Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review

References

• Abe Y, Shimada H, Kitada S. (2008). Raft-targeting and oligomerization of parasporin-2, a Bacillus thuringiensis crystal protein with anti-tumour activity. J Biochem-Tokio, 143, 269–75
   PubMed Web of Science ®Google Scholar
• Akiba T, Abe Y, Kitada S, et al. (2009). Crystal structure of the parasporin-2 Bacillus thuringiensis toxin that recognizes cancer cells. J Mol Biol, 386, 121–33
   PubMed Web of Science ®Google Scholar
• Baxter SW, Badenes-Pérez FR, Morrison A, et al. (2011). Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics, 189, 675–9
   PubMed Web of Science ®Google Scholar
• Baxter SW, Zhao JZ, Gahan LJ, et al. (2005). Novel genetic basis of field-evolved resistance to Bt toxins in Plutella xylostella. Insect Mol Biol, 14, 327–34
   PubMed Web of Science ®Google Scholar
• Beegle CC, Yamamoto T. (1992). History of Bacillus thuringiensis Berliner research and development. Can Entomol, 124, 587–616
   Web of Science ®Google Scholar
• Bhattacharya D, Nagpure A, Gupta RK. (2007). Bacterial chitinases: properties and potential. Crit Rev Biotechnol, 27, 21–8
   PubMed Web of Science ®Google Scholar
• Bonin A, Paris M, Tetreau G, et al. (2009). Candidate genes revealed by a genome scan for mosquito resistance to a bacterial insecticide: sequence and gene expression variations. BMC Genomics, 10, 551
   PubMed Web of Science ®Google Scholar
• Boyer S, Paris M, Jego S, et al. (2012). Influence of insecticide Bacillus thuringiensis subsp. israelensis treatments on resistance and enzyme activities in Aedes rusticus larvae (Diptera: Culicidae). Biol Control, 62, 75–81
   Web of Science ®Google Scholar
• Brar SK, Verma M, Tyagi RD, et al. (2008). Bacillus thuringiensis fermentation of wastewater and wastewater sludge–presence and characterization of chitinases. Environ Technol, 29, 161–70
   PubMed Web of Science ®Google Scholar
• Bravo A, Gill SS, Soberón M. (2007). Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon, 49, 423–35
   PubMed Web of Science ®Google Scholar
• Bravo A, Likitvivatanavong S, Gill SS, Soberón M. (2011). Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol, 41, 423–31
   PubMed Web of Science ®Google Scholar
• Carrière Y, Dutilleul P, Ellers-Kirk C, et al. (2004). Sources, sinks, and the zone of influence of refuges for managing insect resistance to Bt crops. Ecol Appl, 14, 1615–23
   Web of Science ®Google Scholar
• Carrière Y, Ellers-Kirk C, Hartfield K, et al. (2012). Large-scale, spatially-explicit test of the refuge strategy for delaying insecticide resistance. Proc Natl Acad Sci USA Biol, 109, 775–80
   PubMed Web of Science ®Google Scholar
• Chaiharn M, Lumyong S, Hasan N, Plikomol A. (2013). Solid-state cultivation of Bacillus thuringiensis R 176 with shrimp shells and rice straw as a substrate for chitinase production. Ann Microbiol, 63, 443–50
   Web of Science ®Google Scholar
• Chen J, Aimanova K, Fernandez L, 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
   PubMed Web of Science ®Google Scholar
• Cooper MA, Carroll J, Travis ER, et al. (1998). Bacillus thuringiensis Cry1Ac toxin interaction with Manduca sexta aminopeptidase N in a model membrane environment. Biochem J, 333, 677–83
   PubMed Web of Science ®Google Scholar
• Côté J.C. (2007). How early discoveries about Bacillus thuringiensis prejudiced subsequent research and use. In: Vincent C, Goettel MS, Lazarovits G, eds. Biological control. Wallingford: CAB International
   Google Scholar
• Dahiya N, Tewari R, Hoondal GS. (2006). Biotechnological aspects of chitinolytic enzymes: a review. Appl Microbiol Biotechnol, 71, 773–82
   PubMed Web of Science ®Google Scholar
