Physiological and biochemical response of Aedes aegypti tolerance to Bacillus thuringiensisFootnote

† Songqing Wu, Wei Wu, Xiaoli Zhu and Zhaoxia Liu contributed equally to this work.

References

• Araujo, A. P., Araujo Diniz, D. F., Helvecio, E., de Barros, R. A., de Oliveira, C. M., Ayres, C. F., … Silva-Filha, M. H. (2013). The susceptibility of Aedes aegypti populations displaying temephos resistance to Bacillus thuringiensis israelensis: a basis for management. Parasites and Vectors, 6, 297. doi:10.1186/1756-3305-6-297
   PubMed Web of Science ®Google Scholar
• Becker, N., & Ludwig, M. (1993). Investigations on possible resistance in Aedes vexans field populations after a 10-year application of Bacillus thuringiensis israelensis. Journal of the American Mosquito Control Association, 9, 221–224.
   PubMed Web of Science ®Google Scholar
• Benrfield, P. (1955). Amylases, alpha and beta. Methods in Enzymology, 1, 149–158. doi: 10.1016/0076-6879(55)01021-5
   Web of Science ®Google Scholar
• Berry, C., O'Neil, S., Ben-Dov, E., Jones, A. F., Murphy, L., Quail, M. A., … Parkhill, J. (2002). Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp israelensis. Applied And Environmental Microbiology, 68, 5082–5095. doi:10.1128/aem.68.10.5082-5092.2002
   PubMed Web of Science ®Google Scholar
• Bouvier, J. C., Boivin, T., Beslay, D., & Sauphanor, B. (2002). Age-dependent response to insecticides and enzymatic variation in susceptible and resistant codling moth larvae. Archives of Insect Biochemistry and Physiology, 51, 55–66. doi:10.1002/arch.10052
   PubMed Web of Science ®Google Scholar
• Boyer, S., David, J. P., Rey, D., Lemperiere, G., & Ravanel, P. (2006). Response of Aedes aegypti (Diptera: Culicidae) larvae to three xenobiotic exposures: Larval tolerance and detoxifying enzyme activities. Environmental Toxicology and Chemistry, 25, 470–476. doi:10.1897/05-267R2.1
   PubMed Web of Science ®Google Scholar
• Boyer, S., Tilquin, M., & Ravanel, P. (2007). Differential sensitivity to Bacillus thuringiensis var. Israelensis and temephos in field mosquito populations of Ochlerotatus cataphylla (diptera: Culicidae): Toward resistance? Environmental Toxicology and Chemistry, 26, 157–162. doi:10.1897/06-205R.1
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254. doi:10.1016/0003-2697(76)90527-3
   PubMed Web of Science ®Google Scholar
• Bravo, A., Gill, S. S., & Soberon, M. (2007). Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon, 49, 423–435. doi:10.1016/j.toxicon.2006.11.022
   PubMed Web of Science ®Google Scholar
• Brogdon, W. G., & McAllister, J. C. (1998). Insecticide resistance and vector control. Emerging Infectious Diseases, 4, 605–613. doi: 10.3201/eid0404.980410
   PubMed Web of Science ®Google Scholar
• Cancino-Rodezno, A., Lozano, L., Oppert, C., Castro, J. I., Lanz-Mendoza, H., Encarnación, S., … Jurat-Fuentes, J. L. (2012). Comparative proteomic analysis of Aedes aegypti larval midgut after intoxication with Cry11Aa toxin from Bacillus thuringiensis. PloS One, 7, e37034. doi:10.1371/journal.pone.0037034
   Google Scholar
• David, J. P., Huber, K., Failloux, A. B., Rey, D., & Meyran, J. C. (2003). The role of environment in shaping the genetic diversity of the subalpine mosquito, Aedes rusticus (Diptera, Culicidae). Molecular Ecology, 12, 1951–1961. doi:10.1046/j.1365-294X.2003.01870.x
   PubMed Web of Science ®Google Scholar
• Desousa, G., Cuany, A., Brun, A., Amichot, M., Rahmani, R., & Bergé, J. B. (1995). A microfluorometric method for measuring ethoxycoumarin-O-deethylase activity on individual Drosophila melanogaster abdomens: interest for screening resistance in insect populations. Analytical Biochemistry, 229, 86–91. doi:10.1006/abio.1995.1382
   PubMed Web of Science ®Google Scholar
• Dimopoulos, M., Bagnara, A. S., & Edwards, M. R. (2000). Characterisation and sequence analysis of a carbamate kinase gene from the diplomonad Hexamita inflata. Journal of Eukaryotic Microbiology, 47, 499–503. doi:10.1111/j.1550-7408.2000.tb00081.x
   PubMed Web of Science ®Google Scholar
• Feyereisen, R. (1999). Insect P450 Enzymes. Annual Review of Entomology, 44(1), 507–533. doi:10.1146/annurev.ento.44.1.507
   PubMed Web of Science ®Google Scholar
• Fournier, D., Bride, J. M., Hoffmann, F., & Karch, F. (1992). Acetylcholinesterase. Two types of modifications confer resistance to insecticide. Journal of Biological Chemistry, 267, 14270–14274.
