Bacillus thuringiensis: A story of a successful bioinsecticide

Abdullah, 2006, Identification of a Bacillus thuringiensis Cry11Ba toxin-binding aminopeptidase from the mosquito, Anopheles quadrimaculatus, BMC Biochem., 22, 7

Atsumi, 2008, Location of the Bombyx mori 175kDa cadherin-like protein-binding site on Bacillus thuringiensis Cry1Aa toxin, FEBS J., 275, 4913, 10.1111/j.1742-4658.2008.06634.x

Arenas, 2010, Role of alkaline phosphatase from Manduca sexta in the mechanism of action of Bacillus thuringiensis Cry1Ab toxin, J. Biol. Chem., 285, 12497, 10.1074/jbc.M109.085266

Bagla, 2010, Hardy cotton-munching pests are latest blow to GM crops, Science, 327, 1439, 10.1126/science.327.5972.1439

Bayyareddy, 2009, Proteomic identification of Bacillus thuringiensis subsp. israelensis toxin Cry4Ba binding proteins in midgut membranes from Aedes (Stegomyia) aegypti Linnaeus (Diptera, Culicidae) larvae, Insect Biochem. Mol. Biol., 39, 279, 10.1016/j.ibmb.2009.01.002

Bel, 2006, Common genomic structure for the Lepidoptera cadherin-like genes, Gene, 381, 71, 10.1016/j.gene.2006.07.001

Bellier, 2009, Hypoxia and the hypoxic response pathway protect against pore-forming toxins in C. elegans, PLoS Pathogen., 5, e1000689, 10.1371/journal.ppat.1000689

Bischof, 2008, Activation of the unfolded protein response is required for defenses against bacterial pore-forming toxin in vivo, PLoS Pathogens., 4, e1000176, 10.1371/journal.ppat.1000176

Boonserm, 2005, Crystal Structure of the Mosquito-larvicidal Toxin Cry4Ba and Its biological implications, J. Mol. Biol., 348, 363, 10.1016/j.jmb.2005.02.013

Boonserm, 2006, Structure of the functional form of the mosquito larvicidal Cry4Aa toxin from Bacillus thuringiensis at a 2.8-Å resolution, J. Bacteriol., 188, 3391, 10.1128/JB.188.9.3391-3401.2006

Bravo, 1997, Phylogenetic relationships of Bacillus thuringiensis d-endotoxin family proteins and their functional domains, J. Bacteriol., 179, 2793, 10.1128/jb.179.9.2793-2801.1997

Bravo, 2005, Bacillus thuringiensis mechanisms and use, 175

Bravo, 2007, Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control, Toxicon, 49, 423, 10.1016/j.toxicon.2006.11.022

Bravo, 2008, How to cope with resistance to Bt toxins?, Trends Biotechnol., 26, 573, 10.1016/j.tibtech.2008.06.005

Cancino-Rodezno, 2010, The mitogen-activated protein kinase p38 p.thway is involved in insect defense against Cry toxins from Bacillus thuringiensis, Insect Biochem. Mol. Biol., 40, 58, 10.1016/j.ibmb.2009.12.010

Cantón, 2011, Binding of Bacillus thuringiensis subsp. israelensis Cry4Ba to Cyt1Aa has an important role in synergism, Peptides, 32, 595, 10.1016/j.peptides.2010.06.005

Chen, 2007, Synergism of Bacillus thuringiensis toxins by a fragment of a toxin-binding cadherin, Proc. Natl. Acad. Sci. U.S.A., 104, 13901, 10.1073/pnas.0706011104

Chen, 2009, Identification and characterization of Aedes aegypti aminopeptidase N as a putative receptor of Bacillus thuringiensis Cry11A toxin, Insect Biochem. Mol. Biol., 39, 688, 10.1016/j.ibmb.2009.08.003

Chen, 2009, Aedes aegypti cadherin serves as a putative receptor of the Cry11Aa toxin from Bacillus thuringiensis subsp. Israelensis, Biochem. J., 424, 191, 10.1042/BJ20090730

Chen Cha, 2010, WWP-1 is a novel modulator of the DAF-2 insulin-like signaling network involved in pore-forming toxin cellular defenses in Caenorhabditis elegans, PLoS One, 5, e9494, 10.1371/journal.pone.0009494

Cohen, 2008, High-resolution crystal of activated Cyt2Ba monomer from Bacillus thuringiensis subs, Israelensis. J. Mol. Biol., 380, 820, 10.1016/j.jmb.2008.05.010