• Dash HR, Mangwani N, Das S. (2014). Characterization and potential application in mercury bioremediation of highly mercury-resistant marine bacterium Bacillus thuringiensis PW-05. Environ Sci Pollut Res Int, 21, 2642--53
   Google Scholar
• Dorsch JA, Candas M, Griko NB, et al. (2002). Cry1A toxins of Bacillus thuringiensis bind specifically to a region adjacent to the membrane-proximal extracellular domain of Bt-R1 in Manduca sexta: involvement of a cadherin in the entomopathogenicity of Bacillus thuringiensis. Insect Biochem Mol Biol, 32, 1025–36
   PubMed Web of Science ®Google Scholar
• El-Hag H, Safhi M. (2011). Antimalignancy activity of Bacillus thuringiensis Serovar Dakota (H15) in vivo. World J Med Sci, 6, 6–16
   Google Scholar
• Ernandes S, Bianchi VLD, Moraes IDO. (2012). Evaluation of two different culture media for the development of biopesticides based on Bacillus thuringiensis and their application in larvae of Aedes aegypti Acta Sci Technol, 35, 11–18
   Web of Science ®Google Scholar
• Fabrick J, Oppert C, Lorenzen MD, et al. (2009). A novel Tenebrio molitor cadherin is a functional receptor for Bacillus thuringiensis Cry3Aa toxin. J Biol Chem, 284, 18401–10
   PubMed Web of Science ®Google Scholar
• Farinós GP, De La Poza M, Hernández-Crespo P, et al. (2004). Resistance monitoring of field populations of the corn borers Sesamia nonagrioides and Ostrinia nubilalis after 5 years of Bt maize cultivation in Spain. Entomol Exp Appl, 110, 23–30
   Web of Science ®Google Scholar
• Gahan LJ, Pauchet Y, Vogel H, Heckel DG. (2010). An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet, 6, e1001248
   PubMed Web of Science ®Google Scholar
• Georghiou GP, Wirth MC. (1997). Influence of exposure to single versus multiple toxins of Bacillus thuringiensis subsp. israelensis on development of resistance in the mosquito Culex quinquefasciatus (Diptera: Culicidae). Appl Environ Microbiol, 63, 1095–101
   PubMed Web of Science ®Google Scholar
• Goldman IF, Arnold J, Carlton BC. (1986). Selection for resistance to Bacillus thuringiensis subsp. israelensis in field and in laboratory population of the mosquitos Aedes aegypti. J Invertebr Pathol, 47, 317--24
   Google Scholar
• Gómez I, Sánchez J, Miranda R, et al. (2002). Cadherin-like receptor binding facilitates proteolytic cleavage of helix a-1 in domain I and oligomer pre-pore formation of Bacillus thuringiensis Cry1Ab toxin. FEBS Lett, 513, 242–6
   PubMed Web of Science ®Google Scholar
• Hernández-Rodríguez CS, Hernández-Martínez P, Van Rie J, et al. (2012). Specific binding of radiolabeled Cry1Fa insecticidal protein from Bacillus thuringiensis to midgut sites in lepidopteran species. Appl Environ Microbiol, 78, 4048–50
   PubMed Web of Science ®Google Scholar
• Hua G, Jurat-Fuentes JL, Adang MJ. (2004). Fluorescent-based assays establish Manduca sexta Bt-R1a cadherin as a receptor for multiple Bacillus thuringiensis Cry1A toxins in Drosophila S2 cells. Insect Biochem Mol Biol, 34, 193–202
   PubMed Web of Science ®Google Scholar
• Ishiwata S. (1902). Su le bacilli appellé, “sitto”. Bull Assoc Sericulture Jpn, 114, 1–5
   Google Scholar
• Jiménez-Juárez N, Muñoz-Garay C, Gómez I, et al. (2008). The pre-pore from Bacillus thuringiensis Cry1Ab toxin is necessary to induce insect death in Manduca sexta. Peptides, 29, 318–23
   PubMed Web of Science ®Google Scholar
• Jurat-Fuentes JL, Adang MJ. (2006). The Heliothis virescens cadherin protein expressed in Drosophila S2 cells functions as a receptor for Bacillus thuringiensis Cry1A but not Cry1Fa toxins. Biochemistry, 45, 9688–95
   PubMed Web of Science ®Google Scholar
• Katayama H, Yokota H, Akao T, et al. (2005). Parasporin-1, a novel cytotoxic protein to human cells from non-insecticidal parasporal inclusions of Bacillus thuringiensis. J Biochem Tokyo, 137, 17–25
   PubMed Web of Science ®Google Scholar
