Measurements of Cry1F binding and activity of luminal gut proteases in susceptible and Cry1F resistant Ostrinia nubilalis larvae (Lepidoptera: Crambidae)

Journal of Invertebrate Pathology

Volumn 103, Issue 1, 2010, Pages 1-7

  Pereira, Eliseu J G ^a   Siqueira, Herbert A A ^b   Zhuang, Meibao ^d   Storer, Nicholas P ^d   Siegfried, Blair D ^c  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b UNIVERSIDADE FEDERAL RURAL DE PERNAMBUCO   (Brazil)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^d DOW AGROSCIENCES LLC   (United States)

Author keywords

Bacillus thuringiensis; Bt maize; Luminal gut proteases; Ostrinia nubilalis; Resistance; Surface Plasmon Resonance; Toxin binding

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; PEPTIDE HYDROLASE;

ANIMAL; ARTICLE; BACILLUS THURINGIENSIS; ENZYMOLOGY; GASTROINTESTINAL TRACT; ISOLATION AND PURIFICATION; LARVA; LEPIDOPTERA; METABOLISM; MICROBIOLOGY; PROTEIN BINDING;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BACTERIAL TOXINS; GASTROINTESTINAL TRACT; LARVA; LEPIDOPTERA; PEPTIDE HYDROLASES; PROTEIN BINDING;

BACILLUS THURINGIENSIS; CRAMBIDAE; HEXAPODA; LEPIDOPTERA; OSTRINIA NUBILALIS; ZEA MAYS;

EID: 72049119092     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2009.08.014     Document Type: Article

References (46)

