The actions of the neonicotinoid imidacloprid on cholinergic neurons of Drosophila melanogaster

Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies P, de Pablos B, Delcher A, Deng Z, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong F, Gorrell JH, Gu Z, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston KA, Howland TJ, Wei MH, Ibegwam C, Jalali M, Kalush F, Karpen GH, Ke Z, Kennison JA, Ketchum KA, Kimmel BE, Kodira CD, Kraft C, Kravitz S, Kulp D, Lai Z, Lasko P, Lei Y, Levitsky AA, Li J, Li Z, Liang Y, Lin X, Liu X, Mattei B, McIntosh TC, McLeod MP, McPherson D, Merkulov G, Milshina NV, Mobarry C, Morris J, Moshrefi A, Mount SM, Moy M, Murphy B, Murphy L, Muzny DM, Nelson DL, Nelson DR, Nelson KA, Nixon K, Nusskern DR, Pacleb JM, Palazzolo M, Pittman GS, Pan S, Pollard J, Puri V, Reese MG, Reinert K, Remington K, Saunders RD, Scheeler F, Shen H, Shue BC, Siden-Kiamos I, Simpson M, Skupski MP, Smith T, Spier E, Spradling AC, Stapleton M, Strong R, Sun E, Svirskas R, Tector C, Turner R, Venter E, Wang AH, Wang X, Wang ZY, Wassarman DA, Weinstock GM, Weissenbach J, Williams SM, WoodageT, Worley KC, Wu D, Yang S, Yao QA, Ye J, Yeh RF, Zaveri JS, Zhan M, Zhang G, Zhao Q, Zheng L, Zheng XH, Zhong FN, Zhong W, Zhou X, Zhu S, Zhu X, Smith HO, Gibbs RA, Myers EW, Rubin GM, Venter JC (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195

Bai DL, Lummis SCR, Leicht W, Breer H, Sattelle DB (1991) Actions of imidacloprid and a related nitromethylene on cholinergic receptors of an identified insect motor-neuron. Pest Sci 33:197–204

Bertrand D, Ballivet M, Gomez M, Bertrand S, Phannavong B, Gundelfinger ED (1994) Physiological properties of neuronal nicotinic receptors reconstituted from the vertebrate beta 2 subunit and Drosophila alpha subunits. Eur J Neurosci 6:869–875

Blagburn JM, Sattelle DB (1987) Nicotinic acetylcholine receptors on a cholinergic nerve terminal in the cockroach, Periplaneta americana. J Comp Physiol [A] 161:215–225

Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415

Buckingham S, Lapied B, Corronc H, Sattelle DB (1997) Imidacloprid actions on insect neuronal acetylcholine receptors. J Exp Biol 200:2685–2692

Buckingham SD, Balk ML, Lummis SC, Jewess P, Sattelle DB (1995) Actions of nitromethylenes on an alpha-bungarotoxin-sensitive neuronal nicotinic acetylcholine receptor. Neuropharmacology 34:591–597

Cayre M, Buckingham SD, Yagodin S, Sattelle DB (1999) Cultured insect mushroom body neurons express functional receptors for acetylcholine, GABA, glutamate, octopamine, and dopamine. J Neurophysiol 81:1–14

Courjaret R, Lapied B (2001) Complex intracellular messenger pathways regulate one type of neuronal alpha-bungarotoxin-resistant nicotinic acetylcholine receptors expressed in insect neurosecretory cells (dorsal unpaired median neurons). Mol Pharmacol 60:80–91

Deglise P, Grunewald B, Gauthier M (2002) The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells. Neurosci Lett 321:13–16

Delgado R, Latorre R, Labarca P (1994) Shaker mutants lack post-tetanic potentiation at motor end-plates. Eur J Neurosci 6:1160–1166

Fischer JA, Giniger E, Maniatis T, Ptashne M (1988) GAL4 activates transcription in Drosophila. Nature 332:853–856

Grauso M, Reenan RA, Culetto E, Sattelle DB (2002) Novel putative nicotinic acetylcholine receptor subunit genes, Dalpha5, Dalpha6 and Dalpha7, 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

Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440–3450

Hoopengardner B, Bhalla T, Staber C, Reenan R (2003) Nervous system targets of RNA editing identified by comparative genomics. Science 301:832–836

