Affinity maturation of Cry1Aa toxin to the bombyx mori cadherin-like receptor by directed evolution

Molecular Biotechnology

Volumn 54, Issue 3, 2013, Pages 888-899

  Fujii, Yuki ^a   Tanaka, Shiho ^a   Otsuki, Manami ^a   Hoshino, Yasushi ^a   Endo, Haruka ^a   Sato, Ryoichi ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

Author keywords

Affinity maturation; Bacillus thuringiensis; Cadherin like receptor; Cry toxin; Directed evolution

Indexed keywords

AFFINITY MATURATION; BACILLUS THURINGIENSIS; CADHERIN-LIKE RECEPTOR; CRY TOXIN; DIRECTED EVOLUTION;

AMINO ACIDS; ANIMALS; BACTERIOLOGY; BINDING ENERGY; CLONING; GENES; GLYCOPROTEINS; LIBRARIES; METABOLITES; POLYPEPTIDES;

TOXIC MATERIALS;

BACILLUS THURINGIENSIS TOXIN; CADHERIN; CADHERIN LIKE RECEPTOR; CRY1AA TOXIN; MUTANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL MUTATION; BACTERIOPHAGE T7; BINDING AFFINITY; BINDING KINETICS; BOMBYX MORI; CLONE; DIRECTED MOLECULAR EVOLUTION; GENETIC ENGINEERING; INSECTICIDAL ACTIVITY; MATURATION; NONHUMAN; RECEPTOR BINDING; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BOMBYX; CADHERINS; DIRECTED MOLECULAR EVOLUTION; ENDOTOXINS; HEMOLYSIN PROTEINS; INSECTICIDES; KINETICS; LARVA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE LIBRARY; PROTEIN BINDING; RECOMBINANT PROTEINS; SF9 CELLS;

BACILLUS THURINGIENSIS; BOMBYX MORI;

EID: 84882856233     PISSN: 10736085     EISSN: 15590305     Source Type: Journal    
DOI: 10.1007/s12033-012-9638-0     Document Type: Article

References (59)

