A nicotinic acetylcholine receptor transmembrane point mutation (G275E) associated with resistance to spinosad in Frankliniella occidentalis

Journal of Neurochemistry

Volumn 124, Issue 5, 2013, Pages 590-601

  Puinean, Alin M ^a   Lansdell, Stuart J ^a   Collins, Toby ^a   Bielza, Pablo ^b   Millar, Neil S ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b TECHNICAL UNIVERSITY OF CARTAGENA   (Spain)

Author keywords

Frankliniella occidentalis; insecticide resistance; nicotinic acetylcholine receptor; spinosad

Indexed keywords

ACETYLCHOLINE; BUNGAROTOXIN RECEPTOR; CHLORIDE CHANNEL; GLUTAMIC ACID; GLYCINE; IVERMECTIN; NICOTINIC ACETYLCHOLINE RECEPTOR ALPHA6; NICOTINIC RECEPTOR; SPINOSAD; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ANIMAL CELL; BINDING SITE; CONTROLLED STUDY; FRANKLINIELLA; FRANKLINIELLA OCCIDENTALIS; HUMAN; HUMAN CELL; INSECTICIDE RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL MEMBRANE; DRUG COMBINATIONS; HUMANS; INSECTICIDE RESISTANCE; INSECTICIDES; MACROLIDES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PATCH-CLAMP TECHNIQUES; POINT MUTATION; RECEPTORS, NICOTINIC; THYSANOPTERA;

CAENORHABDITIS ELEGANS; FRANKLINIELLA OCCIDENTALIS; HEXAPODA;

EID: 84874111588     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12029     Document Type: Review

References (60)

