1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Entomology
  4. Volume 63, 2018
  5. Article

Annual Review of Entomology

Volume 63, 2018

Neonicotinoids and Other Insect Nicotinic Receptor Competitive Modulators: Progress and Prospects

Abstract

Neonicotinoids (neonics) are remarkably effective as plant systemics to control sucking insects and for flea control on dogs and cats. The nitroimines imidacloprid, clothianidin, thiamethoxam, and dinotefuran are the leaders among the seven commercial neonics that also include the nitromethylene nitenpyram, the nitromethylene-derived cycloxaprid, and the cyanoimines acetamiprid and thiacloprid. Honey bees are highly sensitive to the nitroimines and nitromethylenes, but the cyanoimines are less toxic. All neonics are nicotinic acetylcholine receptor (nAChR) agonists with a common mode of action, target-site cross-resistance, and much higher potency on insect than mammalian nAChRs at defined binding sites. The structurally related sulfoximine sulfoxaflor and butenolide flupyradifurone are also nAChR agonists, and the mesoionic triflumezopyrim is a nAChR competitive modulator with little or no target-site cross-resistance. Some neonics induce stress tolerance in plants via salicylate-associated systems. The neonics in general are readily metabolized and, except for pollinators, have favorable toxicological profiles.

Keyword(s): clothianidin, dinotefuran, honey bees, imidacloprid, nicotinic receptors, thiamethoxam
Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-020117-043042
2018-01-07
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/ento/63/1/annurev-ento-020117-043042.html?itemId=/content/journals/10.1146/annurev-ento-020117-043042&mimeType=html&fmt=ahah

Literature Cited

  1. Akayama A, Minamida I. 1.  1999. Discovery of a new systemic insecticide, nitenpyram and its insecticidal properties. See Ref. 146 127–48
  2. Alptekin S, Bass C, Nicholls C, Paine MJ, Clark SJ. 2.  et al. 2016. Induced thiacloprid insensitivity in honeybees (Apis mellifera L.) is associated with up-regulation of detoxification genes. Insect Mol. Biol. 25:171–80 [Google Scholar]
  3. 3. Aust. Pestic. Vet. Med. Auth. 2013. Public release summary on the evaluation of the new active ingredient sulfoxaflor in the product transform insecticide68 Australian Pesticides and Veterinary Medicines Authority, Kingston, Aust.
  4. Bao H, Shao X, Zhang Y, Deng Y, Xu X. 4.  et al. 2016. Specific synergist for neonicotinoid insecticides: IPPA08, a cis-neonicotinoid compound with a unique oxabridged substructure. J. Agric. Food Chem. 64:5148–55 [Google Scholar]
  5. Bass C, Carvalho RA, Oliphant L, Puinean AM, Field LM. 5.  et al. 2011. Overexpression of a cytochrome P450 monooxygenase, CYP6ER1, is associated with resistance to imidacloprid in the brown planthopper, Nilaparvata lugens. Insect Mol. Biol. 20:763–73 [Google Scholar]
  6. Bass C, Puinean AM, Zimmer CT, Denholm I, Field LM. 6.  et al. 2014. The evolution of insecticide resistance in the peach potato aphid. Myzus persicae. Insect Biochem. Mol. Biol. 51:41–51 [Google Scholar]
  7. Blacquière T, Smagghe G, Van Gestel CAM, Mommaerts V. 7.  2012. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–92 [Google Scholar]
  8. Brunet J-L, Badiou A, Belzunces LP. 8.  2005. In vivo metabolic fate of [14C]-acetamiprid in six biological compartments of the honeybee, Apismellifera L. Pest Manag. Sci. 61:742–48 [Google Scholar]
  9. Cahill M, Denholm I. 9.  1999. Managing resistance to the chloronicotinyl insecticides-rhetoric or reality?. See Ref. 146 253–70
  10. Casida JE. 10.  2011. Neonicotinoid metabolism: compounds, substituents, pathways, enzymes, organisms and relevance. J. Agric. Food Chem. 59:2923–31 [Google Scholar]
  11. Casida JE. 11.  2015. Golden age of RyR and GABA-R diamide and isoxazoline insecticides: common genesis, serendipity, surprises, selectivity, and safety. Chem. Res. Toxicol. 28:560–66 [Google Scholar]
  12. Casida JE, Durkin KA. 12.  2013. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu. Rev. Entomol. 58:99–117 [Google Scholar]