1. Crickmore, N. (2006). Beyond the spore - past and future developments of Bacillus thuringiensis as a biopesticide. Journal of Applied Microbiology, 101, 616-619.
2. Romeis, J.; Meissle, M.; Bigler, F. (2006). Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology, 24, 63-71.
3. Bravo, A.; Likitvivatanavong, S.; Gill, S. S.; Soberon, M. (2011). Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochemistry and Molecular Biology, 41, 423-431.
4. Zhang, X.; Candas, M.; Griko, N. B.; Taussig, R.; Bulla, L. A. (2006). 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, 103, 9897-9902.
5. Gahan, L. J.; Gould, F.; Heckel, D. G. (2001). Identification of a gene associated with Bt resistance in Heliothis virescens. Science, 293, 857-860.
6. Morin, S.; Biggs, R. W.; Sisterson, M. S.; Shriver, L.; Ellers-Kirk, C.; Higginson, D.; et al. (2003). 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, 100, 5004-5009.
7. Xu, X.; Yu, L.; Wu, Y. (2005). Disruption of a cadherin gene associated with resistance to Cry1Ac delta -endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Applied and Environmental Microbiology, 71, 948-954.
8. Yang, Y.; Chen, H.; Wu, Y.; Yang, Y.; Wu, S. (2007). Mutated cadherin alleles from a field population of Helicoverpa armigera confer resistance to Bacillus thuringiensis toxin Cry1Ac. Applied and Environmental Microbiology, 73, 6939-6944.
9. Nagamatu, Y.; Koike, T.; Sasaki, K.; Yoshimoto, A.; Furukawa, Y. (1999). The cadherin-like protein is essential to specificity determination and cytotoxic action of the Bacillus thuringiensis insecticidal Cry1Aa toxin. FEBS Letters, 460, 385-390.
10. Tsuda, Y.; Nakatani, F.; Hashimoto, K.; Ikawa, S.; Matsuura, C.; Fukada, T.; et al. (2003). Cytotoxic activity of Bacillus thuringiensis Cry proteins on mammalian cells transfected with cadherin-like Cry receptor gene of Bombyx mori (silkworm). The Biochemical Journal, 369, 697-703.
11. Hua, G.; Jurat-Fuentes, J. L.; Adang, M. J. (2004). Fluorescent-based assays establish Manduca sexta Bt-R(1a) cadherin as a receptor for multiple Bacillus thuringiensis Cry1A toxins in Drosophila S2 cells. Insect Biochemistry and Molecular Biology, 34, 193-202.
12. Zhang, X.; Candas, M.; Griko, N. B.; Rose-Young, L.; Bulla, L. A. (2005). 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, 12, 1407-1416.
13. Soberon, M.; Pardo-Lopez, L.; Lopez, I.; Gomez, I.; Tabashnik, B. E.; Bravo, A. (2007). Engineering modified Bt toxins to counter insect resistance. Science, 318, 1640-1642.
14. Tabashnik, B. E.; Huang, F.; Ghimire, M. N.; Leonard, B. R.; Siegfried, B. D.; Rangasamy, M.; et al. (2011). Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance. Nature Biotechnology, 29, 1128-1131.
15. Gahan, L. J.; Pauchet, Y.; Vogel, H.; Heckel, D. G. (2010). An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genetics, 6, e1001248.
16. Baxter, S. W.; Badenes-perez, F. R.; Morrison, A.; Vogel, H.; Crickmore, N.; Kain, W.; et al. (2011). Parallel evolution of Bt toxin resistance in Lepidoptera. Genetics, 189, 675-679.
17. Atsumi, S.; Miyamoto, K.; Yamamoto, K.; Narukawa, J.; Kawai, S.; Sezutsu, H.; et al. (2012). Single amino acid mutation in an ATP-binding cassette transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proceedings of the National Academy of Sciences of the United States of America, 109, E1591-E1598.
18. Li, J. D.; Carroll, J.; Ellar, D. J. (1991). Crystal structure of insecticidal delta-endotoxin from Bacillus thuringiensis at 2.5 Å resolution. Nature, 353, 815-821.
19. Grochulski, P.; Masson, L.; Borisova, S.; Pusztai-Carey, M.; Schwartz, J. L.; Brousseau, R.; et al. (1995). Bacillus thuringiensis Cry1A(a) insecticidal toxin: crystal structure and channel formation. Journal of Molecular Biology, 254, 447-464.
20. Galitsky, N.; Cody, V.; Wojtczak, A.; Ghosh, D.; Luft, J. R.; Pangborn, W.; et al. (2001). Structure of the insecticidal bacterial delta-endotoxin Cry3Bb1 of Bacillus thuringiensis. Acta Crystallographica Section D, Biological Crystallography, 57, 1101-1109.
21. Morse, R. J.; Yamamoto, T.; Stroud, R. M. (2001). Structure of Cry2Aa suggests an unexpected receptor binding epitope. Structure, 9, 409-417.
22. Boonserm, P.; Davis, P.; Ellar, D. J.; Li, J. (2005). Crystal structure of the mosquito-larvicidal toxin Cry4Ba and its biological implications. Journal of Molecular Biology, 348, 363-382.
23. Boonserm, P.; Mo, M.; Angsuthanasombat, C.; Lescar, J. (2006). Structure of the functional from of the mosquito larvicidal Cry4Aa toxin from Bacillus thuringiensis at a 2.8-angstorm resolution. Journal of Bacteriology, 188, 3391-3401.
