Selective inhibition of binding of Bacillus thuringiensis Cry1Ab toxin to cadherin-like and aminopeptidase proteins in brush-border membranes and dissociated epithelial cells from Bombyx mori

Biochemical Journal

Volumn 409, Issue 1, 2008, Pages 215-221

  Ibiza Palacios, M Sales ^a   Ferré, Juan ^a   Higurashi, Satoshi ^b   Miyamoto, Kazuhisa ^c   Sato, Ryoichi ^b   Escriche, Baltasar ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^c NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Aminopeptidase N (APN); Bacillus thuringiensis; Cry1AB susceptibility; Irreversible binding; Reversible binding; Toxin receptor binding

Indexed keywords

BIOCHEMISTRY; CELL MEMBRANES; CYTOTOXICITY; PROTEINS;

BACILLUS THURINGIENSIS; INHIBITORY EFFECT; IRREVERSIBLE BINDING; REVERSIBLE BINDING; TOXIN BINDING; TOXIN RECEPTOR BINDING;

ENZYME INHIBITION;

AMINOPEPTIDASE; ANTIBODY; CADHERIN; CRY1AB TOXIN; MICROSOMAL AMINOPEPTIDASE; BACTERIAL PROTEIN; BACTERIAL TOXIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL STRAIN; BRUSH BORDER VESICLE; CYTOTOXICITY; ENZYME BINDING; ENZYME INHIBITION; EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; SILKWORM; ANIMAL; BIOASSAY; CHEMISTRY; DRUG ANTAGONISM; INTESTINE; MEMBRANE; METABOLISM; MICROVILLUS; PROTEIN BINDING;

BACILLUS THURINGIENSIS; BOMBYX MORI; LEPIDOPTERA;

AMINOPEPTIDASES; ANIMALS; ANTIBODIES; ANTIGENS, CD13; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BIOLOGICAL ASSAY; BOMBYX; ENDOTOXINS; EPITHELIAL CELLS; HEMOLYSIN PROTEINS; INTESTINES; MEMBRANES; MICROVILLI; PROTEIN BINDING;

EID: 38149116408     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070956     Document Type: Article

References (46)