  13. Casida JE, Durkin KA. 13.  2017. Pesticide chemical research in toxicology: lessons from nature. Chem. Res. Toxicol. 30:94–104 [Google Scholar]
  14. Casida JE, Quistad GB. 14.  1998. Golden age of insecticide research: past, present, or future?. Annu. Rev. Entomol. 43:1–16 [Google Scholar]
  15. Celie PHN, van Rossum-Fikkert SE, van Dijk WJ, Brejc K, Smit AB, Sixma TK. 15.  2004. Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 41:907–14 [Google Scholar]
  16. Chamaon K, Smalla K-H, Thomas U, Gundelfinger ED. 16.  2002. Nicotinic acetylcholine receptors of Drosophila: Three subunits encoded by genomically linked genes can co-assemble into the same receptor complex. J. Neurochem. 80:149–57 [Google Scholar]
  17. Chao SL, Casida JE. 17.  1997. Interaction of imidacloprid metabolites and analogs with the nicotinic acetylcholine receptor of mouse brain in relation to toxicity. Pestic. Biochem. Physiol. 58:77–88 [Google Scholar]
  18. Chao SL, Dennehy TJ, Casida JE. 18.  1997. Whitefly (Hemiptera: Aleyrodidae) binding site for imidacloprid and related insecticides: a putative nicotinic acetylcholine receptor. J. Econ. Entomol. 90:879–82 [Google Scholar]
  19. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA. 19.  et al. 2006. A deficit of detoxification enzymes: pesticides sensitivity and environmental response in the honeybee. Insect Mol. Biol. 15:615–36 [Google Scholar]
  20. Cordova D, Benner EA, Schroeder ME, Holyoke CW, Zhang W. 20.  et al. 2016. Mode of action of triflumezopyrim: a novel mesoionic insecticide which inhibits the nicotinic acetylcholine receptor. Insect Biochem. Mol. Biol. 74:32–41 [Google Scholar]
  21. Cutler P, Slater R, Edmunds AJ, Maienfisch P, Hall RG. 21.  et al. 2013. Investigating the mode of action of sulfoxaflor: a fourth-generation neonicotinoid. Pest Manag. Sci. 69:607–19 [Google Scholar]
  22. D'Amour KA, Casida JE. 22.  1999. Desnitroimidacloprid and nicotine binding site in rat recombinant α4β2 neuronal nicotinic acetylcholine receptor. Pestic. Biochem. Physiol. 64:55–61 [Google Scholar]
  23. David D, George IA, Peter JV. 23.  2008. Toxicology of the newer neonicotinoid: imidacloprid poisoning in a human. Clin. Toxicol. 45:485–86 [Google Scholar]
  24. Decourtye A, Devillers J. 24.  2010. Ecotoxicity of neonicotinoid insecticides to bees. Insect Nicotinic Acetylcholine Receptor SH Thany 85–95 Adv. Exp. Med. Biol New York: Springer [Google Scholar]
  25. Dick RA, Kanne DB, Casida JE. 25.  2005. Identification of aldehyde oxidase as the neonicotinoid nitroreductase. Chem. Res. Toxicol. 18:317–23 [Google Scholar]
  26. Dick RA, Kanne DB, Casida JE. 26.  2006. Substrate specificity of rabbit aldehyde oxidase for nitroguanidine and nitromethylene neonicotinoid insecticides. Chem. Res. Toxicol. 19:38–43 [Google Scholar]
  27. Elbert A, Haas M, Springer B, Thielert W, Nauen R. 27.  2008. Applied aspects of neonicotinoid uses in crop protection. Pest Manag. Sci. 64:1099–105 [Google Scholar]
  28. Ford KA, Casida JE. 28.  2006. Chloropyridinyl neonicotinoid insecticides: Diverse molecular substituents contribute to facile metabolism in mice. Chem. Res. Toxicol. 19:944–51 [Google Scholar]
  29. Ford KA, Casida JE. 29.  2006. Unique and common metabolites of thiamethoxam, clothianidin and dinotefuran in mice. Chem. Res. Toxicol. 19:1549–56 [Google Scholar]
  30. Ford KA, Casida JE. 30.  2008. Comparative metabolism and pharmacokinetics of seven neonicotinoid insecticides in spinach. J. Agric. Food Chem. 56:10168–75 [Google Scholar]
  31. Ford KA, Casida JE, Chandran D, Gulevich AG, Okrent RA. 31.  et al. 2010. Neonicotinoid insecticides induce salicylate-associated plant defense responses. PNAS 107:17527–32 [Google Scholar]
  32. Ford KA, Gulevich AG, Swenson TL, Casida JE. 32.  2011. Neonicotinoid insecticides: oxidative stress in Planta and metallo-oxidase inhibition. J. Agric. Food Chem. 59:4860–67 [Google Scholar]
  33. Fryday S, Tiede K, Stein J. 33.  2015. Scientific services to support EFSA systematic reviews: Lot 5 Systematic literature review on the neonicotinoids (namely active substances clothianidin, thiamethoxam and imidacloprid) and the risks to bees. EFSA Support. Publ. 12:756E [Google Scholar]
