Insect tolerance to the crystal toxins Cry1Ac and Cry2Ab is mediated by the binding of monomeric toxin to lipophorin glycolipids causing oligomerization and sequestration reactions

Developmental and Comparative Immunology

Volumn 37, Issue 1, 2012, Pages 184-192

  Ma, Gang ^a   Rahman, Mahbub M ^a   Grant, Warwick ^b   Schmidt, Otto ^a   Asgari, Sassan ^c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Bacillus thuringiensis; Coagulation; Cry1Ac; Cry2Ab; Glycolipid; Lipophorin; Oligomerization

Indexed keywords

BACTERIAL TOXIN; BACTERIUM LYSATE; CRY1AC TOXIN; CRY2AB TOXIN; GLYCOLIPID; LIPOPHORIN; RECOMBINANT PROTEIN; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS THURINGIENSIS; HEMOLYMPH; INTESTINE; INTESTINE BRUSH BORDER; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PHYSICAL TOLERANCE; PLASMA; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; TOXIN TOLERANCE;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); HEXAPODA;

EID: 84859807672     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.08.017     Document Type: Article

References (43)

1. Aronson A.I., Geng C., Wu L. Aggregation of Bacillus thuringiensis Cry1A toxins upon binding to target insect larval midgut vesicles. Appl. Environ. Microbiol. 1999, 65:2503-2507.
2. Asgari S., Schmidt O. A coiled-coil region of an insect immune suppressor protein is involved in binding and uptake by hemocytes. Insect Biochem. Mol. Biol. 2002, 32:497-504.
3. Avisar D., Keller M., Gazit E., Prudovsky E., Sneh B., Zilberstein A. The role of Bacillus thuringiensis Cry1C and Cry1E separate structural domains in the interaction with Spodoptera littoralis gut epithelial bells. J. Biol. Chem. 2004, 279:15779-15786.
4. Barrows B.D., Haslam S.M., Bischof L.J., Morris H.R., Dell A., Aroian R.V. Resistance to Bacillus thuringiensis toxin in Caenorhabditis elegans from loss of fucose. J. Biol. Chem. 2007, 282:3302-3311.
5. Bradford M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem. 1976, 72:248-254.
6. Bravo A., Gomez I., Conde J., Munoz-Garay C., Sanchez J., Miranda R., et al. Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochim. Biophys. Acta (BBA) - Biomembranes 2004, 1667:38-46.
7. Bravo A., Gill S.S., Soberon M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 2007, 49:423-435.
8. Burton S.L., Ellar D.J., Li J., Derbyshire D.J. N-acetylgalactosamine on the putative insect receptor aminopeptidase N is recognized by a site on the domain III lectin-like fold of a Bacillus thuringiensis insecticidal toxin. J. Mol. Biol. 1999, 287:1011-1022.
9. Cheon H.-M., Shin S.W., Bian G., Park J.-H., Raikhel A.S. Regulation of lipid metabolism genes, lipid carrier protein lipophorin, and its receptor during immune challenge in the mosquito Aedes aegypti. J. Biol. Chem. 2006, 281:8426-8435.
10. Fernandez L., Aimanova K., Gill S.A.B., Soberon M. A GPI-anchored alkaline phosphatase is a functional midgut receptor of Cry11Aa toxin in Aedes aegypti larvae. Biochem. J. 2006, 15:77-84.
11. Gahan L.J., Gould F., Heckel D.G. Identification of a gene associated with Bt-resistance in Heliothis virescens. Science 2001, 293:857-860.
12. Gassmann A.J., Carriã̈re Y., Tabashnik B.E. Fitness costs of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 2009, 54:147-163.
13. Gazit E., Burshtein N., Ellar D.J., Sawyer T., Shai Y. Bacillus thuringiensis cytolytic toxin associates specifically with its synthetic helices a and C in the membrane bound state - implications for the assembly of oligomeric transmembrane pores. Biochemistry 1997, 36:15546-15554.
14. Gomez I., Oltean D.I., Gill S.S., Bravo A., Soberon M. Mapping the epitope in cadherin-like receptors involved in Bacillus thuringiensis Cry1A toxin interaction using phage display. J. Biol. Chem. 2001, 276:28906-28912.
15. Gomez I., Arenas I., Benitez I., Miranda-Rios J., Becerril B., Grande R., et al. 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. 2006, 281:34032-34039.
16. Griffitts J.S., Whitacre J.L., Stevens D.E., Aroian R.V. Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme. Science 2001, 293:860-864.
17. Griffitts J.S., Haslam S.M., Yang T., Garczynski S.F., Mulloy B., Morris H., et al. Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 2005, 307:922-925.
18. Hall M., Wang R., van Antwerpen R., Sottrup-Jensen L., Söderhäll K. The crayfish plasma clotting protein: a vitellogenin-related protein responsible for clot formation in crustacean blood. Proc. Natl. Acad. Sci. (USA) 1999, 96:1965-1970.
19. Hernández-Rodríguez C.S., Van Vliet A., Bautsoens N., Van Rie J., Ferré J. Specific binding of Bacillus thuringiensis Cry2A insecticidal proteins to a common site in the midgut of Helicoverpa species. Appl. Environ. Microbiol. 2008, 74:7654-7659.