• Kitada S, Abe Y, Shimada H, et al. (2006). Cytocidal actions of parasporin-2, an anti-tumor crystal toxin from Bacillus thuringiensis. J Biol Chem, 281, 26350–60
   PubMed Web of Science ®Google Scholar
• Kranthi KR, Dhawad CS, Naidu SR, et al. (2006). Inheritance of resistance in Indian Helicoverpa armigera (Hübner) to Cry1Ac toxin of Bacillus thuringiensis. Crop Prot, 25, 119–24
   Web of Science ®Google Scholar
• Kroeger I, Duquesne S, Liess M. (2013). Crustacean biodiversity as an important factor for mosquito larval control. J Vector Ecol, 38, 390–400
   PubMed Web of Science ®Google Scholar
• Kruger M, Rensburg JV, Berg JVD. (2011). Resistance to Bt maize in Busseola fusca (Lepidoptera: Noctuidae) from Vaalharts, South Africa. Environ Entomol, 40, 477–83
   Web of Science ®Google Scholar
• Lebel G, Vachon V, Préfontaine G, et al. (2009). Mutations in domain I interhelical loops affect the rate of pore formation by the Bacillus thuringiensis Cry1Aa toxin in insect midgut brush border membrane vesicles. Appl Environ Microbiol, 75, 3842–50
   PubMed Web of Science ®Google Scholar
• Lenormand T, Raymond M. (1998). Resistance management: the stable zone strategy. Proc Biol Sci, 265, 1985–90
   Web of Science ®Google Scholar
• Liu M, Cai QX, Liu HZ, et al. (2002). Chitinolytic activities in Bacillus thuringiensis and their synergistic effects on larvicidal activity. J Appl Microbiol, 93, 374–9
   PubMed Web of Science ®Google Scholar
• Mahon RJ, Olsen KM, Garsia KA, Young SR. (2007). Resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. J Econ Entomol, 100, 894–902
   PubMed Web of Science ®Google Scholar
• Margalit J, Dean D. (1985). The story of Bacillus thuringiensis var. israelensis (Bti). J Am Mosq Control Assoc, 1, 1–7
   PubMed Web of Science ®Google Scholar
• Melo ALA, Sanchuki CE, Woiciechowsk AL, et al. (2012). Utilização da cama de frango em meio de cultivo de Bacillus thuringiensis var. israelensis Berliner para o controle de Aedes aegypti Linnaeus. J Biotechnol Biodivers, 2, 1–6
   Google Scholar
• Milner RJ. (1994). History of Bacillus thuringiensis. Agric Ecosyst Environ, 49, 9–13
   Web of Science ®Google Scholar
• Mizuki E, Ohba M, Akao T, et al. (1999). Unique activity associated with non-insecticidal Bacillus thuringiensis parasporal inclusions: in vitro cell-killing action on human cancer cells. J Appl Microbiol, 86, 477–86
   PubMed Web of Science ®Google Scholar
• Morin S, Biggs RW, Sisterson MS, et al. (2003). Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc Natl Acad Sci USA, 100, 5004–9
   PubMed Web of Science ®Google Scholar
• Nagamatsu Y, Okamura S, Saitou H, et al. (2010). Three Cry toxins in two types from Bacillus thuringiensis strain M019 preferentially kill human hepatocyte cancer and uterus cervix cancer cells. Biosci Biotech Bioch, 74, 494–8
   PubMed Web of Science ®Google Scholar
• Ohba M, Mizuki E, Uemori A. (2009). Parasporin, a new anticancer protein group from Bacillus thuringiensis. Anticancer Res, 29, 427–33
   PubMed Web of Science ®Google Scholar
• Ohba M, Yu M, Aizawa K. (1988). Occurrence of noninsecticidal Bacillus thuringiensis flagellar serotype 14 in the soil of Japan. Syst Appl Microbiol, 11, 85–9
   Web of Science ®Google Scholar
• Okumura S, Ishikawa T, Saitoh H, et al. (2013). Identification of a second cytotoxic protein produced by Bacillus thuringiensis A1470. Biotechnol Lett, 35, 1889–94
   PubMed Web of Science ®Google Scholar
• Okumura S, Saitoh H, Ishikawa T, et al. (2011). Mode of action of parasporin-4, a cytocidal protein from Bacillus thuringiensis. BBA Rev Biomembr, 1808, 1476–82
   PubMed Web of Science ®Google Scholar
• Pardo-López L, Muñoz-Garay C, Porta H, et al. (2009). Strategies to improve the insecticidal activity of Cry toxins from Bacillus thuringiensis. Peptides, 30, 589–95
