Differential protection of Cry1Fa toxin against Spodoptera frugiperda larval gut proteases by cadherin orthologs correlates with increased synergism

Applied and Environmental Microbiology

Volumn 78, Issue 2, 2012, Pages 354-362

  Rahman, Khalidur ^a   Abdullah, Mohd Amir F ^c   Ambati, Suresh ^c   Taylor, Milton D ^c,d   Adang, Michael J ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b InsectiGen Inc ^*  (United States)

^c InsectiGen Inc   (United States)

^d U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS THURINGIENSIS; BIOPESTICIDES; BRUSH BORDER MEMBRANE VESICLES; BT TOXIN; CHEMICAL PESTICIDES; CRY PROTEINS; DIFFERENT MECHANISMS; DIFFERENTIAL PROTECTION; DISEASE VECTORS; HIGH AFFINITY; LARVAL GUT; MANDUCA SEXTA; MODE OF ACTION; ORTHOLOGS; PORE FORMATION; PROTEASE DEGRADATION; RESISTANCE MANAGEMENT; SPODOPTERA FRUGIPERDA; THURINGIENSIS;

BACTERIOLOGY; CELL MEMBRANES; METABOLITES; PEPTIDES; PLANTS (BOTANY); TOXICITY;

GLYCOPROTEINS;

BACTERIAL PROTEIN; CADHERIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; PROTEINASE INHIBITOR;

BACTERIUM; BIOLOGICAL CONTROL; BIOPESTICIDE; CROP PEST; DEGRADATION; DISEASE VECTOR; ENZYME ACTIVITY; METABOLISM; MOTH; PEPTIDE; PESTICIDE RESISTANCE; PROTEIN; STOMACH CONTENT; SYNERGISM; TOXICOLOGY; TOXIN;

ANIMAL; ARMYWORM; ARTICLE; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; ENZYMOLOGY; GASTROINTESTINAL TRACT; HUMAN; LARVA; LEPIDOPTERA;

ANIMALS; BACTERIAL PROTEINS; CADHERINS; DRUG SYNERGISM; ENDOTOXINS; GASTROINTESTINAL TRACT; HEMOLYSIN PROTEINS; HUMANS; LARVA; MANDUCA; PROTEASE INHIBITORS; SPODOPTERA;

BACILLUS THURINGIENSIS; HEXAPODA; MANDUCA SEXTA; SPODOPTERA FRUGIPERDA;

EID: 84855744304     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06212-11     Document Type: Article

References (56)

