6,256
Views
74
CrossRef citations to date
0
Altmetric
Review Article

Ion channels as insecticide targets

, , &
Pages 163-177 | Received 19 May 2016, Accepted 22 Aug 2016, Published online: 02 Nov 2016

References

  • Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D., Amanatides, P.G., …. Craig Venter, J. (2000). The genome sequence of Drosophila melanogaster. Science, 287, 2185–2195. doi:10.1126/science.287.5461.2185.
  • Bao, W.X., Narai, Y., Nakano, A., Kaneda, T., Murai, T., & Sonoda, S. (2014). Spinosad resistance of melon thrips, Thrips palmi, is conferred by G275E mutation in α6 subunit of nicotinic acetylcholine receptor and cytochrome P450 detoxification. Pesticide Biochemistry and Physiology, 112, 51–55. doi:10.1016/j.pestbp.2014.04.013.
  • Barnard, E.A., Bilbe, G., Houamed, K., Moss, S.J., Van Renterghem, C., & Smart, T.G. (1987). Functional expression in the Xenopus oocyte of messenger ribonucleic acids encoding brain neurotransmitter receptors: Further characterisation of the implanted GABA receptor. Neuropharmacology, 26, 837–844. doi:10.1016/0028-3908(87)90060-8.
  • Bass, C., Denholm, I., Williamson, M.S., & Nauen, R. (2015). The global status of insect resistance to neonicotinoid insecticides. Pesticide Biochemistry and Physiology, 121, 78–87. doi:10.1016/j.pestbp.2015.04.004.
  • Bass, C., Puinean, A.M., Andrews, M., Cutler, P., Daniels, M., Elias, J., …Slater, Ret al. (2011). Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neuroscience, 12, 51. doi:10.1186/1471-2202-12-51.
  • Baxter, S.W., Chen, M., Dawson, A., Zhao, J.Z., Vogel, H., Shelton, A.M., … Jiggins, C.D. (2010). Mis-spliced transcripts of nicotinic acetylcholine receptor alpha6 are associated with field evolved spinosad resistance in Plutella xylostella (L.). PLoS Genetics, 6, e1000802. doi:10.1371/journal.pgen.1000802.
  • Bloomquist, J.R. (1993). Toxicology, mode of action and target site-mediated resistance to insecticides acting on chloride channels. Comparative Biochemistry and Physiology. C, Comparative Pharmacology and Toxicology, 106, 301–314. doi:10.1016/0742-8413(93)90138-B.
  • Bloomquist, J.R. (1996). Ion channels as targets for insecticides. Annual Review of Entomology, 41, 163–190. doi:10.1146/annurev.en.41.010196.001115.
  • Buckingham, S.D., Biggin, P.C., Sattelle, B.M., Brown, L.A., & Sattelle, D.B. (2005). Insect GABA receptors: splicing, editing, and targeting by antiparasitics and insecticides. Molecular Pharmacology, 68, 942–951. doi:10.1124/mol.105.015313.
  • Casida, J.E., & Durkin, K.A. (2013). Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annual Review of Entomology, 58, 99–117. doi:10.1146/annurev-ento-120811-153645.
  • Casida, J.E. & Durkin, K.A. (2015). Novel GABA receptor pesticide targets. Pesticide Biochemistry and Physiology, 121, 22–30. doi:10.1016/j.pestbp.2014.11.006.
  • Cordova, D., Benner, E.A., Sacher, M.D., Rauh, J.J., Sopa, J.S., Lahm, G.P., …Tao, Y. (2006). Anthranilic diamides: A new class of insecticides with a novel mode of action, ryanodine receptor activation. Pesticide Biochemistry and Physiology, 84, 196–214. doi:10.1016/j.pestbp.2005.07.005.
  • Corringer, P.J., Le Novere, N., & Changeux, J.P. (2000). Nicotinic receptors at the amino acid level. Annual Review of Pharmacology and Toxicology, 40, 431–458. doi:10.1146/annurev.pharmtox.40.1.431.