1. Schnepf, E., Crickmore, N., Van Rie, J., Lereclus, D., Baum, J., Feitelson, J., Zeigler, D. R. and Dean, D. H. (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62, 775-806
2. Crickmore, N., Zeigler, D. R., Feitelson, J., Schnepf, E., Van Rie, J., Lereclus, D., Baum, J. and Dean, D. H. (1998) Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62, 807-813
3. Griffitts, J. S. and Aroian, R. V. (2005) Many roads to resistance: how invertebrates adapt to Bt toxins. BioEssays 27, 614-624
4. Lee, M. K., Milne, R. E., Ge, A. Z. and Dean, D. H. (1992) Location of a Bombyx mori receptor binding region on a Bacillus thuringiensis δ-endotoxin. J. Biol. Chem. 267, 3115-3121
5. Chen, X. J., Curtiss, A., Alcantara, E. and Dean, D. H. (1995) Mutations in domain I of Bacillus thuringiensis delta;-endotoxin Cry1Ab reduce the irreversible binding of toxin to Manduca sexta brush border membrane vesicles. J. Biol. Chem. 270, 6412-6419
6. Liang, Y., Patel, S. S. and Dean, D. H. (1995) Irreversible binding kinetics of Bacillus thuringiensis Cry1A δ-endotoxins to gypsy moth brush border membrane vesicles is directly correlated to toxicity. J. Biol. Chem. 270, 24719-24724
7. Bravo, A., Gómez, I., Conde, J., Munoz-Garay, C., Sánchez, J., Miranda, R., Zhuang, M., Gill, S. S. and Soberón, M. (2004) 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, 38-46
8. 1 expressed in insect cells. Cell Death Differ. 12, 1407-1416
9. Ferré, J. and Van Rie, J. (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 47, 501-533
10. c toxin. J. Biol. Chem. 270, 17765-17770
11. Masson, L., Lu, Y. J., Mazza, A., Brousseau, R. and Adang, M. J. (1995) Kinetics of Bacillus thuringiensis toxin binding with brush border membrane vesicles from susceptible and resistant larvae of Plutella xylostella. J. Biol. Chem. 270, 20309-20315
12. Luo, K., Lu, Y. J. and Adang, M. J. (1996) A 106 kDa form of aminopeptidase is a receptor for Bacillus thuringiensis Cry1C δ-endotoxin in the brush border membrane of Manduca sexta. Insect Biochem. Mol. Biol. 26, 783-791
13. Yaoi, K., Kadotani, T., Kuwana, H., Shinkawa, A., Takahashi, T., Iwahana, H. and Sato, R. (1997) Aminopeptidase N from Bombyx mori as a candidate for the receptor of Bacillus thuringiensis Cry1Aa toxin. Eur. J. Biochem. 246, 652-657
14. Hua, G., Tsukamoto, K., Rasilo, M. L. and Ikezawa, H. (1998) Molecular cloning of a GPI-anchored aminopeptidase N from Bombyx mori midgut: a putative receptor for Bacillus thuringiensis Cry1A toxin. Gene 214, 177-185
15. Nakanishi, K., Yaoi, K., Nagino, Y., Hara, H., Kitami, M., Atsumi, S., Miura, N. and Sato, R. (2002) Location of the Bombyx mori aminopeptidase N type 1 binding site on Bacillus thuringiensis Cry1Aa toxin. FEBS Lett. 519, 215-220
16. Gahan, L. J., Gould, F. and Heckel, D. G. (2001) Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293, 857-860
17. 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. et al. (2003) Three Cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Natl. Acad. Sci. U.S.A. 100, 5004-5009
18. Gill, M. and Ellar, D. (2002) Transgenic Drosophila reveals a functional in vivo receptor for the Bacillus thuringiensis toxin Cry1Ac1. Insect Mol. Biol. 11, 619-625
19. Tsuda, Y., Nakatani, F., Hashimoto, K., Ikawa, S., Matsuura, C., Fukada, T., Sugimoto, K. and Himeno, M. (2003) Cytotoxic activity of Bacillus thuringiensis Cry proteins on mammalian cells transfected with cadherin-like Cry receptor gene of Bombyx mori (silkworm). Biochem. J. 369, 697-703
20. Lee, M. K. and Dean, D. H. (1996) Inconsistencies in determining Bacillus thuringiensis toxin binding sites relationship by comparing competition assays with ligand blotting. Biochem. Biophys. Res. Commun. 220, 575-580
21. Reference deleted
22. Shibano, Y., Yamagata, A., Nakamura, N., Iizuka, T., Sugisaki, H. and Takanami, M. (1985) Nucleotide sequence coding for the insecticidal fragment of the Bacillus thuringiensis crystal protein. Gene 34, 243-251
23. Kim, Y. S., Kanda, K., Kato, F. and Murata, A. (1998) Effects of Bacillus thuringiensis Cry1Ab toxin on mammalian cells. Appl. Entomol. Zool. 33, 473-477
24. Ang, B. J. and Nickerson, K. W. (1978) Purification of the protein crystal from Bacillus thuringiensis by zonal gradient centrifugation. Appl. Environ. Microbiol. 36, 625-626
25. Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, N. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
26. Bradford, M. 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