   PubMed Web of Science ®Google Scholar
• Franco, O. L., Rigden, D. J., Melo, F. R., & Grossi-de-Sá, M. F. (2002). Plant α-amylase inhibitors and their interaction with insect α-amylases. European Journal of Biochemistry, 269, 397–412. doi:10.1046/j.0014-2956.2001.02656.x
   PubMedGoogle Scholar
• Haubruge, E., Amichot, M., Cuany, A., Berge, J. B., & Araud, L. (2002). Purification and characterization of a carboxylesterase involved in malathion-specific resistance from Tribolium castaneum (Coleoptera: Tenebrionidae). Insect Biochemistry and Molecular Biology, 32, 1181–1190. doi:10.1016/S0965-1748(02)00054-1
   PubMed Web of Science ®Google Scholar
• Hemingway, J. (2000). The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochemistry and Molecular Biology, 30, 1009–1015. doi:10.1016/S0965-1748(00)00079-5
   PubMed Web of Science ®Google Scholar
• Hemingway, J., Hawkes, N. J., McCarroll, L., & Ranson, H. (2004). The molecular basis of insecticide resistance in mosquitoes. Insect Biochemistry and Molecular Biology, 34, 653–665. doi:10.1016/j.ibmb.2004.03.018
   PubMed Web of Science ®Google Scholar
• Herrero, S., Combes, E., Van Oers, M. M., Vlak, J. M., de Maagd, R. A., & Beekwilder, J. (2005). Identification and recombinant expression of a novel chymotrypsin from Spodoptera exigua. Insect Biochemistry and Molecular Biology, 35, 1073–1082. doi:10.1016/j.ibmb.2005.05.006
   PubMed Web of Science ®Google Scholar
• Huffman, D. L., Abrami, L., Sasik, R., Corbeil, J., van der Goot, F. G., & Aroian, R. V. (2004). Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proceedings of the National Academy of Sciences of the United States of America, 101, 10995–11000. doi:10.1073/pnas.0404073101
   PubMed Web of Science ®Google Scholar
• Jurat-Fuentes, J. L., Gahan, L. J., Gould, F. L., Heckel, D. G., & Adang, M. J. (2004). The HevCaLP protein mediates binding specificity of the Cry1A class of Bacillus thuringiensis toxins in Heliothis virescens. Biochemistry, 43, 14299–14305. doi:10.1021/bi048500i
   PubMed Web of Science ®Google Scholar
• Karunaratne, S. H. P. P., & Hemingway, J. (1996). Different insecticides select multiple carboxylesterase isoenzymes and different resistance levels from a single population of Culex quinquefasciatus. Pesticide Biochemistry and Physiology, 54, 4–11. doi:10.1006/pest.1996.0003
   Web of Science ®Google Scholar
• Koodalingam, A., Mullainadhan, P., Rajalakshmi, A., Deepalakshmi, R., & Ammu, M. (2012). Effect of a Bt-based product (Vectobar) on esterases and phosphatases from larvae of the mosquito Aedes aegypti. Pesticide Biochemistry and Physiology, 104, 267–272. doi:10.1016/j.pestbp.2012.09.008
   Web of Science ®Google Scholar
• Lee, S. B., Aimanova, K. G., & Gill, S. S. (2014). Alkaline phosphatases and aminopeptidases are altered in a Cry11Aa resistant strain of Aedes aegypti. Insect Biochemistry and Molecular Biology, 54, 112–121. doi:10.1016/j.ibmb.2014.09.004
   PubMed Web of Science ®Google Scholar
• Likitvivatanavong, S., Chen, J. W., Bravo, A., Soberon, M., & Gill, S. S. (2011). Cadherin, alkaline phosphatase, and aminopeptidase N as receptors of Cry11Ba toxin from Bacillus thuringiensis subsp. jegathesan in Aedes aegypti. Applied and Environmental Microbiology, 77, 24–31. doi:10.1128/Aem.01852-10
   PubMed Web of Science ®Google Scholar
• Lumjuan, N., Rajatileka, S., Changsom, D., Wicheer, J., Leelapat, P., Prapanthadara, L. A., … Ranson, H. (2011). The role of the Aedes aegypti Epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides. Insect Biochemistry and Molecular Biology, 41, 203–209. doi:10.1016/j.ibmb.2010.12.005
   PubMed Web of Science ®Google Scholar
• Mannervik, B., Danielson, U. H., & Ketterer, B. (1988). Glutathione transferases-structure and catalytic activit. Critical Reviews in Biochemistry and Molecular Biology, 23, 283–337. doi: 10.3109/10409238809088226
   Web of Science ®Google Scholar