24. Guo, S.; Ye, S.; Liu, Y.; Wei, L.; Xue, J.; Wu, H.; et al. (2009). Crystal structure of Bacillus thuringiensis Cry8Ea1: an insecticidal toxin toxic to underground pests, the larvae of Holotrichia parallela. Journal of Structural Biology, 168, 259-266.
25. Gomez, I.; Dean, D. H.; Bravo, A.; Soberon, M. (2003). Molecular basis for Bacillus thuringiensis Cry1Ab toxin specificity: two structural determinants in the Manduca sexta Bt-R1 receptor interact with loops alpha-8 and 2 in domain II of Cry1Aa toxin. Biochemistry, 42, 10482-10489.
26. Wu, S. J.; Dean, D. H. (1996). Functional significance of loops in the receptor binding domain of Bacillus thuringiensis CryIIIA delta-endotoxin. Journal of Molecular Biology, 255, 628-640.
27. Gomez, I.; Oltean, D. I.; Gill, S. S.; Bravo, A.; Soberon, M. (2001). Mapping the epitope in cadherin-like receptor involved in Bacillus thuringiensis Cry1A toxin interaction using phage display. The Journal of Biological Chemistry, 276, 28906-28912.
28. Xie, R.; Zhuang, M.; Ross, L. S.; Gomez, I.; Oltean, D. I.; Bravo, A.; et al. (2005). Single amino acid mutations in the cadherin receptor from Heliothis virescens affect its toxin binding ability to Cry1A toxins. The Journal of Biological Chemistry, 280, 8416-8425.
29. Sharma, P.; Nain, V.; Lakhanpaul, S.; Kumar, P. A. (2011). Binding of Bacillus thuringiensis Cry1A toxins with brush border membrane vesicles of maize stem borer (Chilo partellus Swinhoe). Journal of Invertebrate Pathology, 106, 333-335.
30. Dorsch, J. A.; Candas, M.; Griko, N. B.; Maaty, W. S.; Midboe, E. G.; Vadlamudi, R. K.; et al. (2002). Cry1A toxins of Bacillus thuringiensis bind specifically to a region adjacent to the membrane-proximal extracellular domain of BT-R(1) in Manduca sexta: involvement of a cadherin in the entomopathogenicity of Bacillus thuringiensis. Insect Biochemistry and Molecular Biology, 32, 1025-1036.
31. Marks, J. D.; Marks, J. D.; Griffiths, A. D.; Malmqvist, M.; Clackson, T. P.; Bye, J. M.; et al. (1992). By-passing immunization: building high affinity human antibodies by chain shuffling. Bio/Technology, 10, 779-783.
32. Barbas, C. F, 3rd, Hu, D.; Dunlop, N.; Sawyer, L.; Cababa, D.; Hendry, R. M.; et al. (1994). In vitro evolution of a neutralizing human antibody to human immunodeficiency virus type 1 to enhance affinity and broaden strain cross-reactivity. Proceedings of the National Academy of Sciences of the United States of America, 91, 3809-3813.
33. Marzari, R.; Edomi, P.; Bhatnagar, R. K.; Ahmad, S.; Selvapandiyan, A.; Bradbury, A. (1997). Phage display of Bacillus thuringiensis CryIA(a) insecticidal toxin. FEBS Letters, 411, 27-31.
34. Kasman, L. M.; Lukowiak, A. A.; Garczynski, S. F.; Mcnall, R. J.; Youngman, P.; Adang, M. J. (1998). Phage display of a biologically active Bacillus thuringiensis toxin phage display of a biologically active Bacillus thuringiensis Toxin. Applied and Environmental Microbiology, 64, 2995-3003.
35. Vilchez, S.; Jacoby, J.; Ellar, D. J. (2004). Display of biologically functional insecticidal toxin on the surface of lambda phage. Applied and Environmental Microbiology, 70, 6587-6594.
36. Pacheco, S.; Gomez, I.; Sato, R.; Bravo, A.; Soberon, M. (2006). Functional display of Bacillus thuringiensis Cry1Ac toxin on T7 phage. Journal of Invertebrate Pathology, 92, 45-49.
37. Craveiro, K. I.; Gomes Junior, J. E.; Silva, M. C.; Macedo, L. L.; Lucena, W. A.; Silva, M. S.; et al. (2010). Variant Cry1Ia toxins generated by DNA shuffling are active against sugarcane giant borer. Journal of Biotechnology, 145, 215-221.
38. Oliveira, G. R.; Silva, M. C.; Lucena, W. A.; Nakasu, E. Y.; Firmino, A. A.; Beneventi, M. A.; et al. (2011). Improving Cry8Ka toxin activity towards the cotton boll weevil (Anthonomus grandis). BMC Biotechnology, 11, 85.
39. Ishikawa, H.; Hoshino, Y.; Motoki, Y.; Kawahara, T.; Kitajima, M.; Kitami, M.; et al. (2007). A system for the directed evolution of the insecticidal protein from Bacillus thuringiensis. Molecular Biotechnology, 36, 90-101.
40. Obata, F.; Kitami, M.; Inoue, Y.; Atsumi, S.; Yoshizawa, Y.; Sato, R. (2009). Analysis of the region for receptor binding and triggering of oligomerization on Bacillus thuringiensis Cry1Aa toxin. FEBS Journal, 276, 5949-5959.
41. Hara, H.; Atsumi, S.; Yaoi, K.; Nakanishi, K.; Higurashi, S.; Miura, N.; et al. (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 Letters, 538, 29-34.