1. Amiri S., Shimomura M., Vijayan R., Nishiwaki H., Akamatsu M., Matsuda K., Jones A. K., Sansom M. S. P., Biggin P. C., and, Sattelle D. B., (2008) A role for Leu118 of loop E in agonist binding to the α7 nicotinic acetylcholine receptor. Mol. Pharmacol. 73, 1659-1667. (Pubitemid 351724355)
2. Bass C., Puinean A. M., Andrews M., et al,. (2011) Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neurosci. 12, 51.
3. Baxter S. W., Chen M., Dawson A., Zhao J.-Z., Vogel H., Shelton A. M., Heckel D. G., and, Jiggins C. D., (2010) Mis-spliced transcripts of nicotinic acetylcholine receptor α6 are associated with field evolved spinosad resistance in Plutella xylostells (L.). PLoS Genet. 6, e1000802. doi: 10.1371/journal.pgen.1000802.
4. Bielza P., (2008) Insecticide resistance management strategies against the western flower thrips, Frankliniella occidentalis. Pest Manag. Sci. 64, 1131-1138.
5. Bielza P., Quinto V., Contreras J., Torné M., Martín A., and, Espinosa P. J., (2007a) Resistance to spinosad in the western flower thrips, Frankliniella occidentalis (Pergande), in greenhouses of south-eastern Spain. Pest Manag. Sci. 63, 682-687. (Pubitemid 47025962)
6. Bielza P., Quinto V., Fernández E., Grávalos C., and, Contreras J., (2007b) Genetics of spinosad resistance in Frankliniella occidentalis (Thysanoptera: Thripidae). J. Econ. Entomol. 100, 916-920. (Pubitemid 46960193)
7. Broadbent S., Groot-Kormelink P. J., Krashia P. A., Harkness P. C., Millar N. S., Beato M., and, Sivilotti L. G., (2006) Incorporation of the β3 subunit has a dominant-negative effect on the function of recombinant central-type neuronal nicotinic receptors. Mol. Pharmacol. 70, 1350-1356.
8. Collins T., and, Millar N. S., (2010) Nicotinic acetylcholine receptor transmembrane mutations convert ivermectin from a positive to a negative allosteric modulator. Mol. Pharmacol. 78, 198-204.
9. Collins T., Young G. T., and, Millar N. S., (2011) Competitive binding at a nicotinic receptor transmembrane site of two α7-selective positive allosteric modulators with differing effects on agonist-evoked desensitization. Neuropharmacology 61, 1306-1313.
10. Corringer P.-J., Baaden M., Bocquet N., Delarue M., Dufresne V., Nury H., Prevost M., and, Van Renterghem C., (2010) Atomic structure and dynamics of pentameric ligand-gated ion channels: new insight from bacterial homologues. J. Physiol. 588, 565-572.
11. Couturier S., Bertrand D., Matter J. M., Hernandez M. C., Bertrand S., Millar N., Valera S., Barkas T., and, Ballivet M., (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5, 847-856.
12. Craig P. J., Bose S., Zwart R., et al,. (2004) Stable expression and characterisation of a human α7 nicotinic subunit chimera: a tool for functional high-throughput screening. Eur. J. Pharmacol. 502, 31-40. (Pubitemid 39311362)
13. 3H]methyllycaconitine: a new radioligand for α7-type neuronal nicotinic acetylcholine receptors. Neuropharmacology 38, 679-690. (Pubitemid 29150322)
14. Gill J. K., Savolainen M., Young G. T., Zwart R., Sher E., and, Millar N. S., (2011) Agonist activation of α7 nicotinic acetylcholine receptors via an allosteric transmembrane site. Proc. Natl Acad. Sci. USA 108, 5867-5872.
15. Gill J. K., Dhankher P., Sheppard T. D., Sher E., and, Millar N. S., (2012) A series of α7 nicotinic acetylcholine receptor allosteric modulators with close chemical similarity but diverse pharmacological properties. Mol. Pharmacol. 81, 710-718.
16. Grauso M., Reenan R. A., Culetto E., and, 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. (Pubitemid 34454375)
17. Guillén J., and, Bielza P., (2012) Thiamethoxam acts as a target-site synergist of spinosad in resistant strains of Frankliniella occidentalis. Pest Manag. Sci. 68, [published on-line]. doi: 10.1002/ps.3372.
18. Harkness P. C., and, Millar N. S., (2001) Inefficient cell-surface expression of hybrid complexes formed by the co-assembly of neuronal nicotinic acetylcholine receptor and serotonin receptor subunits. Neuropharmacology 41, 79-87. (Pubitemid 32607647)
19. Hibbs R. E., and, Gouaux E., (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474, 54-60.
20. Jones A. K., and, 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:310.1186/1471-2164-1188-1327.
