Nicotinic Acetylcholine Receptors as Spinosyn Targets for Insect Pest Management

Advances in Insect Physiology

Volumn 44, Issue , 2013, Pages 101-210

  Geng, Chaoxian ^a   Watson, Gerald B ^a   Sparks, Thomas C ^a  

^a DOW AGROSCIENCES LLC   (United States)

Author keywords

Insecticide resistance management; Integrated pest management; Natural product; Nicotinic acetylcholine receptor; Quantitative structure activity relationship; Spinosyns; Target site

Indexed keywords

EID: 84873500146     PISSN: 00652806     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394389-7.00003-X     Document Type: Chapter

References (166)

1. Abo Elghar G.E., Elbermawy Z.A., Yousef A.G., Abd Elhady H.K. Monitoring and characterization of insecticide-resistance in cotton leafworm, Spodoptera littoralis (Boisd) (Lepidoptera: Noctuidae). J. Asia-Pac. Entomol. 2005, 8:397-410.
2. Achaleke J., Martin T., Ghogomu R.T., Vaissayre M., Brevault T. Esterase-mediated resistance to pyrethroids in field populations of Helicoverpa armigera (Lepidoptera: Noctuidae) from Central Africa. Pest Manag. Sci. 2009, 65:1147-1154.
3. Ahmad M., Arif M.I. Resistance of Pakistani field populations of spotted bollworm Earias vittella (Lepidoptera: Noctuidae) to pyrethroid, organophosphorus and new chemical insecticides. Pest Manag. Sci. 2009, 65:433-439.
4. Ahmad M., Arif M.I., Ahmad Z. Susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to new chemistries in Pakistan. Crop Prot. 2003, 22:539-544.
5. Ahmad M., Hollingworth R.M., Wise J.C. Broad-spectrum insecticide resistance in obliquebanded leafroller Choristoneura rosaceana (Lepidoptera: Tortricidae) from Michigan. Pest Manag. Sci. 2002, 58:834-838.
6. Ahmad M., Sayyed A.H., Saleem M.A., Ahmad M. Evidence for field evolved resistance to newer insecticides in Spodoptera litura (Lepidoptera: Noctuidae) from Pakistan. Crop Prot. 2008, 27:1367-1372.
7. Ahrnad M., Sayyed A.H., Crickmore N., Saleem M.A. Genetics and mechanism of resistance to deltamethrin in a field population of Spodoptera litura (Lepidoptera: Noctuidae). Pest Manag. Sci. 2007, 63:1002-1010.
8. Attique M.N.R., Khaliq A., Sayyed A.H. Could resistance to insecticides in Plutella xylostella (Lep., Plutellidae) be overcome by insecticide mixtures?. J. Appl. Entomol. 2006, 130:122-127.
9. Baxter S.W., Chen M., Dawson A., Zhao J.Z., Vogel H., Shelton A.M., Heckel D.G., Jiggins C.D. Mis-spliced transcripts of nicotinic acetylcholine receptor alpha6 are associated with field evolved spinosad resistance in Plutella xylostella (L.). PLoS Genet. 2010, 6:e1000802.
10. Bertrand D., Ballivet M., Gomez M., Bertrand S., Phannavong B., Gundelfinger E.D. Physiological properties of neuronal nicotinic receptors reconstituted from the vertebrate beta 2 subunit and Drosophila alpha subunits. Eur. J. Neurosci. 1994, 6:869-875.
11. Bielza P. Insecticide resistance management strategies against the western flower thrips, Frankliniella occidentalis. Pest Manag. Sci. 2008, 64:1131-1138.
12. Bielza P., Quinto V., Contreras J., Torne M., Martin A., Espinosa P.J. Resistance to spinosad in the western flower thrips, Frankliniella occidentalis (Pergande), in greenhouses of south-eastern Spain. Pest Manag. Sci. 2007, 63:682-687.
13. Bielza P., Quinto V., Fernandez E., Gravalos C., Contreras J. Genetics of spinosad resistance in Frankliniella occidentalis (Thysanoptera: Thripidae). J. Econ. Entomol. 2007, 100:916-920.
14. Brejc K., Van Dijk W.J., Klaassen R.V., Schuurmans M., Van Der Oost J., Smit A.B., Sixma T.K. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 2001, 411:269-276.
15. Casida J.E., Tomizawa M. Insecticide interactions with gamma-aminobutyric acid and nicotinic receptors: predictive aspects of structural models. J. Pestic. Sci. 2008, 33:4-8.
