Differential role of manduca sexta aminopeptidase-N and alkaline phosphatase in the mode of action of Cry1Aa, Cry1Ab, and Cry1Ac toxins from Bacillus thuringiensis

Applied and Environmental Microbiology

Volumn 79, Issue 15, 2013, Pages 4543-4550

  Flores Escobar, Biviana ^a   Rodríguez Magadan, Hector ^a   Bravo, Alejandra ^a   Soberón, Mario ^a   Gómez, Isabel ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; BINARY ALLOYS; CELL MEMBRANES; CLONING; ESCHERICHIA COLI; METABOLITES; PHOSPHATASES; PROTEINS; RNA; SURFACE PLASMON RESONANCE; TOXIC MATERIALS; TOXICITY;

ALKALINE PHOSPHATASE; BACILLUS THURINGIENSIS; BACILLUS THURINGIENSIS SUBSP. KURSTAKI; BRUSH BORDER MEMBRANE VESICLES; DOUBLE-STRANDED RNA; INSECTICIDAL PROTEIN; LARVAL DEVELOPMENT; LIGAND BLOT ANALYSIS;

BINS;

BACILLUS THURINGIENSIS; BACILLUS THURINGIENSIS SEROVAR KURSTAKI; ESCHERICHIA COLI; MANDUCA SEXTA;

ALKALINE PHOSPHATASE; BACTERIAL PROTEIN; DOUBLE STRANDED RNA; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; MICROSOMAL AMINOPEPTIDASE; RECOMBINANT PROTEIN;

ANIMAL; ARTICLE; BACILLUS THURINGIENSIS; CHEMISTRY; DOWN REGULATION; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; MANDUCA; METABOLISM; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

ALKALINE PHOSPHATASE; ANIMALS; ANTIGENS, CD13; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; DOWN-REGULATION; ENDOTOXINS; GENE KNOCKDOWN TECHNIQUES; HEMOLYSIN PROTEINS; LARVA; MANDUCA; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS; RNA INTERFERENCE; RNA, DOUBLE-STRANDED;

EID: 84885943293     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01062-13     Document Type: Article

References (32)