  • Cully, D.F., Paress, P.S., Liu, K.K., Schaeffer, J.M., & Arena, J.P. (1996). Identification of a Drosophila melanogaster glutamate-gated chloride channel sensitive to the antiparasitic agent avermectin. Journal of Biological Chemistry, 271, 20187–20191. doi:10.1074/jbc.271.33.20187.
  • Davies, T.G.E., O'Reilly, A.O., Field, L.M., Wallace, B., & Williamson, M.S. (2008). Knockdown resistance to DDT and pyrethroids: from target-site mutations to molecular modelling. Pest Management Science, 64, 1126–1130. doi:10.1002/ps.1617.
  • Dermauw, W., Ilias, A., Riga, M., Tsagkarakou, A., Grbic, M., Tirry, L., … Vontas, J. (2012). The cys-loop ligand-gated ion channel gene family of Tetranychus urticae: Implications for acaricide toxicology and a novel mutation associated with abamectin resistance. Insect Biochemistry and Molecular Biology, 42, 455–465. doi:10.1016/j.ibmb.2012.03.002.
  • Dong, K. (1997). A single amino acid change in the para sodium channel protein is associated with knockdown-resistance (kdr) to pyrethroid insecticides in German cockroach. Insect Biochemistry and Molecular Biology, 27, 93–100. doi:10.1016/S0965-1748(96)00082-3.
  • Dong, K., Du, Y., Rinkevich, F., Nomura, Y., Xu, P., Wang, L., … Zhorov, B.S. (2014). Molecular biology of insect sodium channels and pyrethroid resistance. Insect Biochemistry and Molecular Biology, 50, 1–17. doi:10.1016/j.ibmb.2014.03.012.
  • Dong, K. & Scott, J.G. (1994). Linkage of kdr-type resistance and the para-homologous sodium channel gene in German cockroaches (Blattella germanica). Insect Biochemistry and Molecular Biology, 24, 647–654. doi:10.1016/0965-1748(94)90051-5.
  • Du, Y., Nomura, Y., Satar, G., Hu, Z., Nauen, R., He, S.Y., … Dong, K. (2013). Molecular evidence for dual pyrethroid-receptor sites on a mosquito sodium channel. Proceedings of the National Academy of Sciences of the United States of America, 110, 11785–11790. doi:10.1073/pnas.1305118110.
  • Du, Y., Nomura, Y., Zhorov, B.S., & Dong, K. (2015). Rotational symmetry of two pyrethroid receptor sites in the mosquito sodium channel. Molecular Pharmacology, 88, 273–280. doi:10.1124/mol.115.098707.
  • Feng, G., Deak, P., Chopra, M., & Hall, L.M. (1995). Cloning and functional analysis of TipE, a novel membrane protein that enhances Drosophila para sodium channel function. Cell, 82, 1001–1011. doi:10.1016/0092-8674(95)90279-1.
  • ffrench-Constant, R.H. (1994). The molecular and population genetics of cyclodiene insecticide resistance. Insect Biochemistry and Molecular Biology, 24, 335–345. doi:10.1016/0965-1748(94)90026-4.
  • ffrench-Constant, R.H. & Rocheleau, T.A. (1993). Drosophila gamma-aminobutyric acid receptor gene Rdl shows extensive alternative splicing. Journal of Neurochemistry, 60, 2323–2326. doi:10.1111/j.1471-4159.1993.tb03523.x.
  • ffrench-Constant, R.H., Rocheleau, T.A., Steichen, J.C., & Chalmers, A.E. (1993). A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature, 363, 449–451. doi:10.1038/363449a0.
  • ffrench-Constant, R.H., Steichen, J.C., & Ode, P.J. (1993). Cyclodiene insecticide resistance in Drosophila-melanogaster (Meigen) is associated with a temperature-sensitive phenotype. Pesticide Biochemistry and Physiology, 46, 73–77. doi:10.1006/pest.1993.1038.
  • Grauso, M., Reenan, R.A., Culetto, E., & Sattelle, D.B. (2002). Novel putative nicotinic acetylcholine receptor subunit genes, Dα5, Dα6 and Dα7, in Drosophila melanogaster identify a new and highly conserved target of adenosine deaminase acting on RNA-mediated A-to-I pre-mRNA editing. Genetics, 160, 1519–1533.