  34. Gibbons D, Morrissey C, Mineau P. 34.  2015. A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ. Sci. Pollut. Res. 22:103–18 [Google Scholar]
  35. Glynne Jones D. 35.  1998. Piperonyl Butoxide: The Insecticide Synergist San Diego, CA: Academic
  36. Godfray HC, Blacquière T, Field LM, Hails RS, Petrokofsky G. 36.  et al. 2014. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. R. Soc. B 281:20140558 [Google Scholar]
  37. Gonias ED, Oosterhuis DM, Bibi AC. 37.  2008. Physiologic response of cotton to the insecticide imidacloprid under high temperature stress. J. Plant Growth Regul. 27:77–82 [Google Scholar]
  38. Goulson D. 38.  2013. An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 50:977–87 [Google Scholar]
  39. Green T, Toghill A, Lee R, Waechter F, Weber E. 39.  et al. 2005. Thiamethoxam induced mouse liver tumors and their relevance to humans. Part 2: species differences in response. J. Toxicol. Sci. 86:48–55 [Google Scholar]
  40. Hardstone MC, Scott JG. 40.  2010. Is Apis mellifera more sensitive to insecticides than other insects?. Pest Manag. Sci. 66:1171–80 [Google Scholar]
  41. Holyoke CW Jr., Zhang W, Pahutski TF Jr., Lahm GP, Tong MT. 41.  et al. 2015. Triflumezopyrim: discovery and optimization of a mesoionic insecticide for rice. In Discovery and Synthesis of Crop Protection Products, ed. P Maienfisch, TM Stevenson, pp. 365–75. ACS Sympos. Ser Washington, DC: Am. Chem. Soc. [Google Scholar]
  42. Honda H, Tomizawa M, Casida JE. 42.  2006. Insect nicotinic acetylcholine receptors: Neonicotinoid binding site specificity is usually but not always conserved with varied substituents and species. J. Agric. Food Chem. 54:3365–71 [Google Scholar]
  43. Honda H, Tomizawa M, Casida JE. 43.  2006. Neonicotinoid metabolic activation and inactivation established with coupled nicotinic receptor-CYP3A4 and aldehyde oxidase systems. Toxicol. Lett. 161:108–14 [Google Scholar]
  44. Hopwood J, Vaughan M, Shepherd M, Biddinger D, Mader E. 44.  et al. 2012. Are neonicotinoids killing bees? A review of research into the effects of neonicotinoid insecticides on bees, with recommendations for action Xerces Soc. Invertebr. Conserv Portland, OR:
  45. Iwasa T, Motoyama N, Ambrose JT, Roe RM. 45.  2004. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee. Apis mellifera. Crop. Prot. 23:371–78 [Google Scholar]
  46. Jeschke P, Moriya K, Lantzsch R, Seifert H, Lindner W. 46.  et al. 2001. Thiacloprid (Bay YRC 2894)—a new member of the chloronicotinyl insecticide (CNI) family. Pflanzenschutz Nachr. Bayer 54:147–60 [Google Scholar]
  47. Jeschke P, Nauen R. 47.  2008. Neonicotinoids—from zero to hero in insecticide chemistry. Pest Manag. Sci. 64:1084–98 [Google Scholar]
  48. Jeschke P, Nauen R, Beck ME. 48.  2013. Nicotinic acetylcholine receptor agonists: a milestone for modern crop protection. Angew. Chem. Int. Ed. 52:9464–85 [Google Scholar]
  49. Jeschke P, Nauen R, Gutbrod O, Beck ME, Matthiesen S. 49.  et al. 2014. Flupyradifurone (Sivanto TM) and its novel butenolide pharmacophore: structural considerations. Pestic. Biochem. Physiol. 121:31–38 [Google Scholar]
  50. Johnson RM. 50.  2015. Honey bee toxicology. Annu. Rev. Entomol. 60:415–34 [Google Scholar]
  51. Johnson RM, Mao W, Pollock HS, Niu G, Schuler MA, Berenbaum MR. 51.  2012. Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PLOS ONE 7:2e31051 [Google Scholar]
  52. Jones AK, Raymond-Delpech V, Thany AH, Gauthier M, Sattelle DB. 52.  2006. The nicotinic acetylcholine receptor gene family of the honey bee. Apis mellifera. Genome Res. 16:1422–30 [Google Scholar]
  53. Junquera P. 53.  2014. Neonicotinoids for veterinary use on dogs, cats and livestock against external parasites Parasitipedia.net, Zürich, Switz., updated Aug. 4. http://parasitipedia.net/index.php?option=com_content&view=article&id=2411&Itemid=2676
  54. Kagabu S. 54.  1997. Chloronicotinoyl insecticides—discovery, application and future perspective. Rev. Toxicol. 1:75–129 [Google Scholar]