16. Changeux J., Edelstein S.J. Nictinic Acetylcholine Receptors 2005, Odile Jacob Publishing Corporation, New York.
17. Chen X.L., Yuan L.Z., Du Y.Z., Zhang Y.J., Wang J.J. Cross-resistance and biochemical mechanisms of abamectin resistance in the western flower thrips, Frankliniella occidentalis. Pestic. Biochem. Physiol. 2011, 101:34-38.
18. Couso-Ferrer F., Arouri R., Beroiz B., Perera N., Cervera A., Navarro-Llopis V., Castanera P., Hernandez-Crespo P., Ortegoa F. Cross-resistance to insecticides in a malathion-resistant strain of Ceratitis capitata (Diptera: Tephritidae). J. Econ. Entomol. 2011, 104:1349-1356.
19. Creemer L.C., Kirst H.A., Paschal J.W., Worden T.V. Synthesis and insecticidal activity of spinosyn analogs functionally altered at the 2'-, 3'- and 4'-positions of the rhamnose moiety. J. Antibiot. 2000, 53:171-178.
20. Crouse G.D., Sparks T.C. Naturally derived materials as products and leads for insect control: the spinosyns. Rev. Toxicol. 1998, 2:133-146.
21. Crouse G.D., Sparks T.C., Deamicis C.V., Kirst H.A., Martynow J.G., Creemer L.C., Worden T.V., Anzeveno P.B. Chemistry and insecticidal activity of the spinosyns. Pesticide Chemistry and Bioscience: The Food-Environment Challenge 1999, 155-166. Royal Society of Chemistry, Cambridge, UK. G.T. Brooks, T.R. Roberts (Eds.).
22. Crouse G.D., Sparks T.C., Schoonover J., Gifford J., Dripps J., Bruce T., Larson L.L., Garlich J., Hatton C., Hill R.L., Worden T.V., Martynow J.G. Recent advances in the chemistry of spinosyns. Pest Manag. Sci. 2001, 57:177-185.
23. Darriet F., Duchon S., Hougard J.M. Spinosad: a new larvicide against insecticide-resistant mosquito larvae. J. Am. Mosq. Control Assoc. 2005, 21:495-496.
24. Darriet F., Marcombe S., Etienne M., Yebakima A., Agnew P., Yp-Tcha M.M., Corbel V. Field evaluation of pyriproxyfen and spinosad mixture for the control of insecticide resistant Aedes aegypti in Martinique (French West Indies). Parasit. Vectors 2010, 3:88.
25. Deamicis C.V., Dripps J.E., Hatton C.J., Karr L.L. Physical and biological properties of the spinosyns: Novel macrolide pest-control agents from fermentation. Phytochemicals for Pest Control 1997, 144-154. American Chemical Society, Washington, Symposium Series, no.658. P.A. Hedin, R.M. Hollingworth, E.P. Masler, J. Miyamoto, D.G. Thompson (Eds.).
26. Devillers J.E. Neural Networks in QSAR and Drug Design 1996, Academic Press, New York.
27. Dripps, J.E., Deamicis, C.V., Sparks, T.C., Crouse, G.D., 2008. AGRO 186-Spinosad to spinetoram: evolution of the spinosyns. Abstracts of Papers of the American Chemical Society, 236.
28. Dripps J.E., Boucher R.E., Chloridis A., Cleveland C.B., Deamicis C.V., Gomez L.E., Paroonagian D.L., Pavan L.A., Sparks T.C., Watson G.B. The spinosyn insecticides. Green Trends in Insect Control 2011, 163-212. Royal Society of Chemistry, Cambridge, UK. O. Lopez, J.G. Fernandez-Bolanos (Eds.).
29. Dunley J.E., Brunner J.F., Doerr M.D., Beers E.H. Resistance and cross-resistance in populations of the leafrollers, Choristoneura rosaceana and Pandemis pyrusana, in Washington apples. J. Insect Sci. 2006, 6:1-7.
30. Evans D.A., Black W.C. Total synthesis of (+)-A83543A [(+)-lepicidin A. J. Am. Chem. Soc. 1993, 115:4497-4513.
31. Eziah V.Y., Rose H.A., Clift A.D., Mansfield S. Susceptibility of four field populations of the diamondback moth Plutella xylostella L. (Lepidoptera: Yponomeutidae) to six insecticides in the Sydney region, New South Wales, Australia. Aust. J. Entomol. 2008, 47:355-360.