  • Guo, L., Liang, P., Zhou, X., & Gao, X. (2014). Novel mutations and mutation combinations of ryanodine receptor in a chlorantraniliprole resistant population of Plutella xylostella (L.). Scientific Reports, 4, 6924. doi:10.1038/srep06924.
  • Hanrahan, C.J., Palladino, M.J., Ganetzky, B., & Reenan, R.A. (2000). RNA editing of the Drosophila para Na(+) channel transcript. Evolutionary conservation and developmental regulation. Genetics, 155, 1149–1160.
  • Henderson, J.E., Knipple, D.C., & Soderlund, D.M. (1994). PCR-based homology probing reveals a family of GABA receptor-like genes in Drosophila melanogaster. Insect Biochemistry and Molecular Biology, 24, 363–371. doi:10.1016/0965-1748(94)90029-9.
  • Hermans-Borgmeyer, I., Zopf, D., Ryseck, R.P., Hovemann, B., Betz, H., & Gundelfinger, E.D. (1986). Primary structure of a developmentally regulated nicotinic acetylcholine receptor protein from Drosophila. The EMBO Journal, 5, 1503–1508.
  • Hsu, J.C., Feng, H.T., Wu, W.J., Geib, S.M., Mao, C.H., & Vontas, J. (2012). Truncated transcripts of nicotinic acetylcholine subunit gene Bdα6 are associated with spinosad resistance in Bactrocera dorsalis. Insect Biochemistry and Molecular Biology, 42, 806–815. doi:10.1016/j.ibmb.2012.07.010.
  • Isaacs, A.K., Qi, S., Sarpong, R., & Casida, J.E. (2012). Insect ryanodine receptor: Distinct but coupled insecticide binding sites for [N-(C3)H3] chlorantraniliprole, flubendiamide, and [3H] ryanodine. Chemical Research in Toxicology, 25, 1571–1573. doi:10.1021/tx300326m.
  • Jones, A.K., Buckingham, S.D., Papadaki, M., Yokota, M., Sattelle, B.M., Matsuda, K., & Sattelle, D.B. (2009). Splice-variant- and stage-specific RNA editing of the Drosophila GABA receptor modulates agonist potency. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 29, 4287–4292. doi:10.1523/JNEUROSCI.5251-08.2009.
  • Jones, A.K., & Sattelle, D.B. (2007). The cys-loop ligand-gated ion channel gene superfamily of the red flour beetle, Tribolium castaneum. BMC Genomics, 8, 327. doi:10.1186/1471-2164-8-327.
  • Jones, A.K. & Sattelle, D.B. (2010). Diversity of insect nicotinic acetylcholine receptor subunits. Advances in Experimental Medicine and Biology, 683, 25–43. doi:10.1007/978-1-4419-6445-8_3.
  • Kane, N.S., Hirschberg, B., Qian, S., Hunt, D., Thomas, B., Bronchu, R., …. Cully, D.F. (2000). Drug-resistant Drosophila indicate glutamate-gated chloride channels are targets for the antiparasitics nodulisporic acid and ivermectin. Proceedings of the National Academy of Sciences of the United States of America, 97, 13949–13954. doi:10.1073/pnas.240464697.
  • Kato, K., Kiyonaka, S., Sawaguchi, Y., Tohnishi, M., Masaki, T., Yasokawa, N., …. Mori, Y. (2009). Molecular characterization of flubendiamide sensitivity in the lepidopterous ryanodine receptor Ca2+ release channel. Biochemistry, 48, 10342–10352. doi:10.1021/bi900866s.
  • Knipple, D.C., Doyle, K.E., Marsella-Herrick, P.A., & Soderlund, D.M. (1994). Tight genetic linkage between the KDR insecticide resistance trait and a voltage-sensitive sodium channel gene in the house fly. Proceedings of the National Academy of Sciences of the United States of America, 91, 2483–2487. doi:10.1073/pnas.91.7.2483.
  • Knipple, D.C. & Soderlund, D.M. (2010). The ligand-gated chloride channel gene family of Drosophila melanogaster. Pestcide Biochemistry and Physiology, 97, 140–148. doi:10.1016/j.pestbp.2009.09.002.