  55. Kagabu S. 55.  2003. Molecular design of neonicotinoids: past, present and future. Chemistry of Crop Protection, Progress and Prospects in Science and Regulation G Voss, G Ramos 193–212 Weinheim, Ger.: Wiley-VCH [Google Scholar]
  56. Kagabu S, Maienfisch P, Zhang A, Granda-Minones J, Haettenschwiler J. 56.  et al. 2000. 5-Azidoimidacloprid and an acyclic analogue as candidate photoaffinity probes for mammalian and insect nicotinic acetylcholine receptors. J. Med. Chem. 43:5003–9 [Google Scholar]
  57. Kagabu S, Medej S. 57.  1995. Stability comparison of imidacloprid and related compounds under simulated sunlight, hydrolysis conditions, and to oxygen. Biosci. Biotechnol. Biochem. 59:980–85 [Google Scholar]
  58. Kagabu S, Moriya K, Shibuya K, Hattori Y, Tsuboi S, Kozo S. 58.  1992. 1-(6-Halonicotinyl)-2-nitromethylene-imidazolidines as potential new insecticides. Biosci. Biotechnol. Biochem. 56:362–63 [Google Scholar]
  59. Kanne DB, Dick RA, Tomizawa M, Casida JE. 59.  2005. Neonicotinoid nitroguanidine insecticide metabolites: synthesis and nicotinic receptor potency of guanidines, aminoguanidines, and their derivatives. Chem. Res. Toxicol. 18:1479–84 [Google Scholar]
  60. Karatolos N, Williamson MS, Denholm I, Gorman K, ffrench-Constant RH, Bass C. 60.  2012. Over-expression of a cytochrome P450 is associated with resistance to pyriproxyfen in the greenhouse whitefly Trialeurodes vaporariorum. PLOS ONE 7:2e31077 [Google Scholar]
  61. Karunker I, Benting J, Lueke B, Ponge T, Nauen R. 61.  et al. 2008. Over-expression of cytochrome 450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci Hemiptera: Aleyrodidae). Insect Biochem. Mol. Biol. 38:634–44 [Google Scholar]
  62. Kayser H, Wellmann H, Lee C, Decock A, Gomes M, Cheek B. 62.  et al. 2007. Thiamethoxam: high-affinity binding and unusual mode of interference with other neonicotinoids at aphid membranes. In Synthesis and Chemistry of Agrochemicals VII JW Lyga, G Theodoridis 67–81 ACS Symp. Ser. 948 Washington, DC: Am. Chem. Soc. [Google Scholar]
  63. Kimura-Kuroda J, Komuta Y, Kuroda Y, Hayashi M, Kawano H. 63.  2012. Nicotine-like effects of the neonicotinoid insecticides acetamiprid and imidacloprid on cerebellar neurons from neonatal rats. PLOS ONE 7:2e32432 [Google Scholar]
  64. Kleier D, Holden I, Casida JE, Ruzo LO. 64.  1985. Novel photoreactions of an insecticidal nitromethylene heterocycle. J. Agric. Food Chem. 33:998–1000 [Google Scholar]
  65. Klein O. 65.  2001. Behavior of thiacloprid (YRC 2894) in plants and animals. Pflanzenschutz Nachr. Bayer 54:209–40 [Google Scholar]
  66. Kodaka K, Kinoshita K, Wakita T, Yamada E, Kawahara N, Yasui N. 66.  1998. MTI-446: a novel systemic insect control compound. Proc. Brighton Crop. Prot. Conf. Pests Dis.21–26 Alton, UK: Br. Crop Prot. Counc. [Google Scholar]
  67. Kollmeyer WD, Flattum RF, Foster JP, Powell JE, Schroeder ME, Soloway SB. 67.  1999. Discovery of the nitromethylene heterocycle insecticides. In Nicotinic Insecticides and the Nicotinic Acetylcholine Receptor I Yamamoto, JE Casida 71–89 Tokyo: Springer-Verlag [Google Scholar]
  68. Lansdell SJ, Millar NS. 68.  2000. The influence of nicotinic receptor subunit composition upon agonist, α-bungarotoxin and insecticide (imidacloprid) binding affinity. Neuropharmacology 39:671–79 [Google Scholar]
  69. Lansdell SJ, Millar NS. 69.  2002. D133, an atypical nicotinic acetylcholine receptor subunit from Drosophila: molecular cloning, heterologous expression and coassembly. J. Neurochem. 80:1009–18 [Google Scholar]
  70. Li X, Schuler MA, Berenbaum MR. 70.  2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52:231–53 [Google Scholar]
  71. Liu MY, Casida JE. 71.  1993. High affinity binding of [3H]imidacloprid in the insect acetylcholine receptor. Pestic. Biochem. Physiol. 46:40–46 [Google Scholar]
  72. Liu MY, Lanford J, Casida JE. 72.  1993. Relevance of [3H]imidacloprid binding site in house fly head acetylcholine receptor to insecticidal activity of 2-nitromethylene- and 2-nitroimino-imidazolidines. Pestic. Biochem. Physiol. 46:200–6 [Google Scholar]
