Dominant negative phenotype of bacillus thuringiensis Cry1Ab, Cry11Aa and Cry4Ba mutants suggest hetero-oligomer formation among different Cry toxins

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Carmona, Daniela ^a   Rodríguez Almazán, Claudia ^a   Muñoz Garay, Carlos ^a   Portugal, Leivi ^a   Pérez, Claudia ^a   de Maagd, Ruud A ^b   Bakker, Petra ^b   Soberón, Mario ^a   Bravo, Alejandra ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS THURINGIENSIS TOXIN; CRY11AA TOXIN; CRY1AB TOXIN; CRY1AC TOXIN; CRY1CA TOXIN; CRY1DA TOXIN; CRY1EA TOXIN; CRY1FA TOXIN; CRY4BA TOXIN; OLIGOMER; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS;

AEDES AEGYPTI; ALPHA HELIX; ARTICLE; BACILLUS THURINGIENSIS; BINDING COMPETITION; CONTROLLED STUDY; CYTOTOXICITY; IN VIVO STUDY; INSECTICIDAL ACTIVITY; LARVA; MANDUCA SEXTA; NONHUMAN; OLIGOMERIZATION; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; ANIMAL; CHEMISTRY; DOMINANT GENE; GENETICS; LEPIDOPTERA; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PROTEIN MULTIMERIZATION;

AEDES AEGYPTI; BACILLUS THURINGIENSIS; HEXAPODA; MANDUCA SEXTA;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; ENDOTOXINS; GENES, DOMINANT; HEMOLYSIN PROTEINS; MANDUCA; MUTATION; PROTEIN MULTIMERIZATION;

EID: 79956068802     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019952     Document Type: Article

References (37)