  • Kwon, D.H., Yoon, K.S., Clark, J.M., & Lee, S.H. (2010). A point mutation in a glutamate-gated chloride channel confers abamectin resistance in the two-spotted spider mite, Tetranychus urticae Koch. Insect Molecular Biology, 19, 583–591. doi:10.1111/j.1365-2583.2010.01017.x.
  • Lanner, J.T., Georgiou, D.K., Joshi, A.D., & Hamilton, S.L. (2010). Ryanodine receptors: Structure, expression, molecular details, and function in calcium release. Cold Spring Harbor Perspectives in Biology, 2, a003996. doi:10.1101/cshperspect.a003996.
  • Lansdell, S.J., Collins, T., Goodchild, J., & Millar, N.S. (2012). The Drosophila nicotinic acetylcholine receptor subunits Dα5 and Dα7 form functional homomeric and heteromeric ion channels. BMC Neuroscience, 13, 73. doi: 10.1186/1471-2202-13-73.
  • Lansdell, S.J. & Millar, N.S. (2000). The influence of nicotinic receptor subunit composition upon agonist, alpha-bungarotoxin and insecticide (imidacloprid) binding affinity. Neuropharmacology, 39, 671–679. doi:10.1016/S0028-3908(99)00170-7.
  • Le Goff, G., Hamon, A., Berge, J.B., & Amichot, M. (2005). Resistance to fipronil in Drosophila simulans: influence of two point mutations in the RDL GABA receptor subunit. Journal of Neurochemistry, 92, 1295–1305. doi:10.1111/j.1471-4159.2004.02922.x.
  • Li, J., Shao, Y., Ding, Z., Bao, H., Liu, Z., Han, Z., & Millar, N.S. (2010). Native subunit composition of two insect nicotinic receptor subtypes with differing affinities for the insecticide imidacloprid. Insect Biochemistry and Molecular Biology, 40, 17–22. doi:10.1016/j.ibmb.2009.12.003.
  • Lin, W.H., Wright, D.E., Muraro, N.I., & Baines, R.A. (2009). Alternative splicing in the voltage-gated sodium channel DmNav regulates activation, inactivation, and persistent current. Journal of Neurophysiology, 102, 1994–2006. doi:10.1152/jn.00613.2009.
  • Liu, F., Shi, X., Liang, Y., Wu, Q., Xu, B., Xie, W., … Liu, N. (2014). A 36-bp deletion in the alpha subunit of glutamate-gated chloride channel contributes to abamectin resistance in Plutella xylostella. Entomologia Experimentalis et Applicata, 153, 85–92. doi:10.1111/eea.12232.
  • Liu, Z.W., Williamson, M.S., Lansdell, S.J., Denholm, I., Han, Z.J., & Millar, N.S. (2005). A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proceedings of the National Academy of Sciences of the United States of America, 102, 8420–8425. doi:10.1073/pnas.0502901102.
  • Loughney, K., Kreber, R., & Ganetzky, B. (1989). Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell, 58, 1143–1154. doi:10.1016/0092-8674(89)90512-6.
  • Meyers, J.I., Gray, M., Kuklinski, W., Johnson, L.B., Snow, C.D., Black, W.C., … Foy, B.D. (2015). Characterization of the target of ivermectin, the glutamate-gated chloride channel, from Anopheles gambiae. Journal of Experimental Biology, 218, 1478–1486. doi:10.1242/jeb.118570.
  • Millar, N.S. (2003). Assembly and subunit diversity of nicotinic acetylcholine receptors. Biochemical Society Transactions, 31, 869–874. doi:10.1042/bst0310869.
  • Millar, N.S. & Lansdell, S.J. (2010). Characterisation of insect nicotinic acetylcholine receptors by heterologous expression. Advances in Experimental Medicine and Biology, 683, 65–73.
  • Miyazaki, M., Ohyama, K., Dunlap, D.Y., & Matsumura, F. (1996). Cloning and sequencing of the para-type sodium channel gene from susceptible and kdr-resistant German cockroaches (Blattella germanica) and house fly (Musca domestica). Molecular & General Genetics: MGG, 252, 61–68. doi:10.1007/s004389670007.