1. Anderluh G., Besenicar M., Kladnik A., Lakey J.H., and Macek P. Properties of nonfused liposomes immobilized on an L1 Biacore chip and their permeabilization by a eukaryotic pore-forming toxin. Anal. Biochem. 344 (2005) 43-52
2. Besenicar M., Macek P., Lakey J.H., and Anderluh G. Surface plasmon resonance in protein-membrane interactions. Chem. Phys. Lipids 141 (2006) 169-178
3. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
4. Bravo A., Gomez I., Conde J., Munoz-Garay C., Sanchez J., Miranda R., Zhuang M., Gill S.S., and Soberon M. Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochim. Biophys. Acta 1667 (2004) 38-46
5. Bravo A., and Soberón M. How to cope with insect resistance to Bt toxins. Trends Biotechnol. 10 (2008) 573-579
6. Coates B.S., Sumerford D.V., Hellmich R.L., and Lewis L.C. Mining an Ostrinia nubilialis midgut expressed sequence tag (EST) library for candidate genes and single nucleotide polymorphisms. Insect Mol. Biol. 17 (2008) 607-620
7. de Maagd R.A., Bravo A., and Crickmore N. How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet. 17 (2001) 193-199
8. Ferré J., Real M.D., Vanrie J., Jansens S., and Peferoen M. Resistance to the Bacillus thuringiensis bioinsecticide in a field population of Plutella xylostella is due to a change in a midgut membrane receptor. Proc. Nat. Acad. Sci. USA 88 (1991) 5119-5123
9. Ferré J., and Van Rie J. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Ann. Rev. Entomol. 47 (2002) 501-533
10. Flannagan R.D., Yu C.G., Mathis J.P., Meyer T.E., Shi X.M., Siqueira H.A.A., and Siegfried B.D. Identification, cloning and expression of a Cry1Ab cadherin receptor from European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae). Insect Biochem. Mol. Biol. 35 (2005) 33-40
11. Forcada C., Alcacer E., Garcera M.D., and Martinez R. Differences in the midgut proteolytic activity of two Heliothis virescens strains, one susceptible and one resistant to Bacillus thuringiensis toxins. Arch. Insect Biochem. Physiol. 31 (1996) 257-272
12. Gahan L.J., Gould F., and Heckel D.G. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293 (2001) 857-860
13. Gill S.S., Cowles E.A., and Pietrantonio P.V. The mode of action of Bacillus thuringiensis endotoxins. Annu. Rev. Entomol. 37 (1992) 615-636
14. Griffitts J.S., and Aroian R.V. Many roads to resistance. How invertebrates adapt to Bt toxins. BioEssays 27 (2005) 614-624
15. Gunning R.V., Dang H.T., Kemp F.C., Nicholson I.C., and Moores G.D. New resistance mechanisms in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl. Environ. Microbiol. 71 (2005) 2558-2563
16. Heckel D.G., Gahan L.J., Baxter S.W., Ahao J.Z., Shelton A.M., Gould F., and Tabashnik B.E. The diversity of Bt resistance genes in species of Lepidoptera. J. Invert. Pathol. 95 (2007) 192-197
17. Herrero S., Gechev T., Bakker P.L., Moar W.J., and de Maagd R.A. Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four Aminopeptidase N genes. BMC Genom. 6 (2005) 96-106
18. Hua G., Masson L., Jurat-Fuentes J.L., Schwab G., and Adang M.J. Binding analyses of Bacillus thuringiensis Cry delta-endotoxins using brush border membrane vesicles of Ostrinia nubilalis. Appl. Environ. Microbiol. 67 (2001) 872-879
19. Keeton T.P., Francis B.R., Maaty W.S.A., and Bulla L.A. Effects of midgut-protein-preparative and ligand binding procedures on the toxin binding characteristics of BT-R-1, a common high-affinity receptor in Manduca sexta for Cry1A Bacillus thuringiensis toxins. Appl. Environ. Microbiol. 64 (1998) 2158-2165
20. Keller M., Sneh B., Strizhov N., Prudovsky E., Regev A., Koncz C., Schell J., and Zilberstein A. Digestion of delta-endotoxin by gut proteases may explain reduced sensitivity of advanced instar larvae of Spodoptera littoralis to Cry1C. Insect Biochem. Mol. Biol. 26 (1996) 365-373
21. Knowles B.H. Mechanism of action of Bacillus thuringiensis insecticidal delta-endotoxins. Adv. Insect. Physiol. 24 (1994) 275-308
22. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T 4. Nature 227 (1970) 680-685
23. Li H., Oppert B., Higgins R.A., Huang F.N., Zhu K.Y., and Buschman L.L. Comparative analysis of proteinase activities of Bacillus thuringiensis-resistant and -susceptible Ostrinia nubilalis (Lepidoptera: Crambidae). Insect Biochem. Mol. Biol. 34 (2004) 753-762
24. Loseva O., Ibrahim M., Candas M., Koller C.N., Bauer L.S., and Bulla L.A. 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 (2002) 567-577