• Marcombe, S., Poupardin, R., Darriet, F., Reynaud, S., Bonnet, J., Strode, C., … David, J. P. (2009). Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: A case study in Martinique Island (French West Indies). BMC Genomics, 10, 494. doi:10.1186/1471-2164-10-494
   PubMed Web of Science ®Google Scholar
• Nauen, R. (2007). Insecticide resistance in disease vectors of public health importance. Pest Management Science, 63, 628–633. doi:10.1002/ps.1406
   PubMed Web of Science ®Google Scholar
• Nirmala, X., & James, A. A. (2003). Engineering plasmodium-refractory phenotypes in mosquitoes. Trends in Parasitology, 19, 384–387. doi:10.1016/S1471-4922(03)00188-0
   PubMed Web of Science ®Google Scholar
• Oppert, B. (1999). Protease interactions with Bacillus thuringiensis insecticidal toxins. Archives of Insect Biochemistry and Physiology, 42, 1–12. doi:10.1002/(SICI)1520-6327(199909)42:1<1::AID-ARCH2>3.0.CO;2-#
   PubMed Web of Science ®Google Scholar
• Ortego, F., Novillo, C., & Castañera, P. (1996). Characterization and distribution of digestive proteases of the stalk corn borer, Sesamia nonagrioides Lef. (Lepidoptera: Noctuidae). Archives of Insect Biochemistry and Physiology, 33, 163–180. doi:10.1002/(SICI)1520-6327(1996)33:2<163::AID-ARCH6>3.0.CO;2-Z
   Web of Science ®Google Scholar
• Pardo-Lopez, L., Soberon, M., & Bravo, A. (2013). Bacillus thuringiensis insecticidal three-domain Cry toxins: Mode of action, insect resistance and consequences for crop protection. FEMS Microbiology Review, 37, 3–22. doi:10.1111/j.1574-6976.2012.00341.x
   PubMed Web of Science ®Google Scholar
• Paul, A., Harrington, L. C., Zhang, L., & Scott, J. G. (2005). Insecticide resistance in Culex pipiens from New York. Journal of the American Mosquito Control Association, 21, 305–309. doi:10.2987/8756-971x(2005)21[305:Iricpf]2.0.Co;2
   PubMed Web of Science ®Google Scholar
• Pickett, C. B., & Lu, A. Y. H. (1989). Glutathione S-transferases: Gene structure, regulation, and biological function. Annual Review of Biochemistry, 58, 743–764. doi:10.1146/annurev.bi.58.070189.003523
   PubMed Web of Science ®Google Scholar
• Polson, K. A., Brogdon, W. G., Rawlins, S. C., & Chadee, D. D. (2011). Characterization of insecticide resistance in Trinidadian strains of Aedes aegypti mosquitoes. Acta Tropica, 117, 31–38. doi:10.1016/j.actatropica.2010.09.005
   PubMed Web of Science ®Google Scholar
• Poupardin, R., Reynaud, S., Strode, C., Ranson, H., Vontas, J., & David, J. P. (2008). Cross-induction of detoxification genes by environmental xenobiotics and insecticides in the mosquito Aedes aegypti: Impact on larval tolerance to chemical insecticides. Insect Biochemistry and Molecular Biology, 38, 540–551. doi:10.1016/j.ibmb.2008.01.004
   PubMed Web of Science ®Google Scholar
• Rahman, M. M., Roberts, H. L., Sarjan, M., Asgari, S., & Schmidt, O. (2004). Induction and transmission of Bacillus thuringiensis tolerance in the flour moth Ephestia kuehniella. Proceedings of the National Academy of Sciences of the United States of America, 101, 2696–2699. doi:10.1073/pnas.0306669101
   PubMed Web of Science ®Google Scholar
• Riaz, M. A., Poupardin, R., Reynaud, S., Strode, C., Ranson, H., & David, J. P. (2009). Impact of glyphosate and benzo[a]pyrene on the tolerance of mosquito larvae to chemical insecticides. Role of detoxification genes in response to xenobiotics. Aquatic Toxicology, 93, 61–69. doi:10.1016/j.aquatox.2009.03.005
   PubMed Web of Science ®Google Scholar
• Sébastien, B., Margot, P., Sylvaine, J., Guy, L., & Patrick, R. (2012). Influence of insecticide Bacillus thuringiensis subsp. israelensis treatments on resistance and enzyme activities in Aedes rusticus larvae (Diptera: Culicidae). Biological Control, 62, 75–81. doi:10.1016/j.biocontrol.2012.02.001
   Web of Science ®Google Scholar
• Su, T., & Mulla, M. S. (2004). Documentation of high-level bacillus Sphaericus 2362 resistance in field populations of Culex quinquefasciatus breeding in polluted water in Thailand. Journal of the American Mosquito Control Association, 20, 405–411.