  • Nakao, T., Kawase, A., Kinoshita, A., Abe, R., Hama, M., Kawahara, N., & Hirase, K. (2011). The A2'N mutation of the RDL gamma-aminobutyric acid receptor conferring fipronil resistance in Laodelphax striatellus (Hemiptera: Delphacidae). Journal of Economic Entomology, 104, 646–652. doi:10.1603/EC10391.
  • O'Reilly, A.O., Khambay, B.P., Williamson, M.S., Field, L.M., Wallace, B.A., & Davies, T.G.E. (2006). Modelling insecticide-binding sites in the voltage-gated sodium channel. The Biochemical Journal, 396, 255–263. doi:10.1042/BJ20051925.
  • Olson, R.O., Liu, Z., Nomura, Y., Song, W., & Dong, K. (2008). Molecular and functional characterization of voltage-gated sodium channel variants from Drosophila melanogaster. Insect Biochemistry and Molecular Biology, 38, 604–610. doi:10.1016/j.ibmb.2008.01.003.
  • Perry, T., Chan, J.Q., Batterham, P., Watson, G.B., Geng, C., & Sparks, T.C. (2012). Effects of mutations in Drosophila nicotinic acetylcholine receptor subunits on sensitivity to insecticides targeting nicotinic acetylcholine receptors. Pesticide Biochemistry and Physiology, 102, 56–60. doi:10.1016/j.pestbp.2011.10.010.
  • Perry, T., Heckel, D.G., McKenzie, J.A., & Batterham, P. (2008). Mutations in Dα1 or Dβ2 nicotinic acetylcholine receptor subunits can confer resistance to neonicotinoids in Drosophila melanogaster Insect Biochemistry and Molecular Biology, 38, 520–528. doi:10.1016/j.ibmb.2007.12.007.
  • Perry, T., McKenzie, J.A., & Batterham, P. (2007). A knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad. Insect Biochemistry and Molecular Biology, 37, 184–188. doi:10.1016/j.ibmb.2006.11.009.
  • Perry, T., Somers, J., Yang, Y.T., & Batterham, P. (2015). Expression of insect α6-like nicotinic acetylcholine receptors in Drosophila melanogaster highlights a high level of conservation of the receptor:spinosyn interaction. Insect Biochemistry and Molecular Biology, 64, 106–115. doi:10.1016/j.ibmb.2015.01.017.
  • Pittendrigh, B., Reenan, R., ffrench-Constant, R.H., & Ganetzky, B. (1997). Point mutations in the Drosophila sodium channel gene para associated with resistance to DDT and pyrethroid insecticides. Molecular & General Genetics: MGG, 256, 602–610. doi:10.1007/s004380050608.
  • Puinean, A.M., Lansdell, S.J., Collins, T., Bielza, P., & Millar, N.S. (2013). A nicotinic acetylcholine receptor transmembrane point mutation (G275E) associated with resistance to spinosad in Frankliniella occidentalis. Journal of Neurochemistry, 124, 590–601. doi:10.1111/jnc.12029.
  • Qi, S., Luemmen, P., Nauen, R., & Casida, J.E. (2014). Diamide insecticide target site specificity in the Heliothis and Musca ryanodine receptors relative to toxicity. Journal of Agricultural and Food Chemistry, 62, 4077–4082. doi:10.1021/jf501236h.
  • Remnant, E.J., Good, R.T., Schmidt, J.M., Lumb, C., Robin, C., Daborn, P.J., & Batterham, P. (2013). Gene duplication in the major insecticide target site, RDL, in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 110, 14705–14710. doi:10.1073/pnas.1311341110.
  • Remnant, E.J., Morton, C.J., Daborn, P.J., Lumb, C., Yang, Y.T., Ng, H.L., … Batterham, P. (2014). The role of Rdl in resistance to phenylpyrazoles in Drosophila melanogaster. Insect Biochemistry and Molecular Biology, 54, 11–21. doi:10.1016/j.ibmb.2014.08.008.