1. Abdullah MA, Moussa S, Taylor MD, Adang MJ. 2009. 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 Manag. Sci. 65: 1097-1103.
2. Aronson AI, Geng C, Wu L. 1999. Aggregation of Bacillus thuringiensis Cry1A toxins upon binding to target insect larval midgut vesicles. Appl. Environ. Microbiol. 65:2503-2507.
3. Bernard CB, Philogene BJ. 1993. Insecticide synergists: role, importance, and perspectives. J. Toxicol. Environ. Health 38:199-223.
4. Bradford 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.
5. Bravo A, et al. 2004. Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidaseNreceptor leading to insertion into membrane microdomains. Biochim. Biophys. Acta 1667:38-46.
6. Broderick NA, Goodman RM, Raffa KF, Handelsman J. 2000. Synergy between zwittermicin A and Bacillus thuringiensis subsp. kurstaki against gypsy moth (Lepidoptera: Lymantriidae). Environ. Entomol. 29:101-107.
7. Broderick NA, Raffa KF, Handelsman J. 2006. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. U. S. A. 103:15196-15199.
8. Carbone A, Zinovyev A, Kepes F. 2003. Codon adaptation index as a measure of dominating codon bias. Bioinformatics 19:2005-2015.
9. Carroll J, Ellar DJ. 1993. An analysis of Bacillus thuringiensis deltaendotoxin action on insect-midgut-membrane permeability using a lightscattering assay. Eur. J. Biochem. 214:771-778.
10. Chen J, Hua G, Jurat-Fuentes JL, Abdullah MA, Adang MJ. 2007. Synergism of Bacillus thuringiensis toxins by a fragment of a toxin-binding cadherin. Proc. Natl. Acad. Sci. U. S. A. 104:13901-13906.
11. Dorsch JA, et al. 2002. Cry1A toxins of Bacillus thuringiensis bind specif-ically 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 Biochem. Mol. Biol. 32:1025-1036.
12. Fang S, et al. 2009. Bacillus thuringiensis bel protein enhances the toxicity of Cry1Ac protein to Helicoverpa armigera larvae by degrading insect intestinal mucin. Appl. Environ. Microbiol. 75:5237-5243.
13. Finney DJ. 1971. Probit analysis, 3rd ed. Cambridge University Press, Cambridge, United Kingdom.
14. Flannagan R, Meyer T. August 2009. U.S. patent 7,572,889.
15. Gahan LJ, Gould F, Heckel DG. 2001. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293:857-860.
16. Gao Y, et al. 2011. Increased toxicity of Bacillus thuringiensis Cry3Aa against Crioceris quatuordecimpunctata, Phaedon brassicae and Colaphellus bowringi by a Tenebrio molitor cadherin fragment. Pest Manag. Sci. 67: 1076-1081.
17. Garczynski SF, Crim JW, Adang MJ. 1991. Identification of putative insect brush border membrane-binding molecules specific to Bacillus thuringiensis delta-endotoxin by protein blot analysis. Appl. Environ. Microbiol. 57:2816-2820.
18. Gill SS, Cowles EA, Pietrantonio PV. 1992. The mode of action of Bacillus thuringiensis endotoxins. Annu. Rev. Entomol. 37:615-636.
19. Hua G, Jurat-Fuentes JL, Adang MJ. 2004. Bt-R1a extracellular cadherin repeat 12 mediates Bacillus thuringiensis Cry1Ab binding and cytotoxicity. J. Biol. Chem. 279:28051-28056.
20. Hua G, Zhang R, Abdullah MA, Adang MJ. 2008. Anopheles gambiae cadherin AgCad1 binds the Cry4Ba toxin of Bacillus thuringiensis israelensis and a fragment of AgCad1 synergizes toxicity. Biochemistry 47: 5101-5110.
21. Jimenez-Juarez N, et al. 2008. The pre-pore from Bacillus thuringiensis Cry1Ab toxin is necessary to induce insect death in Manduca sexta. Peptides 29:318-323.
22. Knowles BH, Ellar DJ. 1987. Colloid-osmotic lysis is a general feature of the mechanism of action of Bacillus thuringiensis delta-endotoxins with different insect specificity. Biochim. Biophys. Acta 924:509-518.
23. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
24. Liu C, et al. 2009. Reduction of Bacillus thuringiensis Cry1Ac toxicity against Helicoverpa armigera by a soluble toxin-binding cadherin fragment. J. Insect Physiol. 55:686-693.
25. Lorence A, et al. 1995. Delta-endotoxins induce cation channels in Spodoptera frugiperda brush border membranes in suspension and in planar lipid bilayers. FEBS Lett. 360:217-222.
26. Luo K, Banks D, Adang MJ. 1999. Toxicity, binding, and permeability analyses of four Bacillus thuringiensis Cry1 delta-endotoxins using brush border membrane vesicles of Spodoptera exigua and Spodoptera frugiperda. Appl. Environ. Microbiol. 65:457-464.
27. Matten SR, Head GP, Quemada HD. 2008. How governmental regulation can help or hinder the integration of Bt crops within IPM programs, p 27-39. In Romeis J, Shelton AM, KennedyGG(ed), Integration of insect resistant genetically modified crops within IPM programs. Springer, New York, NY.
28. Miranda R, Zamudio FZ, Bravo A. 2001. Processing of Cry1Ab deltaendotoxin from Bacillus thuringiensis by Manduca sexta and Spodoptera frugiperda midgut proteases: role in protoxin activation and toxin inactivation. Insect Biochem. Mol. Biol. 31:1155-1163.
