A Fragment of Cadherin-Like Protein Enhances Bacillus thuringiensis Cry1B and Cry1C Toxicity to Spodoptera exigua (Lepidoptera: Noctuidae)

Journal of Integrative Agriculture

Volumn 11, Issue 4, 2012, Pages 628-638

  Lu, Qiong ^a,b   Zhang, Yong jun ^b   Cao, Guang chun ^b   Zhang, Li li ^a,b   Liang, Ge mei ^b   Lu, Yan hui ^b   Wu, Kong ming ^b   Gao, Xi wu ^a   Guo, Yu yuan ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Bacillus thuringiensis; Cadherin like; Enhancement toxicity; Spodoptera exigua

Indexed keywords

BACILLUS THURINGIENSIS; HEXAPODA; LEPIDOPTERA; NOCTUIDAE; SPODOPTERA EXIGUA;

EID: 84862496780     PISSN: 20953119     EISSN: None     Source Type: Journal    
DOI: 10.1016/S2095-3119(12)60050-1     Document Type: Article

References (59)

1. Abdullah MA, Moussa S, Taylor MD, Adang MJ Manduca sexta (Lepidoptera: Sphingidae) cadherin fragments function as synergists for Cry1A and Cry1C Bacillus thuringiensis toxins against noctuid moths Helicoverpa zea, Agrotis ipsilon and Spodoptera exigua. Pest Management Science 2009, 65:1097-1103.
2. Abdul-Rauf M, Ellar DJ Toxicity and receptor binding properties of a Bacillus thuringiensis Cry1C toxin active against both lepidoptera and diptera. Journal of Invertebrate Pathology 1999, 73:52-58.
3. Aimanova KG, Zhuang M, Gill SS Expression of Cry1Ac cadherin receptors in insect midgut and cell lines. Journal of Invertebrate Pathology 2006, 92:178-187.
4. Bradford MM A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
5. Bravo A, Gomez I, Conde J, Munoz-Garay C, Sanchez J, Miranda R, Zhuang M, Gill SS, Soberon M Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochimica et Biophysica Acta 2004, 1667:38-46.
6. Broderick NA, Raffa KF, Handelsman J Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:15196-15199.
7. Carriérea Y, Showalter AM, Fabrick JA, Sollome J, Ellers-Kirk C, Tabashnik BE Cadherin gene expression and effects of Bt resistance on sperm transfer in pink bollworm. Journal of Invertebrate Pathology 2009, 55:1058-1064.
8. Chen J, Brown MR, Hua G, Adang MJ Comparison of the localization of Bacillus thuringiensis Cry1A delta-endotoxins and their binding proteins in larval midgut of tobacco hornworm, Manduca sexta. Cell Tissue Research 2005, 321:123-129.
9. Chen J, Hua G, Jurat-Fuentes JL, Abdullah MA, Adang MJ Synergism of Bacillus thuringiensis toxins by a fragment of a toxin-binding cadherin. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:13901-13906.
10. Dror A, Haviva E, Menachem K, Noam R, Michal S, Baruch S, Aciah Z The Bacillus thuringiensis delta-endotoxin Cry1C as a potential bioinsecticide in plants. Plant Science 2009, 176:315-324.
11. Dorsch JA, Candas M, Griko NB, Maaty WSA, Midboe EG, Vadlamudi RK, Bulla JLA Cry1A toxins of Bacillus thuringiensis bind specifically to a region adjacent to the membrane-proximal extracellular domain of BT-R1 in Manduca sexta: involvement of a cadherin in the entomopathogenicity of Bacillus thuringiensis. Insect Biochemisry and Molecular Biology 2002, 32:1025-1036.
12. Fabrick J, Oppert C, Lorenzen MD, Morris K, Oppert B, Jurat-Fuents L A novel Tenebrio Molitor cadherin is a functional receptor for Bacillus thuringiensis Cry3Aa toxin. The Journal of Biological Chemistry 2009, 27:18401-18410.
13. Flannagan RD, Yu C, Mathis JP, Meyer TE, Shi X, Siqueira HAA, Siegfried BD Identification, cloning and expression of a Cry1Ab cadherin receptor from European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae). Insect Biochemisry and Molecular Biology 2005, 35:33-40.
14. Gahan LJ, Gould F, Heckel DG Identification of a gene associated with Bt resistance in Heliothis virescens. Science 2001, 293:857-860.
15. Gill SS, Cowles EA, Francis V Identification, isolation, and cloning of a Bacillus thuringiensis Cry1Ac toxin-binding protein from the midgut of the Lepidopteran insect Heliothis virescens. Journal of Biological Chemistry 1995, 270:27277-27282.
16. Gilliland A, Chambers CE, Bone EJ, Ellar DJ Role of Bacillus thuringiensis Cry1 ?-endotoxin binding in determining potency during Lepidopteran larval development. Applied and Environmental Microbiology 2002, 68:1509-1515.