  • Rinkevich, F.D., Chen, M., Shelton, A.M., & Scott, J.G. (2010). Transcripts of the nicotinic acetylcholine receptor subunit gene Pxylα6 with premature stop codons are associated with spinosad resistance in diamondback moth, Plutella xylostella. Invertebrate Neuroscience, 10, 25–33. doi:10.1007/s10158-010-0102-1.
  • Sattelle, D.B., Cordova, D., & Cheek, T.R. (2008). Insect ryanodine receptors: Molecular targets for novel pest control chemicals. Invertebrate Neuroscience, 8, 107–119. doi:10.1007/s10158-008-0076-4.
  • Shimomura, M., Okuda, H., Matsuda, K., Komai, K., Akamatsu, M., & Sattelle, D.B. (2001). Effects of mutations of a glutamine residue in loop D of the alpha7 nicotinic acetylcholine receptor on agonist profiles for neonicotinoid insecticides and related ligands. British Journal of Pharmacology, 137, 162–169. doi:10.1038/sj.bjp.0704848.
  • Shimomura, M., Yokota, M., Ihara, M., Akamatsu, M., Sattelle, D.B., & Matsuda, K. (2006). Role in the selectivity of neonicotinoids of insect-specific basic residues in loop D of the nicotinic acetylcholine receptor agonist binding site. Molecular Pharmacology, 70, 1255–1263. doi:10.1124/mol.106.026815.
  • Shotkoski, F., Lee, H.J., Zhang, H.G., Jackson, M.B., & ffrench-Constant, R.H. (1994). Functional expression of insecticide-resistant GABA receptors from the mosquito Aedes aegypti. Insect Molecular Biology, 3, 283–287. doi:10.1111/j.1365-2583.1994.tb00179.x.
  • Siddiqi, O., & Benzer, S. (1976). Neurophysiological defects in temperature-sensitive paralytic mutants of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 73, 3253–3257. doi:10.1073/pnas.73.9.3253.
  • Silva, W.M., Berger, M., Bass, C., Williamson, M., Moura, D.M., Ribeiro, L.M., & Siqueira, H.A. (2016). Mutation (G275E) of the nicotinic acetylcholine receptor α6 suresistance to spinosyns in Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Pesticide Biochemistry and Physiology, 131, 1–8. doi:10.1016/j.pestbp.2016.02.006.
  • Slater, R., Paul, V.L., Andrews, M., Garbay, M., & Camblin, P. (2012). Identifying the presence of neonicotinoid resistant peach-potato aphid (Myzus persicae) in the peach-growing regions of southern France and northern Spain. Pest Management Science, 68, 634–638. doi:10.1002/ps.2307.
  • Somers, J., Nguyen, J., Lumb, C., Batterham, P., & Perry, T. (2015). In vivo functional analysis of the Drosophila melanogaster nicotinic acetylcholine receptor Dα6 using the insecticide spinosad. Insect Biochemistry and Molecular Biology, 64, 116–127. doi:10.1016/j.ibmb.2015.01.018.
  • Sparks, T.C., Crouse, G.D., & Durst, G. (2001). Natural products as insecticides: the biology, biochemistry and quantitative structure-activity relationships of spinosyns and spinosoids. Pest Management Science, 57, 896–905. doi:10.1002/ps.358.
  • Steinbach, D., Gutbrod, O., Luemmen, P., Matthiesen, S., Schorn, C., & Nauen, R. (2015). Geographic spread, genetics and functional characteristics of ryanodine receptor based target-site resistance to diamide insecticides in diamondback moth, Plutella Xylostella. Insect Biochemistry and Molecular Biology, 63, 14–22. doi:10.1016/j.ibmb.2015.05.001.
  • Stilwell, G.E., Rocheleau, T., & ffrench-Constant, R.H. (1995). GABA receptor minigene rescues insecticide resistance phenotypes in Drosophila. Journal of Molecular Biology, 253, 223–227. doi:10.1006/jmbi.1995.0547.
  • Suzuki, D.T. (1970). Temperature-sensitive mutations in Drosophila melanogaster. Science, 170, 695–706. doi:10.1126/science.170.3959.695.