  73. Liu Z, Williamson MS, Lansdell SJ, Denholm I, Han Z, Millar NS. 73.  2005. A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). PNAS 102:8420–25 [Google Scholar]
  74. Maienfisch P, Brandl F, Kobel W, Rindlisbacher A, Senn R. 74.  1999. CGA 293′343: a novel, broad-spectrum neonicotinoid insecticide. See Ref. 146 177–209
  75. Mao W, Schuler MA, Berenbaum MR. 75.  2011. CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). PNAS 108:12657–62 [Google Scholar]
  76. Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB. 76.  2001. Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol. Sci. 22:573–80 [Google Scholar]
  77. Matsuda K, Kanaoka S, Akamatsu M, Sattelle DB. 77.  2009. Diverse actions and target-site selectivity of neonicotinoids: structural insights. Mol. Pharmacol. 76:1–10 [Google Scholar]
  78. Millar NS, Denholm I. 78.  2007. Nicotinic acetylcholine receptors: targets for commercially important insecticides. Invert. Neurosci. 7:53–66 [Google Scholar]
  79. Moffat C, Buckland ST, Samson AJ, McArthur R, Pino VC. 79.  et al. 2016. Neonicotinoids target distinct nicotinic acetylcholine receptors and neurons, leading to differential risks to bumblebees. Sci. Rep. Sci. Rep. 6:24764 [Google Scholar]
  80. Mohamed F, Gawarammana I, Robertson TA, Roberts MS, Palangasinghe C. 80.  et al. 2009. Acute human self-poisoning with imidacloprid compound: a neonicotinoid insecticide. PLOS ONE 4:4e5127 [Google Scholar]
  81. Nauen R, Denholm I. 81.  2005. Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Arch. Insect Biochem. Physiol. 58:200–15 [Google Scholar]
  82. Nauen R, Ebbinghaus-Kintscher U, Elbert A, Jeschke P, Tietjen K. 82.  2001. Acetylcholine receptors as sites for developing neonicotinoid insecticides. Biochemical Sites of Insecticide Action and Resistance I Ishaaya 77–105 Berlin: Springer [Google Scholar]
  83. Nauen R, Ebbinghaus-Kintscher U, Salgado VL, Kaussmann M. 83.  2003. Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pestic. Biochem. Physiol. 76:55–69 [Google Scholar]
  84. Nauen R, Ebbinghaus-Kintscher U, Schmuck R. 84.  2001. Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Manag. Sci. 57:577–86 [Google Scholar]
  85. Nauen R, Jeschke P, Velten R, Beck ME, Ebbinghaus-Kintscher U. 85.  et al. 2014. Flupyradifurone: a brief profile of a new butenolide insecticide. Pest Manag. Sci. 71:850–62 [Google Scholar]
  86. Nauen R, Vontas J, Kaussmann M, Wolfe K. 86.  2013. Pymetrozine is hydroxylated by CYP6CM1, a cytochrome P450 conferring neonicotinoid resistance in Bemisia tabaci. Pest Manag. Sci. 69:457–61 [Google Scholar]
  87. Ohkawara Y, Akayama A, Matsuda K, Andersch W. 87.  2002. Clothianidin: a novel broad-spectrum neonicotinoid insecticide. The BCPC Conference: Pests and Diseases51–58 Farnham, UK: Br. Crop Prot. Counc. [Google Scholar]
  88. Orr N, Shaffner AJ, Watson GB. 88.  1997. Pharmacological characterization of an epibatidine binding site in the nerve cord of Periplaneta americana. Pestic. Biochem. Physiol. 58:183–92 [Google Scholar]
  89. Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM. 89.  2010. Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLOS Genet 6:6e1000999 [Google Scholar]
  90. Rose PH. 90.  2012. Nicotine and the neonicotinoids. Mammalian Toxicology of Insecticides TC Marrs 184–220 London, UK: RSC Publ. [Google Scholar]
  91. Schenker R, Tinembart O, Humbert-Droz E, Cavaliero T, Yerly B. 91.  2003. Comparative speed of kill between nitenpyram, fipronil, imidacloprid, selamectin and cythioate against adult Ctenocephalides fells (Bouche) on cats and dogs. Vet. Parasitol. 112:249–54 [Google Scholar]
  92. Schulz-Jander DA, Leimkuehler WM, Casida JE. 92.  2002. Neonicotinoid insecticides: reduction and cleavage of imidacloprid nitroimine substituent by liver microsomal and cytosolic enzymes. Chem. Res. Toxicol. 15:1158–65 [Google Scholar]
  93. Shao X, Fu H, Xu X, Xu X, Liu Z. 93.  et al. 2010. Divalent and oxabridged neonicotinoids constructed by dialdehydes and nitromethylene analogues of imidacloprid: design, synthesis, crystal structure, and insecticidal activities. J. Agric. Food Chem. 58:2696–702 [Google Scholar]