32. Ferguson J.S. Development and stability of insecticide resistance in the leafminer Liriomyza trifolii (Diptera: Agromyzidae) to cyromazine, abamectin, and spinosad. J. Econ. Entomol. 2004, 97:112-119.
33. Forsayeth J.R., Franco A., Rossi A.B., Lansman J.B., Hall Z.W. Expression of functional-mouse muscle acetylcholine-receptors in chinese hamster ovary cells. J. Neurosci. 1990, 10:2771-2779.
34. Gaisser S., Carletti I., Schell U., Graupner P.R., Sparks T.C., Martin C.J., Wilkinson B. Glycosylation engineering of spinosyn analogues containing an L-olivose moiety. Org. Biomol. Chem. 2009, 7:1705-1708.
35. Gao J.R., Deacutis J.M., Scott J.G. The nicotinic acetylcholine receptor subunits Mdalpha5 and Mdbeta3 on autosome 1 of Musca domestica are not involved in spinosad resistance. Insect Mol. Biol. 2007, 16:691-701.
36. Gill H.K., Dhawan A.K. Monitoring of insecticide resistance to Helicoverpa armigeria (Hubner) in cotton growing areas of Punjab. Pest. Res. J. 2006, 18:150-153.
37. Grauso M., Reenan R.A., Culetto E., Sattelle D.B. 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 2002, 160:1519-1533.
38. Guillen J., Bielza P. Thiamethoxam acts as a target-site synergist of spinosad in resistant strains of Frankliniella occidentalis. Pest Manag. Sci. 2012, 10.1002/ps.3372.
39. Hahn D.R., Gustafson G., Waldron C., Bullard B., Jackson J.D., Mitchell J. Butenyl-spinosyns, a natural example of genetic engineering of antibiotic biosynthetic genes. J. Ind. Microbiol. Biotechnol. 2006, 33:94-104.
40. Haider H., Ahmed S., Khan R.R. Determination of level of insecticide resistance in fruit fly, Bactrocera zonata (Saunders) (Diptera: Tephritidae) by bait bioassay. Int. J. Agric. Biol. 2011, 13:815-818.
41. Halevi S., Mckay J., Palfreyman M., Yassin L., Eshel M., Jorgensen E., Treinin M. The C-elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J. 2002, 21:1012-1020.
42. Herron G.A., James T.M. Monitoring insecticide resistance in Australian Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) detects fipronil and spinosad resistance. Aust. J. Entomol. 2005, 44:299-303.
43. Hsu J.C., Feng H.T. Development of resistance to spinosad in oriental fruit fly (Diptera: Tephritidae) in laboratory selection and cross-resistance. J. Econ. Entomol. 2006, 99:931-936.
44. Hsu J.C., Feng H.T., Wu W.J., Geib S.M., Mao C.H., Vontas J. Truncated transcripts of nicotinic acetylcholine subunit gene Bd alpha 6 are associated with spinosad resistance in Bactrocera dorsalis. Insect Biochem. Mol. Biol. 2012, 42:806-815.
45. Hussain R., Ashfaq M., Saleem M.A., Ahmed S. Toxicity of some insecticides with novel mode of action against malathion-resistant organophosphate-susceptible strains of Tribolium castaneum larvae. J. Agric. Biol. 2005, 7:768-772.
46. Hussain R., Ashfaq M., Saleem M.A. Biochemical abnormalities produced by spinosad in Tribolium castaneum adult beetles. Int. J. Agric. Biol. 2009, 11:241-244.
47. Ihara M., Matsuda K., Shimomura M., Sattelle D.B., Komai K. Super agonist actions of clothianidin and related compounds on the SAD beta 2 nicotinic acetylcholine receptor expressed in Xenopus laevis oocytes. Biosci. Biotechnol. Biochem. 2004, 68:761-763.
48. Ihara M., Okajima T., Yamashita A., Oda T., Hirata K., Nishiwaki H., Morimoto T., Akamatsu M., Ashikawa Y., Kuroda S., Mega R., Kuramitsu S., Sattelle D.B., Matsuda K. Crystal structures of Lymnaea stagnalis AChBP in complex with neonicotinoid insecticides imidacloprid and clothianidin. Invert. Neurosci. 2008, 8:71-81.
49. Ishtiaq M., Saleem M.A. Generating susceptible strain and resistance status of field populations of Spodoptera exigua (Lepidoptera: Noctuidae) against some conventional and new chemistry insecticides in Pakistan. J. Econ. Entomol. 2011, 104:1343-1348.