  • Suzuki, D.T., Grigliatti, T., & Williamson, R. (1971). Temperature-sensitive mutations in Drosophila melanogaster. VII. A mutation (para-ts) causing reversible adult paralysis. Proceedings of the National Academy of Sciences of the United States of America, 68, 890–893. doi:10.1073/pnas.68.5.890.
  • Takeshima, H., Nishi, M., Iwabe, N., Miyata, T., Hosoya, T., Masai, I., & Hotta, Y. (1994). Isolation and characterization of a gene for a ryanodine receptor/calcium release channel in Drosophila melanogaster. FEBS Lett, 337, 81–87. doi:10.1016/0014-5793(94)80634-9.
  • Tao, Y., Gutteridge, S., Benner, E.A., Wu, L., Rhoades, D.F., Sacher, M.D., … Cordova, D. (2013). Identification of a critical region in the Drosophila ryanodine receptor that confers sensitivity to diamide insecticides. Insect Biochemistry and Molecular Biology, 43, 820–828. doi:10.1016/j.ibmb.2013.06.006.
  • Taylor-Wells, J., Brooke, B.D., Bermudez, I., & Jones, A.K. (2015). The neonicotinoid imidacloprid, and the pyrethroid deltamethrin, are antagonists of the insect Rdl GABA receptor. Journal of Neurochemistry, 135, 705–713. doi:10.1111/jnc.13290.
  • Thackeray, J.R. & Ganetzky, B. (1994). Developmentally regulated alternative splicing generates a complex array of Drosophila para sodium channel isoforms. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 14, 2569–2578.
  • Thackeray, J.R. & Ganetzky, B. (1995). Conserved alternative splicing patterns and splicing signals in the Drosophila sodium channel gene para. Genetics, 141, 203–214.
  • Tomizawa, M. & Casida, J.E. (2003). Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annual Review of Entomology, 48, 339–364. doi:10.1146/annurev.ento.48.091801.112731.
  • Tomizawa, M. & Casida, J.E. (2005). Neonicotinoid insecticide toxicology: Mechanisms of selective action. Annual Review of Pharmacology and Toxicology, 45, 247–268. doi:10.1146/annurev.pharmtox.45.120403.095930.
  • Troczka, B., Zimmer, C.T., Elias, J., Schorn, C., Bass, C., Davies, T.G.E., …. Nauen, R. (2012). Resistance to diamide insecticides in diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) is associated with a mutation in the membrane-spanning domain of the ryanodine receptor. Insect Biochemistry and Molecular Biology, 42, 873–880. doi:10.1016/j.ibmb.2012.09.001.
  • Troczka, B.J., Williams, A.J., Williamson, M.S., Field, L.M., Luemmen, P., & Davies, T.G.E. (2015). Stable expression and functional characterisation of the diamondback moth ryanodine receptor G4946E variant conferring resistance to diamide insecticides. Scientific Reports, 5, 14680. doi:10.1038/srep14680.
  • Usherwood, P.N., Davies, T.G.E., Mellor, I.R., O'Reilly, A.O., Peng, F., Vais, H., … Williamson, M.S. (2007). Mutations in DIIS5 and the DIIS4-S5 linker of Drosophila melanogaster sodium channel define binding domains for pyrethroids and DDT. FEBS Letters, 581, 5485–5492. doi:10.1016/j.febslet.2007.10.057.
  • Vais, H., Williamson, M.S., Goodson, S.J., Devonshire, A.L., Warmke, J.W., Usherwood, P.N., & Cohen, C.J. (2000). Activation of Drosophila sodium channels promotes modification by deltamethrin. Reductions in affinity caused by knock-down resistance mutations. The Journal of General Physiology, 115, 305–318. doi:10.1085/jgp.115.3.305.
  • Wang, L., Nomura, Y., Du, Y., Liu, N., Zhorov, B.S., & Dong, K. (2015). A mutation in the intracellular loop III/IV of mosquito sodium channel synergizes the effect of mutations in helix IIS6 on pyrethroid resistance. Molecular Pharmacology, 87, 421–429. doi:10.1124/mol.114.094730.