21. Jones A. K., and, Sattelle D. B., (2010) Diversity of insect nicotinic acetylcholine receptor subunits. Adv. Exp. Med. Biol. 683, 25-43.
22. Krause R. M., Buisson B., Bertrand S., Corringer P.-J., Galzi J.-L., Changeux J.-P., and, Bertrand D., (1998) Ivermectin: a positive allosteric effector of the α7 neuronal nicotinic acetylcholine receptor. Mol. Pharmacol. 53, 283-294. (Pubitemid 28099739)
23. Kwon D. H., Yoon K. S., Clark J. M., and, 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 Mol. Biol. 19, 583-591.
24. Lansdell S. J., and, Millar N. S., (2004) Molecular characterisation of Dα6 and Dα7 nicotinic acetylcholine receptor subunits from Drosophila: formation of a high-affinity α-bungarotoxin binding site revealed by expression of subunit chimeras. J. Neurochem. 90, 479-489. (Pubitemid 38938233)
25. Lansdell S. J., Collins T., Yabe A., Gee V. J., Gibb A. J., and, Millar N. S., (2008) Host-cell specific effects of the nicotinic acetylcholine receptor chaperone RIC-3 revealed by a comparison of human and Drosophila RIC-3 homologues. J. Neurochem. 105, 1573-1581. (Pubitemid 351678482)
26. Lester H. A., Dibas M. I., Dahan D. S., Leite J. F., and, Dougherty D. A., (2004) Cys-loop receptors: new twists and turns. Trends Neurosci. 27, 329-336. (Pubitemid 38692414)
27. Liu Z., Williamson M. S., Lansdell S. J., Denholm I., Han Z., and, Millar N. S., (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. (Pubitemid 40862751)
28. Liu Z., Williamson M. S., Lansdell S. J., Han Z., Denholm I., and, Millar N. S., (2006) A nicotinic acetylcholine receptor mutation (Y151S) causes reduced agonist potency to a range of neonicotinoid insecticides. J. Neurochem. 99, 1273-1281. (Pubitemid 44655291)
29. Lynagh T., and, Lynch J. W., (2010) An improved ivermectin-activated chloride channel receptor for inhibiting electrical activity in defined neuronal populations. J. Biol. Chem. 285, 14890-14897.
30. Lynagh T., Webb T., Dixon C. L., Cromer B. A., and, Lynch J. W., (2011) Molecular determinants of ivermectin sensitivity at the glycine receptor chloride channel. J. Biol. Chem. 286, 43913-43924.
31. Markussen M. D. K., and, Kristensen M., (2011) Spinosad resistance in female Musca domestica L. from a field-derived population. Pest Manag. Sci. 68, 75-82.
32. Matsuda K., Shimomura M., Kondo Y., et al,. (2000) Role of loop D of the α7 nicotinic acetylcholine receptor in its interaction with the insecticide imidacloprid and related neonicotinoids. Br. J. Pharmacol. 130, 981-986. (Pubitemid 30453531)
33. Millar N. S., (1999) Heterologous expression of mammalian and insect neuronal nicotinic acetylcholine receptors in cultured cell lines. Biochem. Soc. Trans. 27, 944-950. (Pubitemid 30032158)
34. Millar N. S., (2008) RIC-3: a nicotinic acetylcholine receptor chaperone. Br. J. Pharmacol. 153, S177-S183. (Pubitemid 351341014)
35. Millar N. S., and, Denholm I., (2007) Nicotinic acetylcholine receptors: targets for commercially important insecticides. Invert. Neurosci. 7, 53-66. (Pubitemid 46348846)
36. Millar N. S., and, Gotti C., (2009) Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology 56, 237-246.
37. Millar N. S., and, Lansdell S. J., (2010) Characterisation of insect nicotinic acetylcholine receptors by heterologous expression. Adv. Exp. Med. Biol. 683, 65-73.
38. Mota-Sanchez D., Hollingworth R. M., Grafius E. J., and, Moyer D. D., (2006) Resistance and cross-resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Pest Manag. Sci. 62, 30-37. (Pubitemid 43194381)
39. Orr N., Shaffner A. J., Richey K., and, Crouse G. D., (2009) Novel mode of action of spinosad: receptor binding studies demonstrating lack of interaction with known insecticidal targets. Pest. Biochem. Physiol. 95, 1-5.
40. Peng X., Katz M., Gerzanich V., Anand R., and, Lindstrom J., (1994) Human α7 acetylcholine receptor: cloning of the α7 subunit from the SH-SY5Y cell line and determination of pharmacological properties of native receptors and functional α7 homomers in Xenopus oocytes. Mol. Pharmacol. 45, 546-554.
41. Perry T., McKenzie J. A., and, Batterham P., (2007) A Dα6 knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad. Insect Biochem. Mol. Biol. 37, 184-188. (Pubitemid 46109310)