50. Ishtiaq M., Salem M.A., Razaq M. Monitoring of resistance in Spodoptera exigua (Lepidoptera: Noctuidae) from four districts of the Southern Punjab, Pakistan to four conventional and six new chemistry insecticides. Crop Prot. 2012, 33:13-20.
51. Jeschke P., Nauen R. Neonicotinoids-from zero to hero in insecticide chemistry. Pest Manag. Sci. 2008, 64:1084-1098.
52. Jeschke P., Nauen R. Nicotinic Acetylcholine Receptor Agonists: Target and Selectivity Aspects 2012, Wiley-VCH, Weinheim, Germany.
53. Jones A.K., Sattelle D.B. Diversity of insect nicotinic acetylcholine receptor subunits. Adv. Exp. Med. Biol. 2010, 683:25-43.
54. Kang C.Y., Wu G., Miyata T. Synergism of enzyme inhibitors and mechanisms of insecticide resistance in Bemisia tabaci (Gennadius) (Hom, Aleyrodidae). J. Appl. Entomol. 2006, 130:377-385.
55. Kao C.H., Cheng E.Y. Insecticide resistance in Plutella xylostella (L.) XI. Resistance to new introduced insecticides in Taiwan (1990-2001). J. Agric. Res. China 2001, 50:80-89.
56. Karlin A. Emerging structure of the nicotinic acetylcholine receptors. Nat. Rev. Neurosci. 2002, 3:102-114.
57. Khaliq A., Attique M.N.R., Sayyed A.H. Evidence for resistance to pyrethroids and organophosphates in Plutella xylostella (Lepidoptera: Plutellidae) from Pakistan. Bull. Entomol. Res. 2007, 97:191-200.
58. Kirst H.A. The spinosyn family of insecticides: realizing the potential of natural products research. J. Antibiot. (Tokyo) 2010, 63:101-111.
59. Kirst H.A., Michel K.H., Mynderase J.S., Chio E.H., Yao R.C., Nakasukasa W.M., Boeck L.D., Occlowitz J.L., Paschal J.W., Deeter J.B., Thompson G.D. Discovery, isolation and structure elucidation of a family of the structurally unique, fermentation derived tetracyclic macrolides. ACS Symposium Series 1992, Vol. 504:214-225. D.R. Baker, J.G. Fenyes, J.J. Steffens (Eds.).
60. Kranthi K.R., Kranthi S., Ali S., Banerjee S.K. Resistance to CrylAc delta-endotoxin of Bacillus thuringiensis' in a laboratory selected strain of Helicoverpa armigera (Hubner). Curr. Sci. 2000, 78:1001-1004.
61. Kristensen M., Jespersen J.B. Susceptibility of spinosad in Musca domestica (Diptera: Muscidae) field populations. J. Econ. Entomol. 2004, 97:1042-1048.
62. Kubinyi H. QSAR: Hansch Analysis and Related Approaches 1993, VCH, New York.
63. Lansdell S.J., Millar N.S. The influence of nicotinic receptor subunit composition upon agonist, alpha-bungarotoxin and insecticide (imidacloprid) binding affinity. Neuropharmacology 2000, 39:671-679.
64. Lansdell S.J., Collins T., Goodchild J., Millar N.S. The Drosophila nicotinic acetylcholine receptor subunits Dalpha5 and Dalpha7 form functional hemomeric and heteromeric channels. BMC Neurosci. 2012, 13:73. 10.1186/1471-2202-13-73.
65. Lewer P., Hahn D.R., Karr L.L., Duebelbeis D.O., Gilbert J.R., Crouse G.D., Worden T., Sparks T.C., Edwards P.M., Graupner P.R. Discovery of the butenyl-spinosyn insecticides: novel macrolides from the new bacterial strain Saccharopolyspora pogona. Bioorg. Med. Chem. 2009, 17:4185-4196.
66. Liu N.N., Yue X. Insecticide resistance and cross-resistance in the house fly (Diptera: Muscidae). J. Econ. Entomol. 2000, 93:1269-1275.
67. Liu H., Cupp E.W., Guo A.G., Liu N.N. Insecticide resistance in Alabama and Florida mosquito strains of Aedes albopictus. J. Med. Entomol. 2004, 41:946-952.
68. Liu H.Q., Cupp E.W., Micher K.M., Guo A.G., Liu N.N. Insecticide resistance and cross-resistance in Alabama and Florida strains of Culex quinquefaciatus. J. Med. Entomol. 2004, 41:408-413.
69. Liu S.S., Li Z.M., Liu Y.Q., Feng M.G., Tang Z.H. Promoting selection of resistance to spinosad in the parasitoid Cotesia plutellae by integrating resistance of hosts to the insecticide into the selection process. Biol. Control 2007, 41:246-255.