  • Wang, X., Wang, R., Yang, Y., Wu, S., O'Reilly, A.O., & Wu, Y. (2016). A point mutation in the glutamate-gated chloride channel of Plutella xylostella is associated with resistance to abamectin. Insect Molecular Biology, 25, 116–125. doi:10.1111/imb.12204.
  • Wang, X. & Wu, Y. (2012). High levels of resistance to chlorantraniliprole evolved in field populations of Plutella Xylostella. Journal of Economic Entomology, 105, 1019–1023. doi:10.1603/EC12059.
  • Warmke, J.W., Reenan, R.A., Wang, P., Qian, S., Arena, J.P., Wang, J., …. Cohen, C.J. (1997). Functional expression of Drosophila para sodium channels. Modulation by the membrane protein TipE and toxin pharmacology. The Journal of General Physiology, 110, 119–133. doi:10.1085/jgp.110.2.119.
  • Watson, G.B., Chouinard, S.W., Cook, K.R., Geng, C., Gifford, J.M., Gustafson, G.D., … Stillwell, G.E. (2010). A spinosyn-sensitive Drosophila melanogaster nicotinic acetylcholine receptor identified through chemically induced target site resistance, resistance gene identification, and heterologous expression. Insect Biochemistry and Molecular Biology, 40, 376–384. doi:10.1016/j.ibmb.2009.11.004.
  • Williamson, M.S., Denholm, I., Bell, C.A., & Devonshire, A.L. (1993). Knockdown resistance (kdr) to DDT and pyrethroid insecticides maps to a sodium channel gene locus in the housefly (Musca domestica). Molecular & General Genetics: MGG, 240, 17–22. doi:10.1007/BF00276878.
  • Williamson, M.S., Martinez-Torres, D., Hick, C.A., & Devonshire, A.L. (1996). Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Molecular & General Genetics: MGG, 252, 51–60. doi:10.1007/BF02173204.
  • Wolstenholme, A.J. (2012). Glutamate-gated chloride channels. Journal of Biological Chemistry, 287, 40232–40238. doi:10.1074/jbc.R112.406280.
  • Xu, X.H., Bhat, M.B., Nishi, M., Takeshima, H., & Ma, J.J. (2000). Molecular cloning of cDNA encoding a Drosophila ryanodine receptor and functional studies of the carboxyl-terminal calcium release channel. Biophysical Journal, 78, 1270–1281. doi:10.1016/S0006-3495(00)76683-5.
  • Zhang, H.G., ffrench-Constant, R.H., & Jackson, M.B. (1994). A unique amino acid of the Drosophila GABA receptor with influence on drug sensitivity by two mechanisms. The Journal of Physiology, 479, 65–75. doi:10.1113/jphysiol.1994.sp020278.
  • Zhang, H.G., Lee, H.J., Rocheleau, T., ffrench-Constant, R.H., & Jackson, M.B. (1995). Subunit composition determines picrotoxin and bicuculline sensitivity of Drosophila gamma-aminobutyric acid receptors. Molecular Pharmacology, 48, 835–840.
  • Zhang, Y., Wang, X., Yang, B., Hu, Y., Huang, L., Bass, C., & Liu, Z. (2015). Reduction in mRNA and protein expression of a nicotinic acetylcholine receptor α8 subunit is associated with resistance to imidacloprid in the brown planthopper, Nilaparvata lugens. Journal of Neurochemistry, 135, 686–694. doi:10.1111/jnc.13281.
  • Zhao, X.L., Yeh, J.Z., Salgado, V.L., & Narahashi, T. (2004). Fipronil is a potent open channel blocker of glutamate-activated chloride channels in cockroach neurons. Journal of Pharmacology and Experimental Therapeutics, 310, 192–201. doi:10.1124/jpet.104.065516.
  • Zimmer, C.T., Garrood, W.T., Puinean, A.M., Eckel-Zimmer, M., Williamson, M.S., Davies, T.G.E., & Bass, C. (2016). A CRISPR/Cas9 mediated point mutation in the alpha 6 subunit of the nicotinic acetylcholine receptor confers resistance to spinosad in Drosophila melanogaster. Insect Biochemistry and Molecular Biology, 73, 62–69. doi:10.1016/j.ibmb.2016.04.007.