42. Hawkins, R. E.; Russell, S. J.; Winter, G. (1992). Selection of phage antibodies by binding affinity. Mimicking affinity maturation. Journal of Molecular Biology, 226, 889-896.
43. Schier, R.; Bye, J.; Apell, G.; McCall, A.; Adams, G. P.; Malmqvist, M.; et al. (1996). Isolation of high-affinity monomeric human anti-c-erbB-2 single chain Fv using affinity-driven selection. Journal of Molecular Biology, 255, 28-43.
44. Schier, R.; McCall, A.; Adams, G. P.; Marshall, K. W.; Merritt, H.; Yim, M.; et al. (1996). Isolation of picomolar affinity anti-c-erbB-2 single-chain Fv by molecular evolution of the complementarity determining regions in the center of the antibody binding site. Journal of Molecular Biology, 263, 551-567.
45. Thompson, J.; Pope, T.; Tung, J. S.; Chan, C.; Hollis, G.; Mark, G.; et al. (1996). Affinity maturation of a high-affinity human monoclonal antibody against the third hypervariable loop of human immunodeficiency virus: use of phage display to improve affinity and broaden strain reactivity. Journal of Molecular Biology, 256, 77-88.
46. Gomez, I.; Arenas, I.; Benitez, I.; Miranda-Rios, J.; Becerril, B.; Grande, R.; et al. (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. The Journal of Biological Chemistry, 281, 34032-34039.
47. Yaoi, K.; Kadotani, T.; Kuwana, H.; Shinkawa, A.; Takahashi, T.; Iwahana, H.; et al. (1997). Aminopeptidase N from Bombyx mori as a candidate for the receptor of Bacillus thuringiensis Cry1Aa toxin. European Journal of Biochemistry, 246, 652-657.
48. Yaoi, K.; Nakanishi, K.; Kadotani, T.; Imamura, M.; Koizumi, N.; Iwahara, H.; et al. (1999). Bacillus thuringiensis Cry1Aa toxin-binding region of Bombyx mori aminopeputidase N. FEBS Letters, 463, 221-224.
49. Jurat-Fuentes, J. L.; Adang, M. J. (2004). Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. European Journal of Biochemistry, 271, 3127-3135.
50. Hossain, D. M.; Shitomi, Y.; Moriyama, K.; Higuchi, M.; Hayakawa, T.; Mitsui, T.; et al. (2004). Characterization of a novel plasma membrane protein, expressed in the midgut epithelia of Bombyx mori, that binds to Cry1A toxins. Applied and Environmental Microbiology, 70, 4604-4612.
51. Pacheco, S.; Gomez, I.; Arenas, I.; Saab-Rincon, G.; Rodriguez-Almazan, C.; Gill, S. S.; et al. (2009). Domain II loop3 of Bacillus thuringiensis Cry1Ab toxin is involved in a "ping pong" binding mechanism with Manduca sexta aminopeptidase-N and cadherin receptors. The Journal of Biological Chemistry, 284, 32750-32757.
52. Atsumi, S.; Mizuno, E.; Hara, H.; Nakanishi, K.; Kitami, M.; Miura, N.; et al. (2005). Location of the Bombyx mori Aminopeptidase N Type 1 Binding Site on Bacillus thuringiensis Cry1Aa Toxin. Applied and Environmental Microbiology, 71, 3966-3977.
53. Burton, S. L.; Ellar, D. J.; Li, J.; Derbyshire, D. J. (1999). N-acetylgalactosamine on the putative insect receptor aminopeptidase N is recognised by a site on the domain III lectin-like fold of a Bacillus thuringiensis insecticidal toxin. Journal of Molecular Biology, 287, 1011-1022.
54. de Maagd, R. A.; Bakker, P. L.; Masson, L.; Adang, M. J.; Sangadala, S.; Stiekema, W.; et al. (1999). Domain III of the Bacillus thuringiensis delta-endotoxin Cry1Ac is involved in binding to Manduca sexta brush border membranes and to its purified aminopeptidase N. Molecular Microbiology, 31, 463-471.
55. Jenkins, J. L.; Lee, M. K.; Sangadala, S.; Adang, M. J.; Dean, D. H. (1999). Binding of Bacillus thuringiensis Cry1Ac toxin to Manduca sexta aminopeptidase-N receptor is not directly related to toxicity. FEBS Letters, 462, 373-376.
56. Kitami, M.; Kadotani, T.; Nakanishi, K.; Atsumi, S.; Higurashi, S.; Ishizaka, T.; et al. (2011). Bacillus thuringiensis Cry Toxins Bound Specifically to Various Proteins via Domain III, Which Had a Galactose-Binding Domain-Like Fold. Bioscience, Biotechnology, and Biochemistry, 75, 305-312.
57. Wolfersberger, M. G. (1990). The toxicity of two Bacillus thuringiensis delta-endotoxins to gypsy moth larvae is inversely related to the affinity of binding sites on midgut brush border membranes for the toxins. Experientia, 46, 475-477.
58. Liang, Y.; Patel, S. S.; Dean, D. H. (1995). Irreversible binding kinetics of Bacillus thuringiensis CryIA delta-endotoxins to gypsy moth brush border membrane vesicles is directly correlated to toxicity. The Journal of Biological Chemistry, 270, 24719-24724.
59. Tanaka, S.; Miyamoto, K.; Noda, H.; Jurat-Fuentes, J. L.; Yoshizawa, Y.; Endo, H.; Sato, R. ABC transporter C2 functions both independently and cooperatively with cadherin-like protein as a receptor for Cry toxins (submitted).