1. Bravo A, Soberón M, Gill SS, (2005) Bacillus thuringiensis: mechanism and use. In: Gilbert LI, Gill SS, Iatrou K, editors. Comprehensive Molecular Insect Science Elsevier pp. 175-206 Vol 6 ISBN: 0-44-451516-X.
2. 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.
3. Pacheco S, Gómez I, Arenas I, Saab-Rincon G, Rodríguez-Almazán C, et al. (2009) Domain II loop 3 of Bacillus thuringiensis Cry1Ab toxin is involved in a "ping pong" binding mechanism with Manduca sexta aminopetidase-N and cadherin receptors. J Biol Chem 284: 32750-32757.
4. Arenas I, Bravo A, Soberón M, Gómez 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.
5. Jiménez-Juárez N, Muñoz-Garay C, Gómez I, Saab-Rincon G, Damian-Alamazo JY, et al. (2007) Bacillus thuringiensis Cry1Ab mutants affecting oligomer formation are non toxic to Manduca sexta larvae. J Biol Chem 282: 21222-21229.
6. Girard F, Vachon V, Prefontaine G, Marceau L, Su Y, et al. (2008) Cysteine scanning mutagenesis of α-4 a putative pore lining helix of the Bacillus thuringiensis insecticidal toxin Cry1Aa. Appl Environ Microbiol 74: 2566-2572.
7. Vachon V, Prefontaine G, Coux F, Rang C, Marceau M, et al. (2002) Role of helix 3 in pore formation by Bacillus thuringiensis insecticidal toxin Cry1Aa. Biochemistry 41: 6178-6184.
8. Rodríguez-Almazán C, Zavala LE, Muñoz-Garay C, Jiménez-Juárez N, Pacheco S, et al. (2009) Dominant negative mutants of Bacillus thuringiensis Cry1Ab toxin function as anti-toxins: Demonstration of the role of oligomerization in toxicity. PloS ONE 4: e5545.
9. Mourez M, Yan M, Lacy DB, Dillon L, Bentsen L, et al. (2003) Mapping dominant-negative mutations of anthrax protective antigen by scanning mutagenesis. Proc Natl Acad Sci USA 100: 13803-13808.
10. Sellman BR, Mourez M, Collier RJ, (2001) Dominant-negative mutants of a toxin subunit: an approach to therapy of anthrax. Science 292: 695-697.
11. Wai SN, Westermark M, Oscarsson J, Jass J, Maier E, et al. (2003) Characterization of dominantly negative mutant ClyA Cytotoxin proteins in Escherichia coli. J Bacteriol 185: 5491-5499.
12. Vinion-Dubiel A, McClain MS, Czajkowsky DM, Iwamoto HYD, Cao P, et al. (1999) A dominant negative mutant of Helicobacter pylori vacuolating toxin Vac A inhibits VacA-induced cell vacuolation. J Biol Chem 274: 37736-37742.
13. Er F, Larbig R, Ludwig A, Biel M, Hofmann F, et al. (2003) Dominant-negative suppression of HCN channels markedly reduces the native pacemaker current If and undermines spontaneous beating of neonatal cardiomyocytes. Circulation 107: 485-489.
14. Hernandez-Soto A, Del Rincón-Castro MC, Espinoze AM, Ibarra JE, (2009) Parasporal body formation via overexpression of the Cry10Aa toxin of Bacillus thuringiensis subsp. israelensis and Cry10Aa-Cyt1Aa synergism. Appl Environ Microbiol 75: 4661-4667.
15. 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.
16. Chen J, Aimanova K, Fernandez L, Bravo A, Soberón M, et al. (2009) Aedes aegypti cadherin serves as a putative receptor of the Cry11Aa toxin from Bacillus thuringiensis subsp. israelensis. Biochem J 424: 191-200.
17. Abdullah MA, Valaitis AP, Dean DH, (2006) Identification of a Bacillus thuringiensis Cry11Ba toxin-binding aminopeptidase from the mosquito, Anopheles quadrimaculatus. BMC Biochem 7: 16.
18. Zhang R, Hua G, Andacht TM, Adang MJ, (2008) A 106-kDa aminopeptidase is a putative receptor for Bacillus thuringiensis Cry11Ba toxin in the mosquito Anopheles gambiae. Biochemistry 47: 11263-11272.
19. Fernandez LE, Aimanova KG, Gill SS, Bravo A, Soberón M, (2006) A GPI-anchored alkaline phosphatase is a functional midgut receptor of Cry11Aa toxin in Aedes aegypti larvae. Biochem J 394: 77-84.
20. Fernandez-Luna MT, Tabaschnik B, Lanz-Mendoza H, Bravo A, Soberón M, et al. (2010) Single-Concentration Tests Show Synergism Among Bacillus thuringiensis subsp. israelensis Toxins Against the Malaria Vector Mosquito Anopheles albimanus. J Invertebr Pathol 104: 231-233.
21. Poncet S, Delecluse A, Klier A, Rapoport G, (1995) Evaluation of synergistic interaction among CryIVA, CryIVB and CryIVD toxic components of B. thuringiensis subs israelensis crystals. J Invertebr Pathol 66: 131-135.
22. Crickmore N, Bone EJ, Williams JA, Ellar D, (1995) Contribution of the individual components of the δ-endotoxin crystal to the mosquitocidal activity of Bacillus thuringiensis subsp israelensis. FEMS microbial Lett 131: 249-254.
23. Angsuthanasombat Ch, Keeratichamreon S, Leetacheewa S, Katzenmeier G, Panyim S, (2001) Directed mutagenesis of the Bacillus thuringiensis Cry11A toxin reveals a crucial role in larvicidal activity of arginine136 in helix 4. J Biochem Mol Biol 34: 402-407.
24. Sramala I, Leetacheewa S, Krittanai Ch, Katzenmeier G, Panyim S, et al. (2001) Charged residue screening in helix 4 of the Bacillus thuringiensis Cry4B toxin reveals one critical residue for larvicidal activity. J Biochem Mol Biol Biophys 5: 219-225.
25. Canton PE, Reyes EZ, RuizdeEscudero I, Bravo A, Soberón M, (2010) Binding of Bacillus thuringiensis subsp. israelensis Cry4Ba to Cyt1Aa has an important role in synergism. Peptides 32: 595-600.
26. Muñoz-Garay C, Rodríguez-Almazán C, Aguilar JN, Portugal L, Gómez I, et al. (2009) Oligomerization of Cry11Aa from Bacillus thuringiensis has an important role in toxicity against Aedes aegypti. Appl Environ Microbiol 75: 7548-7550.
27. Taveecharoenkool T, Angsuthanasombat Ch, Kantchanawarin Ch, (2010) Combined molecular dynamics and continuum solvent studies of the pre-pore Cry4Aa trimer suggest its stability in solution and how it may form pore. PMC Biophysics 3: 1-16.
28. Singh Y, Chaudhary VK, Leppla SH, (1989) A deleted variant of Bacillus anthracis protective antigen is non-toxic and blocks anthrax toxin action in vivo. J Biol Chem 264: 19103-19107.
29. Sharma A, Nain V, Lakhanpaul S, Kumar PA, (2010) Synergistic activity between Bacillus thuringiensis Cry1Ab and Cry1Ac toxins against maize stem borer (Chilo partellus Swinhoe). Lett Appl Microbiol 51: 42-47.
30. Lee MK, Curtiss A, Alcantara E, Dean DH, (1996) Synergistic effect of the Bacillus thuringiensis toxins CryIAa and CryIAc on the Gypsy moth Lymantria dispar. Appl Environ Microbiol 62: 583-586.
31. Willrich Siebert M, Nolting S, Leonard BR, Braxton LB, All JN, et al. (2008) Efficacy of transgenic cotton expressing Cry1Ac and Cry1F insecticidal protoxin against heliothines (Lepidoptera Noctuidae). J Econ Entomol 101: 1950-1959.
32. Chang C, Yu YM, Dai SM, Law SK, Gill SS, (1993) High-level cryIVD and cytA gene expression in Bacillus thuringiensis does not require the 20-kilodalton protein and the coexpressed gene products are synergistic in their toxicity to mosquitoes. Appl Environ Microbiol 59: 815-821.
33. Delecluse A, Poncet S, Klier A, Rapoport G, (1993) Expression of cryIVA and cryIVB genes independently or in combination in a crystal negative strain of Bacillus thuringiensis subs israelensis. Appl Environ Microbiol 59: 3922-3927.
34. Arantes O, Lereclus D, (1991) Construction of cloning vectors for Bacillus thuringiensis. Gene 108: 115-119.
35. Muñoz-Garay C, Sánchez J, Darszon A, de Maagd RA, Bakker P, 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.
36. Höfte H, Grave H, Seurinck J, Jansens S, Mahillon J, et al. (1986) Structural and functional analysis of a cloned delta endotoxin of Bacillus thuringiensis berliner 1715. Eur J Biochem 161: 273-280.
37. 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.