17. Gómez I, Dean DH, Bravo A, Soberón M Molecular basis for Bacillus thuringiensis Cry1Ab toxin specificity: two structural determinants in the Manduca sexta: Bt-R1 receptors interact with loops a-8 and 2 in domain II of Cry1Ab toxin. ACS Chemical Biology 2003, 42:10482-10489.
18. Gómez I, Oltean DI, Gill SS, Bravo A, Soberón M Mapping the epitope in Cadherin-like receptors involved in Bacillus thuringiensis Cry1A toxin interaction using phage display. Journal of Biological Chemistry 2001, 276:28906-28912.
19. Granados RR, Fu Y, Corsaro B, Hughes PR Enhancement of Bacillus thuringiensis toxicity to lepidopterous species with the enhancin from Trichoplusia ni granulovirus. Biological Control 2001, 20:153-159.
20. Griffitts JS, Aroian RV Many roads to resistance: how invertebrates adapt to Bt toxins. BioEssays 2005, 27:614-624.
21. Griko N, Candas M, Zhang X, Junker M Selective antagonism to the cadherin BT-R1 interferes with calcium-induced adhesion of epithelial membrane vesicles. Biochemistry 2004, 43:1393-1400.
22. Hernández-Martínez P, Ferré J, Escriche B Susceptibility of Spodoptera exigua to 9 toxins from Bacillus thringiensis. Journal of Invertebrate Pathology 2008, 97:245-250.
23. Herrero S, Gónzalez-Cabrera J, Tabashnik BE, Ferré J Shared binding sites in Lepidoptera for Bacillus thuringiensis Cry1Ja and Cry1A toxins. Applied and Environmental Microbiology 2001, 67:5729-5734.
24. Hara H, Atsumi S, Yaoi K, Nakanishi K, Higurashi S, Miura N, Tabunoki H, Sato R A cadherin-like protein functions as a receptor for Bacillus thuringiensis Cry1Aa and Cry1Ac toxins on midgut epithelial cells of Bombyx mori larvae. FEBS Letters 2003, 538:29-34.
25. Ibiza-Palacios MS, Ferré J, Higurashi S, Miyamoto K, Sato R, Escriche B 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 2008, 409:215-221.
26. James C Global Status of Commercialized Biotech/GM Crops: 2010 2010, ISAAA 41, Ithaca, New York, USA.
27. Jurat-Fuentes JL, Adang MJ Characterization of a Cry1Ac receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. European Journal of Biochemistry 2004, 271:3127-3135.
28. Jurat-Fuentes JL, Adang MJ The Heliothis virescens cadherin protein expressed in Drosophila S2 cells functions as a receptor for Bacillus thuringiensis Cry1A but not Cry1Fa toxins. Biochemistry 2006, 45:9688-9695.
29. Knight PJ, Knowles BH, Ellar DJ Molecular cloning of an insect aminopeptidase N that serves as a receptor for Bacillus thuringiensis Cry1A(c) toxin. Journal of Biological Chemistry 1995, 270:17765-17770.
30. Lee MK, Curtiss A, Alcantara E, Dean DH Synergistic effect of the Bacillus thuringiensis toxins Cry1Aa and Cry1Ac on the gypsy moth, Lymantria dispar. Applied and Environmental Microbiology 1996, 62:583-596.
31. LeOra Software. 1987. POLO-PC: A User's Manual for Probit or Logit Analysis. Berkeley, CA.
32. Liang GM, Tan WJ, Guo YY Improvement technology of artificial feeding bollworm. Plant Protection 1999, 25:15-17. (in Chinese).
33. Liu CX, Wu KM, Wu YD, Gao YL, Ning CM, Oppert B Reduction of Bacillus thuringiensis Cry1Ac toxicity against Helicoverpa armigera by a soluble toxin-binding cadherin fragment. Journal of Invertebrate Pathology 2009, 55:686-693.
34. Luo K, Banks D, Adang MJ Toxicity, binding, permeability analyses of four Bacillus thuringiensis Cry1 d-endotoxins using brush border membrane vesicles of Spodoptera exigua and Spodoptera frugiperda. Applied and Environmental Microbiology 1998, 99:457-464.
35. Luttrell RG, Wan L, Knighten K Variation in susceptibility of noctuid (Lepidoptera) larvae attacking cotton and soybean to purified endotoxin proteins and commercial formulations of Bacillus thuringiensis. Journal of Economic Entomology 1999, 92:21-32.
36. de Maagd R, Weemen-Hendriks M, Stiekema W, Bosch D Bacillus thuringiensis delta-endotoxin Cry1C domain III can function as a specificity determinant for Spodoptera exigua in different, but not all, Cry1-Cry1C hybrids. Applied and Environmental Microbiology 2000, 66:1559-1563.
37. Moar WJ, Pusztai-Carey M, Van Faassen H, Bosh D, Frutis R, Rang C, Luo K, Adang MJ Development of Bacillus thuringiensis Cry1C resistance by Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). Applied and Environmental Microbiology 1995, 95:2086-2092.
38. Morin S, Biggs RW, Sisterson MS, Shriver L, Ellers-Kirk C, Higginson D, Holley D, Gahan LJ, Heckel DG, Carriére Y, et al. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:5004-5009.