25. MacDonald R.C., MacDonald R.I., Menco B.P.M., Takeshita K., Subbarao N.K., and Hu L. Small volume extrusion apparatus for preparation of large, unilamellar vesicles. Biochim. Biophys. Acta 1061 (1991) 297-303
26. Masson L., Mazza A., Brousseau R., and Tabashnik B. Kinetics of Bacillus thuringiensis toxin binding with brush border membrane vesicles from susceptible and resistant larvae of Plutella xylostella. J. Biol. Chem. 270 (1995) 11887-11896
27. Matten S.R., Head G.P., and Quemada H.D. How governmental regulation can help or hinder the integration of Bt crops into IPM programs. In: Romeis J., Shelton A.M., and Kennedy G.G. (Eds). Integration of Insect-Resistant Genetically Modified Crops within IPM Program (2008), Springer, New York 27-39
28. Meihls L.N., Higdon M.L., Siegfried B.D., Miller N.J., Sappington T.W., Ellersieck M.R., Spencer T.A., and Hibbard B.E. Increased survival of western corn rootworm on transgenic corn within three generations of on-plant greenhouse selection. Proc. Natl. Acad. Sci. USA 105 (2008) 19177-19182
29. Minitab 14 Statistical Software, 2005. Minitab, Inc., State College, PA.
30. Morin S., Biggs R.W., Sisterson M.S., Shriver L., Ellers-Kirk C., Higginson D., Holley D., Gahan L.J., Heckel D.G., Carriere Y., Dennehy T.J., Brown J.K., and Tabashnik B.E. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Nat. Acad. Sci. USA 100 (2003) 5004-5009
31. Oppert B., Kramer K.J., Beeman R.W., Johnson D., and McGaughey W.H. Proteinase-mediated insect resistance to Bacillus thuringiensis toxins. J. Biol. Chem. 272 (1997) 23473-23476
32. Oppert B., Kramer K.J., Johnson D., Upton S.J., and McGaughey W.H. Luminal proteinases from Plodia interpunctella and the hydrolysis of Bacillus thuringiensis Cry1Ac protoxin. Insect Biochem. Mol. Biol. 26 (1996) 571-583
33. Pereira E.J.G., Lang B.A., Storer N.P., and Siegfried B.D. Selection for Cry1F resistance in the European corn borer and cross resistance to other Cry toxins. Entomol. Exp. Appl. 126 (2008) 115-121
34. Pereira E.J.G., Storer N.P., and Siegfried B.D. Inheritance of Cry1F resistance in laboratory-selected European corn borer and its survival on transgenic corn expressing the Cry1F toxin. Bull. Entomol. Res. 98 (2008) 621-629
35. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., and Dean D.H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62 (1998) 775-806
36. Siqueira H.A.A., Gonzalez-Cabrera J., Ferré J., Flannagan R., and Siegfried B.D. Analyses of Cry1Ab binding in resistant and susceptible strains of the European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae). Appl. Environ. Microbiol. 72 (2006) 5318-5324
37. Siqueira H.A.A., Nickerson K.W., Moellenbeck D., and Siegfried B.D. Activity of gut proteinases from Cry1Ab-selected colonies of the European corn borer, Ostrinia nubilalis (Lepidoptera: Crambidae). Pest Manage. Sci. 60 (2004) 1189-1196
38. Tabashnik B.E. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39 (1994) 47-79
39. Tabashnik B.E. Delaying insect resistance to transgenic crops. Proc. Natl. Acad. Sci. USA 105 (2008) 19029-19030
40. Takeichi M. Cadherins - a molecular family important in selective cell-cell adhesion. Annu. Rev. Biochem. 59 (1990) 237
41. Terra W.R., and Ferreira C. Insect digestive enzymes: properties, compartmentalization and function. Comp. Biochem. Physiol. B 109 (1994) 1-62
42. Vaughn T.T., Cavat T., Brar G., Coombe T., DeGooyer T., Ford S., Groth M., Howe A., Johnson S., Kolacz K., Pilcher C., Purcell J., Romano C., English L., and Pershing J. A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci. 45 (2005) 931-938
43. Wolfersberger M., Luethy P., Maurer A., Parenti P., Sacchi F.V., Giordana B., and Hanozet G.M. 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. A 86 (1987) 301-308
44. Xu X.J., Yu L.Y., and Wu Y.D. Disruption of a cadherin gene associated with resistance to Cry1Ac delta-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl. Environ. Microbiol. 71 (2005) 948-954
45. Xu X., and Wu Y. Disruption of Ha_BtR alters binding of Bacillus thuringiensis delta-endotoxin Cry1Ac to midgut BBMVs of Helicoverpa armigera. J. Invert. Pathol. 97 (2008) 27-32
46. Zhuang M., and Gill S.S. Mode of action of Bacillus thuringiensis toxins. In: Voss G., and Ranos G. (Eds). Chemistry of Plant Protection - Prospects in Science and Regulation (2003), Willey-VHC, Weihein 212-234