  94. Shao X, Liu Z, Xu X, Li Z, Qian X. 94.  2013. Overall status of neonicotinoid insecticides in China: production, application and innovation. J. Pestic. Sci. 38:1–9 [Google Scholar]
  95. Shao X, Swenson T, Casida JE. 95.  2013. Cycloxaprid insecticide: nicotinic acetylcholine receptor binding site and metabolism. J. Agric. Food. Chem. 61:7883–88 [Google Scholar]
  96. Shao X, Xia S, Durkin KA, Casida JE. 96.  2013. Insect nicotinic receptor interactions in vivo with neonicotinoid, organophosphorus, and methylcarbamate insecticides and a synergist. PNAS 110:17273–77 [Google Scholar]
  97. Sheets LP. 97.  2002. The neonicotinoid insecticides. Handbook of Neurotoxicology 1 EJ Massaro 79–87 Totowa, NJ: Humana [Google Scholar]
  98. Sheets LP, Li AA, Minnema DJ, Collier RH, Creek MR, Peffer RC. 98.  2015. A critical review of neonicotinoid insecticides for developmental neurotoxicity. Crit. Rev. Toxicol. 46:153–90 [Google Scholar]
  99. Shi X, Dick RA, Ford KA, Casida JE. 99.  2009. Enzymes and inhibitors in neonicotinoid insecticide metabolism. J. Agric. Food Chem. 57:4861–66 [Google Scholar]
  100. Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M. 100.  et al. 2014. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ. Sci. Pollut. Res. 22:5–34 [Google Scholar]
  101. Sixma TK, Smit AB. 101.  2003. Acetylcholine binding protein (AChBP): a secreted glial protein that provides a high-resolution model for extracellular domain of pentameric ligand-gated ion channels. Annu. Rev. Biophys. Biomol. Struct. 32:311–34 [Google Scholar]
  102. Skrinjaric-Spoljar M, Matthews HB, Engel JL, Casida JE. 102.  1971. Response of hepatic microsomal mixed-function oxidases to various types of insecticide chemical synergists administered to mice. Biochem. Pharmacol. 20:1607–18 [Google Scholar]
  103. Soloway SB, Henry AC, Kollmeyer WD, Padgett WM, Powell JE. 103.  et al. 1978. Nitromethylene heterocycles as insecticides. Pesticide and Venom Neurotoxicity DL Shankland, RM Hollingworth, T Smyth Jr 153–58 New York: Plenum [Google Scholar]
  104. Spande TF, Garraffo HM, Edwards MW, Yeh HJC, Pannell L, Daly JW. 104.  1992. Epibatidine: a novel (chloropyridyl) azabicycloheptane with potent analgesic activity from an Ecuadoran poison frog. J. Am. Chem. Soc. 114:3475–78 [Google Scholar]
  105. Sparks TC, DeBoer GJ, Wang NX, Hasler JM, Loso MR, Watson GB. 105.  2012. Differential metabolism of sulfoximine and neonicotinoid insecticides by Drosophila melanogaster monooxygenase CYP6G1. Pestic. Biochem. Physiol. 103:159–65 [Google Scholar]
  106. Sparks TC, Nauen R. 106.  2015. IRAC: Mode of Action classification and insecticide resistance management. Pest. Biochem. Physiol. 121:122–28 [Google Scholar]
  107. Sparks TC, Watson GB, Loso MR, Geng C, Babcock JM, Thomas JD. 107.  2013. Sulfoxaflor and the sulfoximine insecticides: chemistry, mode of action and basis for efficacy on resistant insects. Pestic. Biochem. Physiol. 107:1–7 [Google Scholar]
  108. Suchail S, Guez D, Belzunces LP. 108.  2001. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ. Toxicol. Chem. 20:2482–86 [Google Scholar]
  109. Swenson TL, Casida JE. 109.  2013. Aldehyde oxidase importance in vivo in xenobiotic metabolism: imidacloprid nitroreduction in mice. Toxicol. Sci. 133:22–28 [Google Scholar]
  110. Swenson TL, Casida JE. 110.  2013. Neonicotinoid formaldehyde generators: possible mechanism of mouse-specific hepatotoxicity/hepatocarcinogenicity of thiamethoxam. Toxicol. Lett. 216:139–45 [Google Scholar]
  111. Szczepaniec A, Raupp MJ, Parker RD, Kerns D, Eubanks MD. 111.  2013. Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants. PLOS ONE 8:5e62620 [Google Scholar]
  112. Taillebois E, Beloula A, Quinchard S, Jaubert-Possamai S, Daguin A. 112.  et al. 2014. Neonicotinoid binding, toxicity and expression of nicotinic acetylcholine receptor subunits in the aphid Acyrthosiphon pisum. PLOS ONE 9:5e96669 [Google Scholar]
  113. Talley TT, Harel M, Hibbs RH, Radio Z, Tomizawa M. 113.  et al. 2008. Atomic interactions of neonicotinoid agonists with AChBP: molecular recognition of the distinctive electronegative pharmacophore. PNAS 105:7606–11 [Google Scholar]