1. Bravo A, Likitvivatanavong S, Gill SS, Soberon M. 2011. Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem. Mol. Biol. 41:423-431
2. Tabashnik BE, Van Rensburg JB, Carriere Y. 2009. Field-evolved insect resistance to Bt crops: definition, theory, and data. J. Econ. Entomol. 102: 2011-2025
3. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:775-806
4. Soberón M, Pardo L, Munoz-Garay C, Sanchez J, Gomez I, Porta H, Bravo A. 2010. Pore formation by Cry toxins. Adv. Exp. Med. Biol. 677: 127-142
5. Gómez I, Sanchez J, Miranda R, Bravo A, Soberon M. 2002. Cadherinlike receptor binding facilitates proteolytic cleavage of helix alpha-1 in domain I and oligomer pre-pore formation of Bacillus thuringiensis Cry1Ab toxin. FEBS Lett. 513:242-246
6. Pigott CR, Ellar DJ. 2007. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 71:255-281
7. Arenas I, Bravo A, Soberon M, Gomez I. 2010. Role of alkaline phosphatase from Manduca sexta in the mechanism of action of Bacillus thuringiensis Cry1Ab toxin. J. Biol. Chem. 285:12497-12503
8. Pacheco S, Gomez I, Arenas I, Saab-Rincon G, Rodriguez-Almazan C, Gill SS, Bravo A, Soberon M. 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
9. Soberón M, Gill SS, Bravo A. 2009. Signaling versus punching hole: how do Bacillus thuringiensis toxins kill insect midgut cells? Cell. Mol. Life Sci. 66:1337-1349
10. Zhang X, Candas M, Griko NB, Taussig R, and Bulla LA, Jr. 2006. A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc. Natl. Acad. Sci. U. S. A. 103:9897-9902
11. Nagamatsu 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 CryIAa toxin. FEBS Lett. 460:385-390
12. Fabrick J, Oppert C, Lorenzen MD, Morris K, Oppert B, Jurat-Fuentes JL. 2009. A novel Tenebrio molitor cadherin is a functional receptor for Bacillus thuringiensis Cry3Aa toxin. J. Biol. Chem. 284: 18401-18410
13. Soberón M, Pardo-Lopez L, Lopez I, Gomez I, Tabashnik BE, Bravo A. 2007. Engineering modified Bt toxins to counter insect resistance. Science 318:1640-1642
14. Gill M, Ellar D. 2002. Transgenic Drosophila reveals a functional in vivo receptor for the Bacillus thuringiensis toxin Cry1Ac1. Insect Mol. Biol. 11:619-625
15. Rajagopal R, Sivakumar S, Agrawal N, Malhotra P, Bhatnagar RK. 2002. Silencing of midgut aminopeptidase N of Spodoptera litura by doublestranded RNA establishes its role as Bacillus thuringiensis toxin receptor. J. Biol. Chem. 277:46849-46851
16. Burton SL, Ellar DJ, Li J, Derbyshire DJ. 1999. N-Acetylgalactosamine on the putative insect receptor aminopeptidaseNis recognised by a site on the domain III lectin-like fold of a Bacillus thuringiensis insecticidal toxin. J. Mol. Biol. 287:1011-1022
17. You TH, Lee MK, Jenkins JL, Alzate O, Dean DH. 2008. Blocking binding of Bacillus thuringiensis Cry1Aa to Bombyx mori cadherin receptor results in only a minor reduction of toxicity. BMC Biochem. 9:3. doi:10.1186/1471-2091-9-3
18. Jurat-Fuentes JL, Karumbaiah L, Jakka SR, Ning C, Liu C, Wu K, Jackson J, Gould F, Blanco C, Portilla M, Perera O, Adang M. 2011. Reduced levels of membrane-bound alkaline phosphatase are common to lepidopteran strains resistant to Cry toxins from Bacillus thuringiensis. PLoS One 6:e17606. doi:10.1371/journal.pone.0017606
19. Hofte H, Whiteley HR. 1989. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol. Rev. 53:242-255
20. de Maagd RA, Bakker PL, Masson L, Adang MJ, Sangadala S, Stiekema W, Bosch D. 1999. Domain III of the Bacillus thuringiensis deltaendotoxin Cry1Ac is involved in binding to Manduca sexta brush border membranes and to its purified aminopeptidase N. Mol. Microbiol. 31: 463-471
21. Lereclus D, Arantes O, Chaufaux J, Lecadet M. 1989. Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol. Lett. 51:211-217
22. Arantes O, Lereclus D. 1991. Construction of cloning vectors for Bacillus thuringiensis. Gene 108:115-119
23. Lereclus D, Agaisse H, Gominet M, Chaufaux J. 1995. Overproduction of encapsulated insecticidal crystal proteins in a Bacillus thuringiensis spo0A mutant. Biotechnology 13:67-71
24. Thomas WE, Ellar DJ. 1983. Bacillus thuringiensis var. israelensis crystal delta-endotoxin: effects on insect and mammalian cells in vitro and in vivo. J. Cell Sci. 60:181-197
25. Bradford MM. 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
26. Wolfersberger MG. 1993. Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the gypsy moth (Lymantria dispar). Arch. Insect Biochem. Physiol. 24:139-147
27. Pauchet Y, Wilkinson P, Vogel H, Nelson DR, Reynolds SE, Heckel DG, Ffrench-Constant RH. 2010. Pyrosequencing the Manduca sexta larval midgut transcriptome: messages for digestion, detoxification and defence. Insect Mol. Biol. 19:61-75
28. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
29. Masson L, Lu YJ, Mazza A, Brousseau R, Adang MJ. 1995. The CryIA(c) receptor purified from Manduca sexta displays multiple specificities. J. Biol. Chem. 270:20309-20315
30. Jiménez AI, Reyes EZ, Cancino-Rodezno A, Bedoya-Perez LP, Caballero-Flores GG, Muriel-Millan LF, Likitvivatanavong S, Gill SS, Bravo A, Soberon M. 2012. Aedes aegypti alkaline phosphatase ALP1 is a functional receptor of Bacillus thuringiensis Cry4Ba and Cry11Aa toxins. Insect Biochem. Mol. Biol. 42:683-689
31. Chen J, Brown MR, Hua G, Adang MJ. 2005. Comparison of the localization of Bacillus thuringiensis Cry1A delta-endotoxins and their binding proteins in larval midgut of tobacco hornworm, Manduca sexta. Cell Tissue Res. 321:123-129
32. Perera OP, Willis JD, Adang MJ, Jurat-Fuentes JL. 2009. Cloning and characterization of the Cry1Ac-binding alkaline phosphatase (HvALP) from Heliothis virescens. Insect Biochem. Mol. Biol. 39:294-302