Huang Y, Williamson MS, Devonshire AL, Windass JD, Lansdell SJ, Millar NS (1999) Molecular characterization and imidacloprid selectivity of nicotinic acetylcholine receptor subunits from the peach-potato aphid Myzus persicae. J Neurochem 73:380–389

Kao PN, Karlin A (1986) Acetylcholine receptor binding site contains a disulfide cross-link between adjacent half-cystinyl residues. J Biol Chem 261:8085–8088

Lane NJ, Sattelle DB, Hufnagel LA (1983) Pre- and post-synaptic structures in insect CNS: intramembranous features and sites of alpha-bungarotoxin binding. Tissue Cell 15:921–937

Lane NJ, Swales LS, David JA, Sattelle DB (1982) Differential accessibility to two insect neurones does not account for differences in sensitivity to alpha-bungarotoxin. Tissue Cell 14:489–500

Lansdell SJ, Millar NS (2000a) Cloning and heterologous expression of Dalpha4, a Drosophila neuronal nicotinic acetylcholine receptor subunit: identification of an alternative exon influencing the efficiency of subunit assembly. Neuropharmacology 39:2604–2614

Lansdell SJ, Millar NS (2000b) The influence of nicotinic receptor subunit composition upon agonist, alpha-bungarotoxin and insecticide (imidacloprid) binding affinity. Neuropharmacology 39:671–679

Lansdell SJ, Millar NS (2004) Molecular characterization of Dalpha6 and Dalpha7 nicotinic acetylcholine receptor subunits from Drosophila: formation of a high-affinity alpha-bungarotoxin binding site revealed by expression of subunit chimeras. J Neurochem 90:479–489

Littleton JT, Ganetzky B (2000) Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26:35–43

Liu Z, Williamson MS, Lansdell SJ, Denholm I, Han Z, Millar NS (2005) A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proc Natl Acad Sci USA 102:8420–8425

Matsuda K, Buckingham SD, Freeman JC, Squire MD, Baylis HA, Sattelle DB (1998) Effects of the alpha subunit on imidacloprid sensitivity of recombinant nicotinic acetylcholine receptors. Br J Pharmacol 123:518–524

Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573–580

Oertner TG, Single S, Borst A (1999) Separation of voltage- and ligand-gated calcium influx in locust neurons by optical imaging. Neurosci Lett 274:95–98

Salvaterra PM, Kitamoto T (2001) Drosophila cholinergic neurons and processes visualized with Gal4/UAS-GFP. Brain Res Gene Exp Patterns 1:73–82

Sattelle DB, Jones AK, Sattelle BM, Matsuda K, Reenan R, Biggin PC (2005) Edit, cut and paste in the nicotinic acetylcholine receptor gene family of Drosophila melanogaster. Bioessays 27:366–376

Schulz R, Sawruk E, Mulhardt C, Bertrand S, Baumann A, Phannavong B, Betz H, Bertrand D, Gundelfinger ED, Schmitt B (1998) Dalpha3, a new functional alpha subunit of nicotinic acetylcholine receptors from Drosophila. J Neurochem 71:853–862

Su H, O’Dowd DK (2003) Fast synaptic currents in Drosophila mushroom body Kenyon cells are mediated by alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors and picrotoxin-sensitive GABA receptors. J Neurosci 23:9246–9253

Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–268

Vermehren A, Qazi S, Trimmer BA (2001) The nicotinic alpha subunit MARA1 is necessary for cholinergic evoked calcium transients in Manduca neurons. Neurosci Lett 313:113–116

Webster N, Jin JR, Green S, Hollis M, Chambon P (1988) The yeast UASG is a transcriptional enhancer in human HeLa cells in the presence of the GAL4 trans-activator. Cell 52:169–178

Wegener C, Hamasaka Y, Nassel DR (2004) Acetylcholine increases intracellular Ca2+ via nicotinic receptors in cultured PDF-containing clock neurons of Drosophila. J Neurophysiol 91:912–923

Wu CF, Suzuki N, Poo MM (1983) Dissociated neurons from normal and mutant Drosophila larval central nervous system in cell culture. J Neurosci 3:1888–1899