  114. Tamura S, Sakata K, Sakurai A. 114.  1978. Stemofoline as insecticide. Jpn. Patent No. JP 53127825
  115. Thany SH. 115.  2010. Insect Nicotinic Acetylcholine Receptors Adv. Exp. Med. Biol. 683 New York: Springer
  116. Thany SH. 116.  2010. Neonicotinoid insecticides: historical evolution and resistance mechanisms. Insect Nicotinic Acetylcholine Receptors SH Thany 75–84 Adv. Exp. Med. Biol. 683 New York: Springer [Google Scholar]
  117. Thielert W. 117.  2006. A unique product: the story of the imidacloprid stress shield. Pflanzenschutz Nachr. Bayer 59:73–86 [Google Scholar]
  118. Thompson HM, Fryday SL, Harkin S, Milner S. 118.  2014. Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops. Apidologie 45:545–53 [Google Scholar]
  119. Tomizawa M. 119.  2004. Neonicotinoids and derivatives: effects in mammalian cells and mice. J. Pestic. Sci. 29:177–83 [Google Scholar]
  120. Tomizawa M, Casida JE. 120.  1999. Minor structural changes in nicotinoid insecticides confer differential subtype selectivity for mammalian nicotinic acetylcholine receptors. Brit. J. Pharmacol. 127:115–22 [Google Scholar]
  121. Tomizawa M, Casida JE. 121.  2000. Imidacloprid, thiacloprid and their imine derivatives up-regulate the α4β2 nicotinic acetylcholine receptor in M10 cells. Toxicol. Appl. Pharmacol. 169:114–20 [Google Scholar]
  122. Tomizawa M, Casida JE. 122.  2001. Structure and diversity of insect nicotinic acetylcholine receptors. Pest Manag. Sci. 57:914–22 [Google Scholar]
  123. Tomizawa M, Casida JE. 123.  2002. Desnitro-imidacloprid activates the extracellular signal-regulated kinase cascade via the nicotinic receptor and intracellular calcium mobilization in N1E-115 cells. Toxicol. Appl. Pharmacol. 184:180–86 [Google Scholar]
  124. Tomizawa M, Casida JE. 124.  2003. Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annu. Rev. Entomol. 48:339–64 [Google Scholar]
  125. Tomizawa M, Casida JE. 125.  2005. Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu. Rev. Pharmacol. Toxicol. 45:247–68 [Google Scholar]
  126. Tomizawa M, Casida JE. 126.  2009. Molecular recognition of neonicotinoid insecticides: the determinants of life or death. Acc. Chem. Res. 42:260–69 [Google Scholar]
  127. Tomizawa M, Casida JE. 127.  2011. Unique neonicotinoid binding conformations conferring selective receptor interactions. J. Agric. Food Chem. 59:2825–28 [Google Scholar]
  128. Tomizawa M, Cowan A, Casida JE. 128.  2001. Analgesic and toxic effects of neonicotinoid insecticides in mice. Toxicol. Appl. Pharmacol. 177:77–83 [Google Scholar]
  129. Tomizawa M, Latli B, Casida JE. 129.  1999. Structure and function of insect nicotinic acetylcholine receptors studied with nicotinoid insecticide affinity probes. See Ref. 146 271–92
  130. Tomizawa M, Lee DL, Casida JE. 130.  2000. Neonicotinoid insecticides: molecular features conferring selectivity for insect versus mammalian nicotinic receptors. J. Agric. Food Chem. 48:6016–24 [Google Scholar]
  131. Tomizawa M, Maltby D, Talley TT, Durkin KA, Medzihradszky KF. 131.  et al. 2008. Atypical nicotinic agonist bound conformations conferring subtype selectivity. PNAS 105:1728–32 [Google Scholar]
  132. Tomizawa M, Millar NS, Casida JE. 132.  2005. Pharmacological profiles of recombinant and native insect nicotinic acetylcholine receptors. Insect Biochem. Mol. Biol. 35:1347–55 [Google Scholar]
  133. Tomizawa M, Talley TT, Maltby D, Durkin KA, Medzihradszky KF. 133.  et al. 2007. Mapping the elusive neonicotinoid binding site. PNAS 104:9075–80 [Google Scholar]
  134. Tomizawa M, Wen Z, Chin HL, Morimoto H, Kayser H, Casida JE. 134.  2001. Photoaffinity labeling of insect nicotinic acetylcholine receptors with a novel [3H]azidoneonicotinoid. J. Neurochem. 78:1359–66 [Google Scholar]
  135. Tomizawa M, Zhang N, Durkin KA, Olmstead MM, Casida JE. 135.  2003. The neonicotinoid electronegative pharmacophore plays the crucial role in the high affinity and selectivity for the Drosophila nicotinic receptor: an anomaly for the nicotinoid cation-π interaction model. Biochemistry 42:7819–27 [Google Scholar]