   PubMed Web of Science ®Google Scholar
• Paris M, Melodelima C, Coissac E, et al. (2012). Transcription profiling of resistance to Bti toxins in the mosquito Aedes aegypti using next-generation sequencing. J Invertebr Pathol, 109, 201–8
   PubMed Web of Science ®Google Scholar
• Patil CD, Borase HP, Salunke BK, Patil SV. (2013a). Alteration in Bacillus thuringiensis toxicity by curing gut flora: novel approach for mosquito resistance management. Parasitol Res, 112, 3283–8
   PubMed Web of Science ®Google Scholar
• Patil SR, Amena S, Vikas A, et al. (2013b). Utilization of silkworm litter and pupal waste-an eco-friendly approach for mass production of Bacillus thuringiensis. Bioresource Technol, 131, 545–7
   PubMed Web of Science ®Google Scholar
• Pérez C, Muñoz-Garay C, Portugal LC, 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, 2931–7
   PubMed Web of Science ®Google Scholar
• Perez CJ, Shelton AM. (1997). Resistance of Plutella xylostella (Lepidoptera: Plutellidae) to Bacillus thuringiensis Berliner in Central America. J Econ Entomol, 90, 87–93
   Web of Science ®Google Scholar
• Poornima K, Selvanayagam P, Shenbagarathai R. (2010). Identification of native Bacillus thuringiensis strain from South India having specific cytocidal activity against cancer cells. J Appl Microbiol, 109, 348–54
   PubMed Web of Science ®Google Scholar
• Ramırez-Suero M, Valerio-Alfaro G, Bernal JS, Ramírez-Lepe M. (2011). Synergistic effect of chitinases and Bacillus thuringiensis israelensis spore-toxin complex against Aedes aegypti larvae. Can Entomol, 143, 157–64
   Web of Science ®Google Scholar
• Rausell C, García-Robles I, Sánchez J, et al. (2004). Role of toxin activation on binding and pore formation activity of the Bacillus thuringiensis Cry3 toxins in membranes of Leptinotarsa decemlineata (Say). Biochim Biophys Acta, 1660, 99–105
   PubMed Web of Science ®Google Scholar
• Reyes-Ramírez A, Escudero-Abarca BI, Aguilar-Uscanga G, et al. (2004). Antifungal activity of Bacillus thuringiensis chitinase and its potential for the biocontrol of phytopathogenic fungi in soybean seeds. J Food Sci, 69, 131–4
   Google Scholar
• Roh JY, Choi JY, Li MS, et al. (2007). Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J Microbiol Biotechnol, 17, 547–59
   PubMed Web of Science ®Google Scholar
• Sampson MN, Gooday GW. (1998). Involvement of chitinases of Bacillus thuringiensis during pathogenesis in insects. Microbiology, 144, 2189–94
   PubMed Web of Science ®Google Scholar
• Sanchis V. (2012) Genetic improvement of Bt strains and development of novel biopesticides. Bacillus thuringiensis biotechnology. Netherlands: Springer
   Google Scholar
• Schwartz JL, Laprade R. (2000). Membrane permeabilisation by Bacillus thuringiensis toxins: protein insertion and pore formation. In: Charles JF, Delécluse A, Nielsen-LeRoux C, eds. Entomopathogenic bacteria: from laboratory to field application. Norwell, MA: Kluwer Associate Publishing
   Google Scholar
• Schwartz JL, Lu YJ, Söhnlein P, et al. (1997). Ion channels formed in planar lipid bilayers by Bacillus thuringiensis toxins in the presence of Manduca sexta midgut receptors. FEBS Lett, 412, 270–6
   PubMed Web of Science ®Google Scholar
• Soberón M, Pardo L, Muñóz-Garay C, et al. (2010). Pore formation by Cry toxins. In: Anderluh G, Lakey JH, eds. Proteins: membrane binding and pore formation. New York: Springer
   Google Scholar
• Stalinski R, Tetreau G, Gaude T, Després L. (2014). Pre-selecting resistance against individual Bti Cry toxins facilitates the development of resistance to the Bti toxins cocktail. J Invertebr Pathol, 119, 50--53
   Google Scholar
• Tabashnik BE. (1994). Evolution of resistance to Bacillus thuringiensis. Ann Rev Entomol, 39, 47–79