27. Sayyed, A. H., Gatsi, R., Ibiza-Palacios, S., Escriche, B., Wright, D. J. and Crickmore, N. (2005) Common, but complex, mode of resistance of Plutella xylostella to Bacillus thuringiensis toxins Cry1Ab and Cry1Ac. Appl. Environ. Microbiol. 71, 6863-6869
28. Hernandez, C. S., Rodrigo, A. and Ferré, J. (2004) Lyophilization of lepidopteran midguts: a preserving method for Bacillus thuringiensis toxin binding studies. J. Invertebr. Pathol. 85, 182-187
29. Sayyed, A. H., Raymond, B., Ibiza-Palacios, M. S., Escriche, B. and Wright, D. J. (2004) Genetic and biochemical characterization of field-evolved resistance to Bacillus thuringiensis toxin Cry1Ac in the diamondback moth, Plutella xylostella. Appl. Environ. Microbiol. 70, 7010-7017
30. Hara, H., Atsumi, S., Yaoi, K., Nakanishi, K., Higurashi, S., Miura, N., Tabunoki, H. and Sato, R. (2003) A cadherin-like protein functions as a receptor for Bacillus thuringiensis Cry1Aa and Cry1Ac toxins on midgut epithelial cells of Bombyx mori larvae. FEBS Lett. 538, 29-34
31. Van Rie, J., Jansens, S., Hofte, H., Degheele, D. and Van Mellaert, H. (1989) Specificity of Bacillus thuringiensis δ-endotoxins. Importance of specific receptors on the brush border membrane of the mid-gut of target insects. Eur. J. Biochem. 186, 239-247
32. a toxin. Biosci. Biotechnol. Biochem. 62, 718-726
33. González-Cabrera, J., Herrero, S., Sayyed, A. H., Escriche, B., Liu, Y. B., Meyer, S. K., Wright, D. J., Tabashnik, B. E. and Ferré, J. (2001) Variation in susceptibility to Bacillus thuringiensis toxins among unselected strains of Plutella xylostella. Appl. Environ. Microbiol. 67, 4610-4613
34. Ge, A. Z., Shivarova, N. I. and Dean, D. H. (1989) Location of the Bombyx mori specificity domain on a Bacillus thuringiensis δ-endotoxin protein. Proc. Natl. Acad. Sci. U.S.A. 86, 4037-4041
35. Masson, L., Mazza, A., Gringorten, L., Baines, D., Aneliunas, V. and Brousseau, R. (1994) Specificity domain localization of Bacillus thuringiensis insecticidal toxins is highly dependent on the bioassay system. Mol. Microbiol. 14, 851-860
36. Gringorten, J. L., Sohi, S. S. and Masson, L. (1999) Activity spectra of Bacillus thuringiensis δ-endotoxins against eight insect cell lines. In Vitro Cell Dev. Biol. Anim. 35, 299-303
37. Ihara, H., Kuroda, E., Wadano, A. and Himeno, M. (1993) Specific toxicity of δ-endotoxins from Bacillus thuringiensis to Bombyx mori. Biosci. Biotechnol. Biochem. 57, 200-204
38. Jenkins, J. L. and Dean, D. H. (2001) Binding specificity of Bacillus thuringiensis Cry1Aa for purified, native Bombyx mori aminopeptidase N and cadherin-like receptors. BMC Biochem. 2, 12
39. Hussain, S. R., Aronson, A. I. and Dean, D. H. (1996) Substitution of residues on the proximal side of Cry1A Bacillus thuringiensis δ-endotoxins affects irreversible binding to Manduca sexta midgut membrane. Biochem. Biophys. Res. Commun. 226, 8-14
40. Vadlamudi, R. K., Weber, E., Ji, I., Ji, T. H. and Bulla, Jr, L. A. (1995) Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. J. Biol. Chem. 270, 5490-5494
41. Flannagan, R. D., Yu, C. G., Mathis, J. P., Meyer, T. E., Shi, X., Siqueira, H. A. and Siegfried, B. D. (2005) Identification, cloning and expression of a Cry1Ab Cadherin receptor from European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae). Insect Biochem. Mol. Biol. 35, 33-40
42. Nagamatsu, Y., Koike, T., Sasaki, K., Yoshimoto, A. and Furukawa, Y. (1999) The cadherin-like protein is essential to specificity determination and cytotoxic action of the Bacillus thuringiensis insecticidal Cry1Aa toxin. FEBS Lett. 460, 385-390
43. Xu, X., Yu, L. and Wu, Y. (2005) Disruption of a Cadherin gene associated with resistance to Cry1Ac δ-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl. Environ. Microbiol. 71, 948-954
44. Sivakumar, S., Rajagopal, R., Venkatesh, G. R., Srivastava, A. and Bhatnagar, R. K. (2007) Knockdown of aminopeptidase-N from Helicoverpa amigera larvae and in transfected Sf21 cells by RNA interference reveals its functional interaction with Bacillus thuringiensis insecticidal protein Cry1Ac. J. Biol. Bichem. 282, 7312-7319
45. Gómez, I., Arenas, I., Benítez, I., Miranda-Rios, J., Becerril, B., Grande, R., Almagro, J. C., Bravo, A. and Soberón, M. (2006) Specific epitopes of domains II and III of Bacillus thuringiensis Cry1Ab toxin involved in the sequential interaction with cadherin and aminopeptidase-N receptors in Manduca sexta. J. Biol. Chem. 281, 34032-34039
46. Herrero, S., Gechev, T., Bakker, P. L., Moar, W. J. and de Maagd, R. A. (2005) Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four aminopeptidase N genes. BMC Genomics 6, 96