer, and M. Zuercher. 2002. Digestive proteinases in Lasioderma serricorne (Coleoptera:Anobiidae). Bull. Entomol. Res. 92:331-336.
44. Perlak, F. J., T. B. Stone, Y. M. Muskopf, L. J. Peterson, G. B. Parker, S. L. McPherson, J. Wyman, S. Love, G. Reed, D. Biever, and D. A. Fischoff. 1993. Genetically improved potatoes: protection from Colorado potato beetles. Plant Mol. Biol. 22:313-321.
45. Purcell, J. P., J. T. Greenplate, and R. D. Sammons. 1992. Examination of midgut luminal proteinase activities in six economically important insects. Insect Biochem. Mol. Biol. 22:41-47.
46. Rausell, C., I. García-Robles, J. Sánchez, C. Muñoz-Garay, A. C. Martínez-Ramírez, M. D. Real, and A. Bravo. 2004. Role of toxin activation on binding and pore formation activity of the Bacillus thuringiensis Cry3 toxins in membranes of Leptinotarsa decemlineata (Say). Biochim. Biophys. Acta 1660:99-105.
47. Schnepf, E., N. Crickmore, J. Van Rie, D. Lereclus, J. Baum, J. Feitelson, D. R. Ziegler, and D. H. Dean. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:775-806.
48. Schnepf, H. E., H. C. Wong, and H. R. Whiteley. 1985. The amino acid sequence of a crystal protein from Bacillus thuringiensis deduced from the DNA base sequence. J. Biol. Chem. 260:6264-6272.
49. Sekar, V., D. V. Thompson, M. J. Maroney, R. G. Bookland, and M. J. Adang. 1987. Molecular cloning and characterization of the insecticidal crystal protein gene of Bacillus thuringiensis var. tenebrionis. Proc. Natl. Acad. Sci. USA 84:7036-7040.
50. Shelton, A. M., J.-Z. Zhao, and R. T. Rousch. 2002. Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu. Rev. Entomol. 47:845-881.
51. Slaney, A. C., H. L. Robbins, and L. English. 1992. Mode of action of Bacillus thuringiensis toxin CryIIIA: an analysis of toxicity in Leptinotarsa decemlineata (Say) and Diabrotica undecempunctata Howardi Barber. Insect Biochem. Mol. Biol. 22:9-18.
52. Tanaka, T., Y. Minematsu, C. F. Reilly, J. Travis, and J. C. Powers. 1985. Human leukocyte cathepsin G. Subsite mapping with 4-nitroanilides, chemical modification, and effect of possible cofactors. Biochemistry 24:2040-2047.
53. Vaje, S., D. Mossakowski, and D. Gabel. 1984. Temporal, intra- and interspecific variation of proteolytic enzymes in carabid-beetles. Insect Biochem. 14:313-320.
54. Vaughn, T., T. Cavato, G. Brar, T. Coombe, T. DeGooyer, S. Ford, M. Groth, A. Howe, S. Johnson, K. Kolacz, C. Pilcher, J. Purcell, C. Romano, L. English, and J. Pershing. 2005. A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci. 45:931-938.
55. Von Tersch, M. A., S. L. Slatin, C. A. Kulesza, and L. H. English. 1994. Membrane-permeabilizing activities of Bacillus thuringiensis coleopteran-active toxin CryIIIB2 and CryIIIB2 domain I peptide. Appl. Environ. Microbiol. 60:3711-3717.
56. Walters, F. S., C. A. Kulesza, A. T. Phillips, and L. H. English. 1994. A stable oligomer of Bacillus thuringiensis delta-endotoxin, Cry IIIA. Insect Biochem. Mol. Biol. 24:963-968.
57. Wolfersberger, M., P. Luethy, A. Maurer, P. Parenti, F. V. Sacchi, B. Giordana, and G. M. Hanozet. 1987. Preparation of brush border membrane vesicles (BBMV) from larval lepidopteran midgut. Comp. Biochem. Physiol. 86A:301-308.
58. Zhu, Y.-C., and J. E. Baker. 2000. Molecular cloning and characterization of a midgut chymotrypsin-like enzyme from the lesser grain borer, Rhyzopertha dominica. Arch. Insect Biochem. Physiol. 43:173-184.