42. Raymond V., and, Sattelle D. B., (2002) Novel animal-health drug targets from ligand-gated chloride channels. Nat. Rev. Drug Discov. 1, 427-436. (Pubitemid 37361485)
43. Rinkevich F. D., and, Scott J. G., (2009) Transcriptional diversity and allelic variation in nicotinic acetylcholine receptor subunits of the red flour beetle, Tribolium castaneum. Insect Mol. Biol. 18, 233-242.
44. Rinkevich F. D., Chen M., Shelton A. M., and, 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. Invert Neurosci. 10, 25-33.
45. Roe R. M., Young H. P., Iwasa T., Wyss C. F., Stumpf C. F., Sparks T. C., Watson G. B., Sheets J. J., and, Thompson G. D., (2010) Mechanism of resistance to spinosyn in the tobacco budworm, Heliothis virescens. Pest. Biochem. Physiol. 96, 8-13.
46. Salgado V. L., and, Saar R., (2004) Desensitizing and non-desensitizing subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in cockroach neurons. J. Insect Physiol. 50, 867-879. (Pubitemid 39415792)
47. Salgado V. L., Sheets J. J., Watson G. B., and, Schmidt A. L., (1998) Studies on the mode of action of spinosad: the internal effective concentration and the concentration dependence of neural excitation. Pest. Biochem. Physiol. 60, 103-110. (Pubitemid 28343937)
48. Scott J. G., (1999) Cytochrome P450 and insecticide resistance. Insect Biochem. Mol. Biol. 29, 757-777.
49. Shimomura M., Okuda H., Matsuda K., Komai K., Akamatsu M., and, Sattelle D. B., (2002) Effects of mutations of a glutamine residue in loop D of the α7 nicotinic acetylcholine receptor on agonist profiles for neonicotinoid insecticides and related ligands. Br. J. Pharmacol. 137, 162-169.
50. Shimomura M., Yokota M., Okumura M., Matsuda K., Akamatsu M., Sattelle D. B., and, Komai K., (2003) Combinatorial mutations in loops D and F strongly influence responses of the α7 nicotinic acetylcholine receptor to imidacloprid. Brain Res. 991, 71-77. (Pubitemid 37297935)
51. Shono T., and, Scott J. G., (2003) Spinosad resistance in the housefly, Musca domestica, is due to a recessive factor on autosome 1. Pest. Biochem. Physiol. 75, 1-7. (Pubitemid 36521981)
52. Sparks T. C., Thompson G. D., Kirst H. A., Hertlein M. B., Larson L. L., Worden T. V., and, Thibault S. T., (1998) Biological activity of the spinosyns, new fermentation derived insect control agents, on tobacco budworm (Lepidoptera: Noctuidae) Larvae. J. Econ. Entomol. 91, 1277-1283. (Pubitemid 128500147)
53. Thompson G. D., Dutton R., and, Sparks T. C., (2000) Spinosad-a case study: an example from a natural products discovery programme. Pest Manag. Sci. 56, 696-702. (Pubitemid 30483322)
54. Unwin N., (2005) Refined structure of the nicotinic acetylcholine receptor at 4Å resolution. J. Mol. Biol. 346, 967-989. (Pubitemid 40215523)
55. Watson G. B., Chouinard S. W., Cook K. R., et al,. (2010) A spinosyn-sensitive Drosophila melanogaster nicotinic acetylcholine receptor identified through chemically induced target site resistance, resistance gene identification, and heterologous expression. Insect Biochem. Mol. Biol. 40, 376-384.
56. Wolstenholme A. J., (2010) Recent progress in understanding the interaction between avermectins and ligand-gated ion channels: putting the pests to sleep. Invert. Neurosci. 10, 5-10.
57. Wolstenholme A. J., and, Kaplan R. M., (2012) Resistance to macrocyclic lactones. Curr. Pharm. Biotechnol. 13, 873-887.
58. Young H. P., Bailey W. D., and, Roe R. M., (2003) Spinosad selection of a laboratory strain of the tobacco budworm, Heliothis virescens (Lepidoptera: Noctuidae), and characterization of resistance. Crop Protection 22, 265-273. (Pubitemid 36247100)
59. Young G. T., Broad L. M., Zwart R., Astles P. C., Bodkin M., Sher E., and, Millar N. S., (2007) Species selectivity of a nicotinic acetylcholine receptor agonist is conferred by two adjacent extracellular β4 amino acids that are implicated in the coupling of binding to channel gating. Mol. Pharmacol. 71, 389-397. (Pubitemid 46147905)
60. Young G. T., Zwart R., Walker A. S., Sher E., and, Millar N. S., (2008) Potentiation of α7 nicotinic acetylcholine receptors via an allosteric transmembrane site. Proc. Natl Acad. Sci. USA 105, 14686-14691.