Crickmore

Christou, 2006, Recent developments and future prospects in insect pest control in transgenic crops, Trends Plant Sci., 11, 302, 10.1016/j.tplants.2006.04.001

de Maagd, 2000, Domain III substitution in Bacillus thuringiensis delta-endotoxin Cry1C domain III can function as a specific determinant for Spodoptera exigua in different, but not all, Cry1-Cry1C hybrids, Appl. Environ. Microbiol., 66, 1559, 10.1128/AEM.66.4.1559-1563.2000

de Maagd, 2001, How Bacillus thuringiensis has evolved specific toxins to colonize the insect world, Trends Genet., 17, 193, 10.1016/S0168-9525(01)02237-5

Devine, 2007, Insecticide use: contexts and ecological consequences, Agr. Hum. Values, 24, 281, 10.1007/s10460-007-9067-z

Estruch, 1996, Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects, Proc. Natl. Sci. U.S.A., 93, 5389, 10.1073/pnas.93.11.5389

Fabrick, 2009, A novel Tenebrio molitor cadherin is a functional receptor for Bacillus thuringiensis Cry3Aa toxin, J. Biol. Chem., 284, 18401, 10.1074/jbc.M109.001651

Fernández, 2005, Cry11Aa toxin from Bacillus thuringiensis binds its receptor in Aedes aegypti mosquito larvae through loop α-8 of domain II, FEBS Lett., 579, 3508, 10.1016/j.febslet.2005.05.032

Fernández, 2006, A GPI-anchored alkaline phosphatase is a functional midgut receptor of Cry11Aa toxin in Aedes aegypti larvae, Biochem. J., 394, 77, 10.1042/BJ20051517

Fernández, 2009, Cloning and epitope mapping of Cry11Aa-binding sites in the Cry11Aa-receptor alkaline phosphatase from Aedes aegypti, Biochemistry, 48, 8899, 10.1021/bi900979b

Fernández-Luna, 2010, An α-amylase is a novel receptor for Bacillus thuringiensis subsp. israelensis Cry4Ba and Cry11Aa toxins in the malaria vector mosquito Anopheles albimanus (Diptera: Culicidae), Environ. Microbiol., 12, 746, 10.1111/j.1462-2920.2009.02117.x

Franklin, 2009, Modified Bacillus thuringiensis toxins and a hybrid B. thuringiensis strain counter greenhouse-selected resistance in Trichoplusia ni, Appl. Environ. Microbiol., 75, 5739, 10.1128/AEM.00664-09

Gahan, 2001, Identification of a gene associated with Bt resistance in Heliothis virescens, Science, 293, 857, 10.1126/science.1060949

Gahan, 2010, An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin, PLoS Genet., 6, e1001248, 10.1371/journal.pgen.1001248

Galitsky, 2001, Structure of the insecticidal bacterial d-endotoxin Cry3Bb1 of Bacillus thuringiensis, Acta Cryst., D57, 1101

Garczynski, 2000, Investigations of Bacillus thuringiensis Cry1 toxin receptor structure and function, 181

Gómez, 2002, Cadherin-like 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, 10.1016/S0014-5793(02)02321-9

Gómez, 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, J. Biol. Chem., 281, 34032, 10.1074/jbc.M604721200

Griffitts, 2003, Resistance to a bacterial toxin is mediated by removal of a conserved glycosylation pathway required for toxin–host interactions, J. Biol. Chem., 278, 45594, 10.1074/jbc.M308142200

Griffits, 2005, Glycolipids as receptors for Bacillus thuringiensis crystal toxin, Science, 307, 922, 10.1126/science.1104444

Griffits, 2005, Many roads to resistance: how invertebrates adapt to Bt toxins, BioEssays, 27, 614, 10.1002/bies.20239

Grochulski, 1995, Bacillus thuringiensis CryIA(a) insecticidal toxin: crystal structure and channel formation, J. Mol. Biol., 254, 447, 10.1006/jmbi.1995.0630

Gunning, 2005, New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin, Appl. Environ. Microbiol., 71, 2558, 10.1128/AEM.71.5.2558-2563.2005

Guo, 2009, Crystal structure of Bacillus thuringiensis Cry8Ea1: An insecticidal toxin toxic to underground pests, the larvae of Holotrichia parallela, J. Struct. Biol., 168, 259, 10.1016/j.jsb.2009.07.004

Hernández-Martínez, 2010, Constitutive activation of the midgut response to Bacillus thuringiensis in Bt resistant Spodoptera exigua, PLoS One, 5, e12795, 10.1371/journal.pone.0012795

Herrero, 2005, Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four Aminopeptidase N genes, BMC Genomics, 24, 6

Hua, 2008, Anopheles gambiae cadherin AgCad1 binds the Cry4Ba toxin of Bacillus thuringiensis israelensis and a fragment of AgCad1 synergizes toxicity, Biochemistry, 47, 5101, 10.1021/bi7023578