70. Liu, S., Li, M., Ou, X., Pei, H., Liu, L., Wang, X., 2010. Spinosad derivatives, their preparation method and application as insecticide. China Patent Application.
71. Loughner R.L., Warnock D.F., Cloyd R.A. Resistance of greenhouse, laboratory, and native populations of western flower thrips to spinosad. HortScience 2005, 40:146-149.
72. Magana C., Hernandez-Crespo P., Ortego F., Castanera P. Resistance to malathion in field populations of Ceratitis capitata. J. Econ. Entomol. 2007, 100:1836-1843.
73. Mao F.L.R., Gusukuma-Minuto L. Diamondback moth, Plutella xylostella (L.), resistance management in Hawaii 2004, N.M. Endersby, P.M. Ridland (Eds.).
74. Markussen M.D.K., Kristensen M. Spinosad resistance in female Musca domestica L. from a field-derived population. Pest Manag. Sci. 2012, 68:75-82.
75. Mascarenhas R.N., Boethel D.J. Responses of field-collected strains of soybean looper (Lepidoptera: Noctuidae) to selected insecticides using an artificial diet overlay bioassay. J. Econ. Entomol. 1997, 90:1117-1124.
76. Matsuda K., Buckingham S.D., Freeman J.C., Squire M.D., Baylis H.A., Sattelle D.B. Effects of the alpha subunit on imidacloprid sensitivity of recombinant nicotinic acetylcholine receptors. Br. J. Pharmacol. 1998, 123:518-524.
77. Mergott D.J., Frank S.A., Roush W.R. Total synthesis of (-)- spinosyn A. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:11955-11959.
78. Mertz F.P., Yao R.C. Saccharopolyspora spinosa sp. nov. isolated from soil collected in a sugar mill rum still. Int. J. Syst. Bacteriol. 1990, 40:34-39.
79. Meunier J.C., Boquet P., Changeux J.P., Fromageo P., Menez A., Olsen R.W. Studies on cholinergic receptor protein of electrophorus-electricus. 2. Some physical properties of cholinergic receptor protein from electrophorus-electricus revealed by a tritiated alpha-toxin from Naja nigricollis venom. Biochemistry 1972, 11:1200-1210.
80. Miles M., Lysandrou M. Evidence for negative cross resistance to insecticides in field collected Spodoptera littoralis (Boisd.) from Lebanon in laboratory bioassays. Meded. Rijksuniv. Gent Fak. Landbouwkd. Toegep. Biol. Wet. 2002, 67:665-669.
81. Millar N.S. A review of experimental techniques used for the heterologous expression of nicotinic acetylcholine receptors. Biochem. Pharmacol. 2009, 78:766-776.
82. Millar N.S., Denholm I. Nicotinic acetylcholine receptors: targets for commercially important insecticides. Invert. Neurosci. 2007, 7:53-66.
83. Miller R.J., White W.H., Davey R.B., George J.E., Perez De Leon A. Efficacy of spinosad against acaricide-resistant and -susceptible Rhipicephalus (Boophilus) microplus and acaricide-susceptible Amblyomma americanum and Dermacentor variabilis. J. Med. Entomol. 2011, 48:358-365.
84. Mishina M., Kurosaki T., Tobimatsu T., Morimoto Y., Noda M., Yamamoto T., Terao M., Lindstrom J., Takahashi T., Kuno M., Numa S. Expression of functional acetylcholine-receptor from cloned cDNAs. Nature 1984, 307:604-608.
85. Mota-Sanchez D., Hollingworth R.M., Grafius E.J., Moyer D.D. Resistance and cross-resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Pest Manag. Sci. 2006, 62:30-37.
86. Mota-Sanchez D., Wise J.C., Poppen R.V., Gut L.J., Hollingworth R.M. Resistance of codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), larvae in Michigan to insecticides with different modes of action and the impact on field residual activity. Pest Manag. Sci. 2008, 64:881-890.
87. Moulton J.K., Pepper D.A., Dennehy T.J. Beet armyworm (Spodoptera exigua) resistance to spinosad. Pest Manag. Sci. 2000, 56:842-848.
88. MSU Arthropod Pesticide Resistance Database 2012, Michigan State University. http://www.pesticideresistance.org.
89. Nasirian H., Ladonni H., Aboulhassani M., Limoee M. Susceptibility of field populations of Blattella germanica (Blattaria: Blattellidae) to spinosad. Pak. J. Biol. Sci. 2011, 14:862-868.