29. Munoz-Garay C, et al. 2006. Permeability changes of Manduca sexta midgut brush border membranes induced by oligomeric structures of different cry toxins. J. Membr. Biol. 212:61-68.
30. Nair MS, Dean DH. 2008. All domains of Cry1A toxins insert into insect brush border membranes. J. Biol. Chem. 283:26324-26331.
31. Oppert B, Kramer KJ, Beeman RW, Johnson D, McGaughey WH. 1997. Proteinase-mediated insect resistance to Bacillus thuringiensis toxins. J. Biol. Chem. 272:23473-23476.
32. Oppert B, Kramer KJ, Johnson DE, MacIntosh SC, McGaughey WH. 1994. Altered protoxin activation by midgut enzymes from a Bacillus thuringiensis resistant strain of Plodia interpunctella. Biochem. Biophys. Res. Commun. 198:940-947.
33. Pacheco S, et al. 2009. Domain II loop 3 of Bacillus thuringiensis Cry1Ab toxin is involved in a "ping pong" binding mechanism with Manduca sexta aminopeptidase-N and cadherin receptors. J. Biol. Chem. 284: 32750-32757.
34. Pacheco S, Gomez I, Gill SS, Bravo A, Soberon M. 2009. Enhancement of insecticidal activity of Bacillus thuringiensis Cry1A toxins by fragments of a toxin-binding cadherin correlates with oligomer formation. Peptides 30:583-588.
35. Park Y, Abdullah MA, Taylor MD, Rahman K, Adang MJ. 2009. Enhancement of Bacillus thuringiensis Cry3Aa and Cry3Bb toxicities to coleopteran larvae by a toxin-binding fragment of an insect cadherin. Appl. Environ. Microbiol. 75:3086-3092.
36. Park Y, Hua G, Abdullah MA, Rahman K, Adang MJ. 2009. Cadherin fragments from Anopheles gambiae synergize Bacillus thuringiensis Cry4Ba's toxicity against Aedes aegypti larvae. Appl. Environ. Microbiol. 75:7280-7282.
37. Peng D, Xu X, Ruan L, Yu Z, Sun M. 2010. Enhancing Cry1Ac toxicity by expression of the Helicoverpa armigera cadherin fragment in Bacillus thuringiensis. Res. Microbiol. 161:383-389.
38. Peng D, Xu X, Ye W, Yu Z, Sun M. 2009. Helicoverpa armigera cadherin fragment enhances Cry1Ac insecticidal activity by facilitating toxinoligomer formation. Appl. Microbiol. Biotechnol. 85:1033-1040.
39. Perez C, et al. 2005. Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proc. Natl. Acad. Sci. U. S. A. 102:18303-18308.
40. Perez C, et al. 2007. Bacillus thuringiensis ssp. israelensis Cyt1Aa enhances activity of Cry11Aa toxin by facilitating the formation of a pre-pore oligomeric structure. Cell. Microbiol. 9:2931-2937.
41. Peyronnet O, et al. 1997. Effect of Bacillus thuringiensis toxins on the membrane potential of lepidopteran insect midgut cells. Appl. Environ. Microbiol. 63:1679-1684.
42. Pigott CR, Ellar DJ. 2007. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 71:255-281.
43. Regev A, et al. 1996. Synergistic activity of a Bacillus thuringiensis deltaendotoxin and a bacterial endochitinase against Spodoptera littoralis larvae. Appl. Environ. Microbiol. 62:3581-3586.
44. Rosner B. 1995. Fundamentals of biostatistics, 4th ed. Duxbury Press, Belmont, CA.
45. Sayyed AH, Crickmore N, Wright DJ. 2001. Cyt1Aa from Bacillus thuringiensis subsp. israelensis is toxic to the diamondback moth, Plutella xylostella, and synergizes the activity of Cry1Ac towards a resistant strain. Appl. Environ. Microbiol. 67:5859-5861.
46. Schnepf E, et al. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:775-806.
47. Sena JA, Hernandez-Rodriguez CS, Ferre J. 2009. Interaction of Bacillus thuringiensis Cry1 and Vip3A proteins with Spodoptera frugiperda midgut binding sites. Appl. Environ. Microbiol. 75:2236-2237.
48. Storer NP, et al. 2010. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J. Econ. Entomol. 103:1031-1038.
49. Wirth MC, Federici BA, Walton WE. 2000. Cyt1A from Bacillus thuringiensis synergizes activity of Bacillus sphaericus against Aedes aegypti (Diptera: Culicidae). Appl. Environ. Microbiol. 66:1093-1097.
50. Wolfersberger M, et al. 1987. 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 Physiol. 86:301-308.
51. Wolfersberger MG, Chen XJ, Dean DH. 1996. Site-directed mutations in the third domain of Bacillus thuringiensis delta-endotoxin CryIAa affect its ability to increase the permeability of Bombyx mori midgut brush border membrane vesicles. Appl. Environ. Microbiol. 62:279-282.
52. 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. Appl. Environ. Microbiol. 71:948-954.
53. Yang Y, Chen H, Wu S, Xu X, Wu Y. 2006. Identification and molecular detection of a deletion mutation responsible for a truncated cadherin of Helicoverpa armigera. Insect Biochem. Mol. Biol. 36:735-740.
54. Zavala LE, et al. 2011. Domains II and III of Bacillus thuringiensis Cry1Ab toxin remain exposed to the solvent after insertion of part of domain I into the membrane. J. Biol. Chem. 286:19109-19117.
55. Zhang X, Candas M, Griko NB, Rose-Young L, Bulla LA, Jr. 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 Differ. 12:1407-1416.
56. Zhu YC, Adamczyk JJ, Jr, West S. 2005. Avidin, a potential biopesticide and synergist to Bacillus thuringiensis toxins against field crop insects. J. Econ. Entomol. 98:1566-1571.