  136. Turner JA. 136.  2015. The Pesticide Manual Alton, UK: Br. Crop Prod. Counc. , 17th Ed..
  137. Lopez-Antia A, Feliu J, Camarero PR, Ortiz-Santaliestra ME, Mateo R. 137.  2016. Risk assessment of pesticide seed treatment for farmland birds using refined field data. J. Appl. Ecol. 53:1373–81 [Google Scholar]
  138. Ujvary I. 138.  1999. Nicotine and other insecticidal alkaloids. See Ref. 146 29–69
  139. Ušaj MM, Kaferle P, Toplak A, Trebše P, Petrovič U. 139.  2014. Determination of toxicity of neonicotinoids on the genome level using chemogenomics in yeast. Chemosphere 104:91–96 [Google Scholar]
  140. Watson GB, Loso MR, Babcock JM, Hasler JM, Letherer TJ. 140.  et al. 2011. Novel nicotinic action of the sulfoximine insecticide sulfoxaflor. Insect Biochem. Mol. Biol. 41:432–39 [Google Scholar]
  141. Wellmann H, Gomes M, Lee C, Kayser H. 141.  2004. Comparative analysis of neonicotinoid binding to insect membranes: II. An unusual high affinity site for [3H]thiamethoxam in Myzus persicae and Aphis craccivora. Pest Manag. Sci. 60:959–70 [Google Scholar]
  142. Wollweber D, Tietjen K. 142.  1999. Chloronicotinyl insecticides: a success of the new chemistry. See Ref. 146 109–26
  143. Yamada T, Takahashi H, Hatano R. 143.  1999. A novel insecticide, acetamiprid. See Ref. 146 149–76
  144. Yamamoto I. 144.  1965. Nicotinoids as insecticides. Advances in Pest Control Research RL Metcalf 6231–60 New York: Wiley [Google Scholar]
  145. Yamamoto I. 145.  1999. Nicotine to nicotinoids: 1962 to 1997. See Ref. 146 3–27
  146. Yamamoto I, Casida JE. 146.  1999. Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor Tokyo: Springer-Verlag
  147. Yasuda M, Kusajima M, Nakajima M, Akutsu K, Kudo T. 147.  et al. 2006. Thiadiazole carboxylic acid moiety of tiadinil, SV-03, induces systemic acquired resistance in tobacco without salicylic acid accumulation. J. Pestic. Sci. 31:329–34 [Google Scholar]
  148. Zhang A, Kaiser H, Maienfisch P, Casida JE. 148.  2000. Insect nicotinic acetylcholine receptor: conserved neonicotinoid specificity of [3H]imidacloprid binding site. J. Neurochem. 75:1294–303 [Google Scholar]
  149. Zhang N, Tomizawa M, Casida JE. 149.  2003. 5-Azidoepibatidine: an exceptionally potent photoaffinity ligand for neuronal α4β2 and α7 nicotinic acetylcholine receptors. Bioorg. Med. Chem. Lett. 13:525–27 [Google Scholar]
  150. Zhang N, Tomizawa M, Casida JE. 150.  2004. Drosophila nicotinic receptors: evidence for imidacloprid insecticide and α-bungarotoxin binding to distinct sites. Neurosci. Lett. 371:56–59 [Google Scholar]
  151. Zhu Y, Loso MR, Watson GB, Sparks TC, Rogers RB. 151.  et al. 2011. Discovery and characterization of sulfoxaflor, a novel insecticide targeting sap-feeding pests. J. Agric. Food Chem. 59:2950–57 [Google Scholar]
/content/journals/10.1146/annurev-ento-020117-043042
Loading
Neonicotinoids and Other Insect Nicotinic Receptor Competitive Modulators: Progress and Prospects
Annual Review of Entomology 63, 125 (2018); https://doi.org/10.1146/annurev-ento-020117-043042
/content/journals/10.1146/annurev-ento-020117-043042
/content/journals/10.1146/annurev-ento-020117-043042
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error