90. Nauen R., Elbert A., Mccaffery A., Slater R., Sparks T.C. IRAC: insecticide resistance, and mode of action classification of insecticides. Modern Crop Protection Compounds 2012, Wiley-VCH, Weinheim, Germany. 2 ed. W. Kramer, U. Schirmer, P. Jeschke, M. Witschel (Eds.).
91. Nauen R., Konanz S., Hirooka H., Nishimatsu T., Kodama H. Flubendiamide: a unique tool in resistance management tactics for pest Lapidoptera difficult to control. Pflanzenschutz Nachr. Bayer 2007, 60:247-262.
92. Noda M., Furutani Y., Takahashi H., Toyosato M., Tanabe T., Shimizu S., Kikyotani S., Kayano T., Hirose T., Inayama S., Numa S. Cloning and sequence-analysis of calf cDNA and human genomic DNA encoding alpha-subunit precursor of muscle acetylcholine-receptor. Nature 1983, 305:818-823.
93. Numa S., Noda M., Takahashi H., Tanabe T., Toyosato M., Furutani Y., Kikyotani S. Molecular-structure of the nicotinic acetylcholine-receptor. Cold Spring Harb. Symp. Quant. Biol. 1983, 48:57-69.
94. Orr N., Hasler J., Watson G.B., Mitchell J., Gustafson G., Gifford J., Geng C., Chouinard S.W., Cook K.D. Spinosad: from nature to green chemistry to novel mode of action 2006.
95. Orr N., Shaffner A.J., Richey K., Crouse G.D. Novel mode of action of spinosad: receptor binding studies demonstrating lack of interaction with known insecticidal target sites. Pestic. Biochem. Physiol. 2009, 95:1-5.
96. Osorio A., Martinez A.M., Schneider M.I., Diaz O., Corrales J.L., Aviles M.C., Smagghe G., Pineda S. Monitoring of beet armyworm resistance to spinosad and methoxyfenozide in Mexico. Pest Manag. Sci. 2008, 64:1001-1007.
97. Paquette L.A., Collado I., Purdie M. Total synthesis of spinosyn A. 2. Degradation studies involving the pure factor and its complete reconstitution. J. Am. Chem. Soc. 1998, 120:2553-2562.
98. Perry T., Mckenzie J.A., Batterham P. A Dalpha6 knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad. Insect Biochem. Mol. Biol. 2007, 37:184-188.
99. Perry T., Chan J.Q., Batterham P., Watson G.B., Geng C.X., Sparks T.C. Effects of mutations in Drosophila nicotinic acetylcholine receptor subunits on sensitivity to insecticides targeting nicotinic acetylcholine receptors. Pestic. Biochem. Physiol. 2012, 102:56-60.
100. Pollizzi S., Payne G. Laboratory evaluation of selected insecticides on field-collected populations on bollworm and tobacco budworm larvae 2004, 1832-1835.
101. Pu X., Yang Y.H., Wu S.W., Wu Y.D. Characterisation of abamectin resistance in a field-evolved multiresistant population of Plutella xylostella. Pest Manag. Sci. 2010, 66:371-378.
102. Puinean A.M., Lansdell S.J., Collins T., Bielza P., Millar N.S. A nicotinic acetylcholine receptor transmembrane point mutation (G275E) associated with resistance to spinosad in Frankliniella occidentalis. J. Neurochem. 2012, 10.1111/jnc.12029.
103. Raftery M.A., Hunkapiller M.W., Strader C.D., Hood L.E. Acetylcholine-receptor-complex of homologous subunits. Science 1980, 208:1454-1457.
104. Raymond Delpech V., Ihara M., Coddou C., Matsuda K., Sattelle D.B. Action of nereistoxin on recombinant neuronal nicotinic acetylcholine receptors expressed in Xenopus laevis oocytes. Invert. Neurosci. 2003, 5:29-35.
105. Reiter M.J., Prives J.M., Cowburn D.A., Karlin A. Affinity labeling of acetylcholine receptor in electroplax-electrophoretic separation in sodium dodecyl sulfate. Proc. Natl. Acad. Sci. U.S.A. 1972, 69:1168-1172.
106. Reyes M., Sauphanor B. Resistance monitoring in codling moth: a need for standardization. Pest Manag. Sci. 2008, 64:945-953.
107. Reyes M., Rocha K., Alarcon L., Siegwart M., Sauphanor B. Metabolic mechanisms involved in the resistance of field populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to spinosad. Pestic. Biochem. Physiol. 2012, 102:45-50.