   PubMed Web of Science ®Google Scholar
• Tietze, F. (1969). Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Applications to mammalian blood and other tissues. Analytical Biochemistry, 27, 502–522. doi:10.1016/0003-2697(69)90064-5
   PubMed Web of Science ®Google Scholar
• Valencia, A., Bustillo, A. E., Ossa, G. E., & Chrispeels, M. J. (2000). α-Amylases of the coffee berry borer (Hypothenemus hampei) and their inhibition by two plant amylase inhibitors. Insect Biochemistry and Molecular Biology, 30, 207–213. doi:10.1016/S0965-1748(99)00115-0
   PubMed Web of Science ®Google Scholar
• Van Munster, M., Préfontaine, G., Meunier, L., Elias, M., Mazza, A., Brousseau, R., & Masson, L. (2007). Altered gene expression in Choristoneura fumiferana and Manduca sexta in response to sublethal intoxication by Bacillus thuringiensis Cry1Ab toxin. Insect Molecular Biology, 16, 25–35. doi:10.1111/j.1365-2583.2006.00692.x
   PubMed Web of Science ®Google Scholar
• Vontas, J. G., Small, G. J., & Hemingway, J. (2001). Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochemical Journal, 357, 65–72. doi: 10.1042/bj3570065
   PubMed Web of Science ®Google Scholar
• Walker, A. J., Ford, L., Majerus, M. E. N., Geoghegan, I. E., Birch, N., Gatehouse, J. A., & Gatehouse, A. M. R. (1998). Characterisation of the mid-gut digestive proteinase activity of the two-spot ladybird (Adalia bipunctata L.) and its sensitivity to proteinase inhibitors. Insect Biochemistry and Molecular Biology, 28, 173–180. doi:10.1016/S0965-1748(97)00114-8
   Web of Science ®Google Scholar
• Wheelock, C. E., Shan, G., & Ottea, J. (2005). Overview of carboxylesterases and their role in the metabolism of insecticides. Journal of Pesticide Science, 30, 75–83. doi:10.1584/jpestics.30.75
   Web of Science ®Google Scholar
• WHO. (2005). Guidelines for laboratory and field testing of mosquito larvicides. WHO/CDS/WHOPES/GCDPP/1.3. Geneva: Author.
   Google Scholar
• WHO. (2008). Dengue haemorrhagic fever (Vol. 2, pp. 25–28). Factsheet No 117, revised May 2008. Geneva: Author.
   Google Scholar
• Zhang, H., Yang, C., Huang, J., & Lü, L. (2004). Susceptibility of field populations of Anopheles sinensis (Diptera: Culicidae) to Bacillus thuringiensis subsp. israelensis. Biocontrol Science and Technology, 14, 321–325. doi:10.1080/09583150310001639187
   Web of Science ®Google Scholar
• Zhang, L., Huang, E., Lin, J., Gelbic, I., Zhang, Q., Guan, Y., … Guan, X. (2010). A novel mosquitocidal Bacillus thuringiensis strain LLP29 isolated from the phylloplane of Magnolia denudata. Microbiological Research, 165, 133–141. doi:10.1016/j.micres.2009.03.002
   PubMed Web of Science ®Google Scholar
• Zhang, L., Wu, S., Peng, Y., Li, M., Sun, L., Huang, E., … Gelbic, I. (2011). The potential of the novel mosquitocidal Bacillus thuringiensis strain LLP29 for use in practice. Journal of Vector Ecology, 36, 458–460. doi:10.1111/j.1948-7134.2011.00189.x
   PubMed Web of Science ®Google Scholar