Hua, 2009, Anopheles gambiae alkaline phosphatase is a functional receptor of Bacillus thuringiensis jegathesan Cry11Ba toxin, Biochemistry, 48, 9785, 10.1021/bi9014538

Huffman, 2004, Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins, Proc. Natl. Acad. Sci. U.S.A., 101, 10995, 10.1073/pnas.0404073101

James, 2009

Janmaat, 2003, Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Tricoplusia ni, Proc. R. Soc. Lond., B270, 2263, 10.1098/rspb.2003.2497

Jiménez-Juárez, 2007, Bacillus thuringiensis Cry1Ab mutants affecting oligomer formation are non-toxic to Manduca sexta larvae, J. Biol. Chem., 282, 21222, 10.1074/jbc.M701314200

Jurat-Fuentes, 2004, The HevCaLP protein mediates binding specificity of the Cry1A class of Bacillus thuringiensis toxins in Heliothis virescens, Biochemistry, 43, 14299, 10.1021/bi048500i

Khasdan, 2001, Toxicity and synergism in transgenic Escheichia coli expressing four genes from Bacillus thuringiensis subsp. israeliensis, Environ. Microbiol., 3, 798, 10.1046/j.1462-2920.2001.00253.x

Krishnamoorthy, 2007, Identification of novel Cry1Ac binding proteins in midgut membranes from Heliothis virescens using proteomic analyses, Insect Biochem. Mol. Biol., 37, 189, 10.1016/j.ibmb.2006.10.004

Li, 1991, Crystal structure of insecticidal δ-endotoxin from Bacillus thuringiensis at 2.5 Å resolution, Nature, 353, 815, 10.1038/353815a0

Likitvivatanavong, 2010, Role of cadherin, alkaline phosphatase and aminopeptidase N as receptors of Cry11Ba toxin from Bacillus thuringiensis jegathesan in Aedes aegypti, Appl. Environ. Microbiol

Ma, 2005, Is the mature endotoxin Cry1Ac from Bacillus thuringiensis inactivated by a coagulation reaction in the gut lumen of resistant Helicoverpa armigera larvae?, Insect Biochem. Mol. Biol., 35, 729, 10.1016/j.ibmb.2005.02.011

Margalith, 2000, Biological control by Bacillus thuringiensis subsp. israeliensis, 243

Martins, 2010, Midgut GPI-anchored proteins with alkaline phosphatase activity from the cotton boll weevil (Anthonomus grandis) are putative receptors for the Cry1B protein of Bacillus thuringiensis, Insect Biochem. Mol. Biol., 40, 138, 10.1016/j.ibmb.2010.01.005

McGaughey, 1985, Insect resistance to the biological insecticide Bacillus thuringiensis, Science, 229, 193, 10.1126/science.229.4709.193

McNall, 2003, Identification of novel Bacillus thuringiensis Cry1Ac binding proteins in Manduca sexta midgut through proteomic analysis, Insect Biochem. Mol. Biol., 33, 999, 10.1016/S0965-1748(03)00114-0

Morin, 2003, Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm, Proc. Nat. Acad. Sci. U.S.A., 100, 5004, 10.1073/pnas.0831036100

Morse, 2001, Structure of Cry2Aa suggests an unexpected receptor binding epitope, Structure, 9, 409, 10.1016/S0969-2126(01)00601-3

Muñoz-Garay, 2009, Characterization of the mechanism of action of the genetically modified Cry1AbMod toxin that is active against Cry1Ab-resistant insects, Biochim. Biophys. Acta. Biomemb., 1788, 2229, 10.1016/j.bbamem.2009.06.014

Ochoa-Campuzano, 2007, An ADAM metalloprotease is a Cry3Aa Bacillus thuringiensis toxin receptor, Biochem. Biophys. Res. Commun., 362, 437, 10.1016/j.bbrc.2007.07.197

Oppert, 1997, Proteinase-mediated insect resistance to Bacillus thuringiensis toxins, J. Biol. Chem., 272, 23473, 10.1074/jbc.272.38.23473

Ounjai, 2007, Two conformational states of the membrane-associated Bacillus thuringiensis Cry4Ba delta-endotoxin complex revealed by electron crystallography: implications for toxin-pore formation, Biochem. Biophys. Res. Commun., 361, 890, 10.1016/j.bbrc.2007.07.086

Pacheco, 2009, Enhancement of insecticidal activity of Bacillus thuringiensis Cry1A toxins by fragments of a toxin-binding cadherin correlates with oligomer formation, Peptides, 30, 583, 10.1016/j.peptides.2008.08.006

Pacheco, 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, 10.1074/jbc.M109.024968

Pandian, 2008, Bombyx mori midgut membrane protein P252 which binds to Cry1A of Bacillus thuringiensis is a chlorophyllide binding protein and its resulting complex has antimicrobial activity, Appl. Environ. Microbiol., 74, 1324, 10.1128/AEM.01901-07