108. Rinkevich F.D., Chen M., Shelton A.M., Scott J.G. Transcripts of the nicotinic acetylcholine receptor subunit gene Pxyl alpha 6 with premature stop codons are associated with spinosad resistance in diamondback moth, Plutella xylostella. Invert. Neurosci. 2010, 10:25-33.
109. Roe R.M., Young H.P., Iwasa T., Wyss C.F., Stumpf C.F., Sparks T.C., Watson G.B., Sheets J.J., Thompson G.D. Mechanism of resistance to spinosyn in the tobacco budworm, Heliothis virescens. Pestic. Biochem. Physiol. 2010, 96:8-13.
110. Salgado V.L. The modes of action of spinosad and other insect control products. Down to Earth 1997, 52:35-43.
111. Salgado V.L. Studies on the mode of action of spinosad: insect symptoms and physiological correlates. Pestic. Biochem. Physiol. 1998, 60:91-102.
112. Salgado V.L., Saar R. Desensitizing and non-desensitizing subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in cockroach neurons. J. Insect Physiol. 2004, 50:867-879.
113. Salgado V.L., Sparks T.C. The spinosyns: chemistry, biochemistry, mode of action, and resistance. Insect Control: Biological and Synthetic Agents 2010, 207-243. Academic Press, New York. L.I. Gilbert, S.S. Gill (Eds.).
114. Salgado V.L., Sheets J.J., Watson G.B., Schmidt A.L. Studies on the mode of action of spinosad: the internal effective concentration and the concentration dependence of neural excitation. Pestic. Biochem. Physiol. 1998, 60:103-110.
115. Salgado V.L., Watson G.B., Sheets J.J. Studies on the mode of action of spinosad, the active ingredient in Tracer insect control 1997, 1082-1084.
116. Salt D.W., Yildiz N., Livingstone D.J., Tinsley C.J. The use of artificial neural networks in QSAR. Pestic. Sci. 1992, 36:161-170.
117. Sattelle D.B. Invertebrate nicotinic acetylcholine receptors-targets for chemicals and drugs important in agriculture, veterinary medicine and human health. J. Pestic. Sci. 2009, 34:233-240.
118. Sattelle D.B., Jones A.K., Sattelle B.M., Matsuda K., Reenan R., Biggin P.C. Edit, cut and paste in the nicotinic acetylcholine receptor gene family of Drosophila melanogaster. Bioessays 2005, 27:366-376.
119. Sayyed A.H., Omar D., Wright D.J. Genetics of spinosad resistance in a multi-resistant field-selected population of Plutella xylostella. Pest Manag. Sci. 2004, 60:827-832.
120. Sayyed A.H., Ahmad M., Saleem M.A. Cross-resistance and genetics of resistance to indoxacarb in Spodoptera litura (Lepidoptera: Noctuidae). J. Econ. Entomol. 2008, 101:472-479.
121. Sayyed A.H., Wright D.J. Fipronil resistance in the diamondback moth (Lepidoptera: Plutellidae): inheritance and number of genes involved. J. Econ. Entomol. 2004, 97:2043-2050.
122. Sayyed A.H., Attique M.N.R., Khaliq A. Stability of field-selected resistance to insecticides in Plutella xylostella (Lep., Plutellidae) from Pakistan. J. Appl. Entomol. 2005, 129:542-547.
123. Sayyed A.H., Attique M.N.R., Khaliq A., Wright D.J. Inheritance of resistance and cross-resistance to deltamethrin in Plutella xylostella (Lepidoptera: Plutellidae) from Pakistan. Pest Manag. Sci. 2005, 61:636-642.
124. Scott J.G. Toxicity of spinosad to susceptible and resistant strains of house flies, Musca domestica. Pestic. Sci. 1998, 54:131-133.
125. Scott J.G. Unraveling the mystery of spinosad resistance in insects. J. Pestic. Sci. (Tokyo, Japan) 2008, 33:221-227.
126. Sheehan L.S., Lill R.E., Wilkinson B., Sheridan R.M., Vousden W.A., Kaja A.L., Crouse G.D., Gifford J., Graupner P.R., Karr L., Lewer P., Sparks T.C., Leadlay P.F., Waldron C., Martin C.J. Engineering of the spinosyn PKS: directing starter unit incorporation. J. Nat. Prod. 2006, 69:1702-1710.
127. Shelton A.M., Sances F.V., Hawley J., Tang J.D., Boune M., Jungers D., Collins H.L., Farias J. Assessment of insecticide resistance after the outbreak of diamondback moth (Lepidoptera: Plutellidae) in California in 1997. J. Econ. Entomol. 2000, 93:931-936.