20. Hofte H., Whiteley H.R. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol. Rev. 1989, 53:242-255.
21. Ideo H., Fukushima K., Gengyo-Ando K., Mitani S., Dejima K., Nomura K., et al. A Caenorhabditis elegans glycolipid-binding galectin functions in host defense against bacterial infection. J. Biol. Chem. 2009, 284:26493-26501.
22. Jimenez-Juarez N., Munroz-Garay C., Gormez I., Saab-Rincon G., Damian-Almazo J.Y., Gill S.S., et al. Bacillus thuringiensis Cry1Ab mutants affecting oligomer formation are non-toxic to Manduca sexta larvae. J. Biol. Chem. 2007, 282:21222-21229.
23. Jiménez-Juárez N., Muñoz-Garay C., Gómez I., Gill S.S., Soberón M., Bravo A. The pre-pore from Bacillus thuringiensis Cry1Ab toxin is necessary to induce insect death in Manduca sexta. Peptides 2008, 29:318-323.
24. Jurat-Fuentes J.L., Adang M.J. Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. Eur. J. Biochem. 2004, 271:3127-3135.
25. Kitov P.I., Mulvey G.L., Griener T.P., Lipinski T., Solomon D., Paszkiewicz E., et al. In vivo supramolecular templating enhances the activity of multivalent ligands: a potential therapeutic against the Escherichia coli O157 AB5 toxins. Proc. Natl. Acad. Sci. (USA) 2008, 105:16837-16842.
26. Knight P.J.K., Carroll J., Ellar D.J. Analysis of glycan structures on the 120kDa aminopeptidase N of Manduca sexta and their interactions with Bacillus thuringiensis Cry1Ac toxin. Insect Biochem. Mol. Biol. 2004, 34:101-112.
27. Lee M.K., You T.H., Gould F.L., Dean D.H. Identification of residues in domain III of Bacillus thuringiensis Cry1Ac toxin that affect binding and toxicity. Appl. Environ. Microbiol. 1999, 65:4513-4520.
28. Liao C., Heckel D., Akhurst R. Toxicity of Bacillus thuringiensis insecticidal proteins for Helicoverpa armigera and Helicoverpa punctigera (Lepidoptera: Noctuidae), major pests of cotton. J. Invertebr. Pathol. 2002, 80:55-63.
29. Ma G., Hay D., Li D., Asgari S., Schmidt O. Recognition and inactivation of LPS by lipophorin particles. Dev. Comp. Immunol. 2006, 30:619-626.
30. Obata F., Kitami M., Inoue Y., Atsumi S., Yoshizawa Y., Sato R. Analysis of the region for receptor binding and triggering of oligomerization on Bacillus thuringiensis Cry1Aa toxin. FEBS J. 2009, 276:5949-5959.
31. Rahman M.M., Roberts H.L.S., Sarjan M., Asgari S., Schmidt O. Induction and transmission of Bacillus thuringiensis tolerance in the flour moth Ephestia kuehniella. Proc. Natl. Acad. Sci. (USA) 2004, 101:2696-2699.
32. Rahman M.M., Ma G., Roberts H.L.S., Schmidt O. Cell-free immune reactions in insects. J. Insect Physiol. 2006, 52:754-762.
33. Rahman M.M., Roberts H.L.S., Schmidt O. Tolerance to Bacillus thuringiensis endotoxin in immune-suppressed larvae of the flour moth Ephestia kuehniella. J. Invertebr. Pathol. 2007, 96:125-132.
34. Rahman M., Glatz R., Roush R., Schmidt O. Developmental penalties associated with inducible tolerance in Helicoverpa armigera to insecticidal toxins from Bacillus thuringiensis. Appl. Environ. Microbiol. 2011, 77:1443-1448.
35. Rensen P.C.N., van Leeuwen S.H., Sliedregt L., van Berkel T.J.C., Biessen E.A.L. Design and synthesis of novel N-acetylgalactosamine-terminated glycolipids for targeting of lipoproteins to the hepatic asialoglycoprotein receptor. J. Med. Chem. 2004, 47:5798-5808.
36. Roush R.T., Tabashnik B.E. Pesticide Resistance in Arthropods 1990, Chapman and Hall Ltd.
37. Schmidt O., Söderhäll K., Theopold U., Faye I. The role of adhesion in immune recognition. Annu. Rev. Entomol. 2010, 55:485-504.
38. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., et al. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 1998, 62:775-806.
39. Shelton A.M., Zhao J.-Z., Roush R.T. Economic, ecological, food safety, and social consequences of the development of Bt transgenic plants. Annu. Rev. Entomol. 2002, 47:845-881.
40. Soberon M., Pardo-Lopez L., Lopez I., Gomez I., Tabashnik B.E., Bravo A. Engineering modified Bt toxins to counter insect resistance. Science 2007, 318:1640-1642.
41. Soulages J.I., Wells M.A. Lipophorin: the structure of an insect lipoprotein and its role in lipid transport in insects. Adv. Protein Chem. 1994, 45:371-415.
42. Tabashnik B.E., Unnithan G.C., Masson L., Crowder D.W., Li X., Carrière Y. Asymmetrical cross-resistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm. Proc. Natl. Acad. Sci. (USA) 2009, 106:11889-11894.
43. Tigue N.J., Jacoby J., Ellar D.J. The alpha-helix 4 residue, Asn135, is involved in the oligomerization of Cry1Ac1 and Cry1Ab5 Bacillus thuringiensis toxins. Appl. Environ. Microbiol. 2001, 67:5715-5720.