Pardo-López, 2006, Structural changes of the Cry1Ac oligomeric pre-pore from Bacillus thuringiensis induced by N-acetylgalactosamine facilitates toxin membrane insertion, Biochemistry, 45, 10329, 10.1021/bi060297z

Park, 2009, Cadherin fragments from Anopheles gambiae synergize Bacillus thuringiensis Cry4Ba’s toxicity against Aedes aegypti larvae, Appl. Environ. Microbiol., 75, 7280, 10.1128/AEM.01870-09

Park, 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, 10.1128/AEM.00268-09

Pérez, 2005, Bacillus thuringiensis subsp. israeliensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor, Proc. Natl. Acad. Sci. U.S.A., 102, 18303, 10.1073/pnas.0505494102

Pérez, 2007, Bacillus thuringiensis subsp. israelensis Cyt1Aa enhances activity of Cry11Aa toxin by facilitating the formation of a pre-pore oligomeric structure, Cell. Microbiol., 9, 2931, 10.1111/j.1462-5822.2007.01007.x

Pigott, 2007, Role of receptors in Bacillus thuringiensis crystal toxin activity, Microbiol. Mol. Biol. Rev., 71, 255, 10.1128/MMBR.00034-06

Raymond, 2010, Bacillus thuringiensis: an impotent pathogen?, Trends Microbiol., 18, 189, 10.1016/j.tim.2010.02.006

Rodríguez-Almazan, 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, 10.1371/journal.pone.0005545

Soberón, 2007, Engineering modified Bt toxins to counter insect resistance, Science, 318, 1640, 10.1126/science.1146453

Soberón, 2009, Signaling versus punching hole: how do Bacillus thuringiensis toxins kill insect midgut cells?, Cell. Mol. Life Sci., 66, 1337, 10.1007/s00018-008-8330-9

Storer, 2010, Discovery and characterization of field resistance to Bt Maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico, J. Econ. Entomol., 103, 1031, 10.1603/EC10040

Tabashnik, 1994, Evolution of resistance to Bacillus thuringiensis, Annu. Rev. Entomol., 39, 47, 10.1146/annurev.en.39.010194.000403

Tabashnik, 2008, Insect resistance to Bt crops: evidence versus theory, Nat. Biotechnol., 26, 199, 10.1038/nbt1382

Tabashnik, 2010, Supressing resistance to Bt cotton with sterile insect releases, Nat. Biotechnol, 10.1038/nbt.1704

Taveecharoenkool, 2010, Combined molecular dynamics and continuum solvent Studies of the pre-pore Cry4Aa trimer suggest its stability in solution and how it may form a pore, PMC Biophys., 3, 1, 10.1186/1757-5036-3-10

van Rensburg, 2007, First report of field resistance by stem borer Busseola fusca (Fuller) to Bt-transgenic maize, S. Afr. J. Plant Soil, 24, 147, 10.1080/02571862.2007.10634798

Walters, 2010, Lepidopteran-active variable-region sequence imparts coleopteran activity in eCry3.1Ab, an engineered Bacillus thuringiensis hybrid insecticidal protein, Appl. Environ. Microbiol., 76, 3082, 10.1128/AEM.00155-10

Warren, 1997, Vegetative insecticidal proteins: novel proteins for control of corn pests, 109

Wirth, 1997, CytA enables CryIV endotoxins of Bacillus thuringiensis to overcome high levels of CryIV resistance in the mosquito, Culex, Proc. Natl. Acad. Sci. U.S.A., 94, 10536, 10.1073/pnas.94.20.10536

Xie, 2005, Single amino acid mutations in the cadherin receptor from Heliothis virescens affect its toxin binding ability to Cry1A toxins, J. Biol. Chem., 280, 8416, 10.1074/jbc.M408403200

Xu, 2005, Disruption of a cadherin gene associated with resistance to Cry1Ac delta-endotoxin of Bacillus thuringiensis in Helicoverpa armigera, Appl. Environ. Microbiol., 71, 948, 10.1128/AEM.71.2.948-954.2005

Zhang, 2008, A 106-kDa aminopeptidase is a putative receptor for Bacillus thuringiensis Cry11Ba toxin in the mosquito Anopheles gambiae, Biochemistry, 47, 11263, 10.1021/bi801181g

Zhang, 2010, Synergistic and inhibitory effects of aminopeptidase peptides on Bacillus thuringiensis Cry11Ba toxicity in the mosquito Anopheles gambiae, Biochemistry, 10.1021/bi1009908

Zhang, 2009, Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin, Insect Biochem. Mol. Biol., 39, 421, 10.1016/j.ibmb.2009.04.003

Zhang, 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, 10.1073/pnas.0604017103