39. Moulton JK, Pepper DA, Dennehy TJ Beet armyworm (Spodoptera exigua) resistance to spinosad. Pest Management Science 2000, 56:842-848.
40. Nagamatsu Y, Toda S, Koike T, Miyoshi Y, Shigematsu S, Kogure M Cloning, sequencing, and Expression of the Bombyx mori receptor for Bacillus thuringiensis insecticidal CryIA(a) toxin. Bioscience Biotechnology Biochemistry 1998, 62:727-734.
41. Nagamatsu Y, Toda S, Yamaguchi F, Ogo M, Kogure M, Nakamura M, Shibata Y, Katsumoto T Identification of Bombyx mori midgut receptor for Bacillus thuringiensis insecticidal CryIA(a) toxin. Bioscience Biotechnology Biochemistry 1998, 62:718-726.
42. Pacheco S, Gómez I, Gill SS, Bravo A, Soberón M Enhancement of insecticidal activity of Bacillus thuringiensis Cry1A toxins by fragments of a toxin-binding cadherin correlates with oligomer formation. Peptides 2009, 30:533-588.
43. Pérez C, Fernandez LE, Sun J, Folch JL, Gill SS, Soberón M, Bravo A Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:18303-18308.
44. Pigott CR, Ellar DJ Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiology and Molecular Biology Reviews 2007, 71:255-281.
45. Regev A, Keller M, Strizhov N, Sneh B, Prudovsky E, Chet I, Ginzberg I, Koncz-Kalman Z, Koncz C, Schell J, et al. Synergistic activity of a Bacillus thuringiensis delta-endotoxin and a bacterial endochitinase against Spodoptera littoralis larvae. Applied and Environmental Microbiology 1996, 62:3581-3586.
46. Sayed A, Nekl ER, Siqueira HAA, Wang HC, Ffrench-Constant RH, Bagley M, Siegfried BD A novel cadherin-like gene from western corn rootworm, Diabrotica vigifera (Coleoptera: Chrysomelidae), larval midgut tissue. Insect Biochemisry and Molecular Biology 2007, 16:591-600.
47. Smits PH, van Velden MC, van de Vrie M, Vlak JM Feeding and dispersion of Spodoptera exigua larvae and its relevance for control with a nuclear polyhedrosis virus. Entomologia Experimentalis et Applicata 1987, 43:67-72.
48. Tabashnik BE, Gassmann AJ, Crowder DW, Carriere Y Insect resistance to Bt crops: evidence versus theory. Nature Biotechnology 2008, 26:199-202.
49. Tabashnik BE Evalution of synergism among Bacillus thuringiensis toxins. Applied and Environmental Microbiology 1992, 58:3343-3346.
50. Tabashnik BE Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology 1994, 39:47-79.
51. Tsuda Y, Nakatani F, Hashimoto K, Ikawa S, Matsuura C, Fukada T, Sugimoto K, Himeno M Cytotoxic activity of Bacillus thuringiensis Cry proteins on mammalian cells transfected with cadherin-like Cry receptor gene of Bombyx mori (silkworm). Biochemical Journal 2003, 369:697-703.
52. Vadlamudi RK, Ji TH, Bulla LA A specific binding protein from Manduca sexta for the insecticidal toxin of Bacillus thuringiensis subsp. berliner. Journal of Biological Chemistry 1993, 268:12334-12340.
53. Vadlamudi RK, Weber E, Ji I, Ji TH, Bulla LA Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. Journal of Biological Chemistry 1995, 270:5490-5494.
54. Wang G, Wu K, Liang G, Guo Y Gene cloning and expression of cadherin in midgut of Helicoverpa armigera and its Cry1A binding region. Science in China Series 2005, 48:346-356. (C: Life Sciences).
55. Wu K, Lu Y, Feng H, Jiang Y, Zhao J Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 2008, 321:1676-1678.
56. Xie R, Zhuang M, Ross LS, Gómez I, Oltean DI, Bravo A, Soberon M, Gill SS Single amino acid mutations in the cadherin receptor from Heliothis virescens affect its toxin binding ability to Cry1A toxins. The Journal of Biological Chemistry 2005, 280:8416-8425.
57. Zhang X, Candas M, Griko NB, Rose-Young L, Bulla LA Cytotoxicity of Bacillus thuringiensis Cry1Ab toxin depends on specific binding of the toxin to the cadherin receptor BT-R1 expressed in insect cells. Cell Death and Differentiation 2005, 12:1407-1416.
58. Zhang X, Candas M, Griko NB, Taussig R, Bulla LA A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:9897-9902.
59. Zhang X, Griko NB, Corona SK, Bulla LA Enhanced exocytosis of the receptor BT-R1 induced by Cry1Ab toxin of Bacillus thuringiensis directly correlates to the execution of cell death. Comparative Biochemistry and Physiology 2008, 149:581-588. (Part B).