   Web of Science ®Google Scholar
• Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y. (2008). Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol, 26, 199–202
   PubMed Web of Science ®Google Scholar
• Tabashnik BE, Unnithan GC, Masson L, et al. (2009). Asymmetrical cross-resistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm. Proc Natl Acad Sci USA Biol, 106, 11889–94
   PubMed Web of Science ®Google Scholar
• Tan F, Zheng A, Zhu J, et al. (2010). Rapid cloning, identification, and application of one novel crystal protein gene cry30Fa1 from Bacillus thuringiensis. FEMS Microbiol Lett, 302, 46–51
   PubMed Web of Science ®Google Scholar
• Tan SY, Cayabyab BF, Alcantara EP, et al. (2013). Comparative binding of Cry1Ab and Cry1F Bacillus thuringiensis toxins to brush border membrane proteins from Ostrinia nubilalis, Ostrinia furnacalis and Diatraea saccharalis (Lepidoptera: Crambidae) midgut tissue. J Invertebr Pathol, 114, 234–40
   PubMed Web of Science ®Google Scholar
• Tetreau G, Bayyareddy K, Jones CM, et al. (2012). Larval midgut modifications associated with Bti resistance in the yellow fever mosquito using proteomic and transcriptomic approaches. BMC Genomics, 13, 248
   PubMed Web of Science ®Google Scholar
• Tetreau G, Stalinski R, David JP, Despres L. (2013). Monitoring resistance to Bacillus thuringiensis subsp. israelensis in the field by performing bioassays with each Cry toxin separately. Mem I Oswaldo Cruz, 108, 894–900
   PubMed Web of Science ®Google Scholar
• Tiewsiri K, Wang P. (2011). Differential alteration of two aminopeptidases N associated with resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper. P Natl Acad Sci-Biol, 108, 14037–42
   PubMed Web of Science ®Google Scholar
• Vachon V, Laprade R, Schwartz JL. (2012). Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J Invertebr Pathol, 111, 1–12
   PubMed Web of Science ®Google Scholar
• Vu KD, Yan S, Tyagi RD, et al. (2009). Induced production of chitinase to enhance entomotoxicity of Bacillus thuringiensis employing starch industry wastewater as a substrate. Bioresource Technol, 100, 5260–9
   PubMed Web of Science ®Google Scholar
• Wang SL, Lin TY, Yen YH, et al. (2006). Bioconversion of shellfish chitin wastes for the production of Bacillus subtilis W-118 chitinase. Carbohydr Res, 341, 2507–15
   PubMed Web of Science ®Google Scholar
• Wiwat C, Thaithanun S, Pantuwatana S, Bhumiratana A. (2000). Toxicity of chitinase-producing Bacillus thuringiensis ssp. kurstaki HD-1 (G) toward Plutella xylostella. J Invertebr Pathol, 76, 270–7
   PubMed Web of Science ®Google Scholar
• Wirth MC, Walton WE, Federici BA (2012). Inheritance, stability, and dominance of Cry resistance in Culex quinquefasciatus (Diptera: Culicidae) selected with the three Cry toxins of Bacillus thuringiensis subsp. israelensis. J Med Entomol, 49, 886–94
   PubMed Web of Science ®Google Scholar
• Wong SYR. (2009). A study on the cytotoxic effect of Bacillus thuringiensis 18 toxin on a leukaemic cell line (CEM-SS). Thesis submitted to the International Medical University, Malaysia
   Google Scholar
• Yamashita S, Katayama H, Saitoh H, et al. (2005). Typical three-domain Cry proteins of Bacillus thuringiensis strain A1462 exhibit cytocidal activity on limited human cancer cells. J Biochem Tokyo, 138, 663–72
   PubMed Web of Science ®Google Scholar
• Zhang X, Candas M, Griko NB, et al. (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, 1407–16
   PubMed Web of Science ®Google Scholar
• Zhuang MB, Oltean DI, Gómez I, et al. (2002). Heliothis virescens and Manduca sexta lipid rafts are involved in Cry1A toxin binding to the midgut epithelium and subsequent pore formation. J Biol Chem, 277, 13863–72
   PubMed Web of Science ®Google Scholar