128. Shi J., Zhang L., Gao X.W. Characterisation of spinosad resistance in the housefly Musca domestica (Diptera: Muscidae). Pest Manag. Sci. 2011, 67:335-340.
129. Shono T., Scott J.G. Spinosad resistance in the housefly, Musca domestica, is due to a recessive factor on autosome 1. Pestic. Biochem. Physiol. 2003, 75:1-7.
130. Shono T., Zhang L., Scott J.G. Indoxacarb resistance in the house fly, Musca domestica. Pestic. Biochem. Physiol. 2004, 80:106-112.
131. Sial A.A., Brunner J.F. Selection for resistance, reversion towards susceptibility and synergism of chlorantraniliprole and spinetoram in obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae). Pest Manag. Sci. 2012, 68:462-468.
132. Sial A.A., Brunner J.F., Doerr M.D. Susceptibility of Choristoneura rosaceana (Lepidoptera: Tortricidae) to two new reduced-risk insecticides. J. Econ. Entomol. 2010, 103:140-146.
133. Sial A.A., Brunner J.F., Garczynski S.F. Biochemical characterization of chlorantraniliprole and spinetoram resistance in laboratory-selected obliquebanded leafroller, Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae). Pestic. Biochem. Physiol. 2011, 99:274-279.
134. Silva G.A., Picanco M.C., Bacci L., Crespo A.L., Rosado J.F., Guedes R.N. Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag. Sci. 2011, 67:913-920.
135. Smirle M.J., Lowery D.T., Zurowski C.L. Susceptibility of leafrollers (Lepidoptera: Tortricidae) from organic and conventional orchards to azinphosmethyl, spinosad, and Bacillus thuringiensis. J. Econ. Entomol. 2003, 96:879-884.
136. Sparks T.C., Thompson G.D., Larson L.L., Kirst H.A., Jantz O.K., Worden T.V., Hertlein M.B., Busacca J.D. Biological characteristics of the spinosyns: a new class of naturally derived insect control agents 1995, National Cotton Council, Memphis, TN.
137. Sparks T.C., Thompson G.D., Kirst H.A., Hertlein M.B., Larson L.L., Worden T.V., Thibault S.T. Biological activity of the spinosyns, new fermentation derived insect control agents, on tobacco budworm (Lepidoptera : Noctuidae) larvae. J. Econ. Entomol. 1998, 91:1277-1283.
138. Sparks T.C., Thompson G.D., Kirst H.A., Hertlein M.B., Mynderse J.S., Turner J.R., Worden T.V. Fermentation-detived insect control agents: the spinosyns. Biopesticides: Use and Delivery 1999, 171-188. Humana Press, Totowa, New Jersey. R. Hall, J.J. Menn (Eds.).
139. Sparks T.C., Anzeveno P.B., Martynow J.G., Gifford J.M., Hertlein M.B., Worden T.V., Kirst H.A. The application of artificial neural networks to the identification of new spinosoids with improved biological activity toward larvae of Heliothis virescens. Pestic. Biochem. Physiol. 2000, 67:187-197.
140. Sparks T.C., Crouse G.D., Durst G. Natural products as insecticides: the biology, biochemistry and quantitative structure-activity relationships of spinosyns and spinosoids. Pest Manag. Sci. 2001, 57:896-905.
141. Sparks T.C., Crouse G.D., Dripps J.E., Anzeveno P., Martynow J., Deamicis C.V., Gifford J. Neural network-based QSAR and insecticide discovery: spinetoram. J. Comput. Aided Mol. Des. 2008, 22:393-401.
142. Sparks T.C., Dripps J.E., Watson G.B., Paroonagian D. Resistance and cross-resistance to the spinosyns - A review and analysis. Pestic. Biochem. Physiol 2012, 102:1-10.
143. Talley T.T., Harel M., Hibbs R.E., Radic Z., Tomizawa M., Casida J.E., Taylor P. Atomic interactions of neonicotinoid agonists with AChBP: molecular recognition of the distinctive electronegative pharmacophore. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:7606-7611.
144. Thompson G.D., Sparks T.C. Spinosad: a green natural product for insect control. Advancing Sustainability through Green Chemistry and Engineering 2002, 61-73. American Chemical Society, Washington, D.C. R.L. Lankey, P.T. Anastas (Eds.).
145. Thompson G.D., Dutton R., Sparks T.C. Spinosad - a case study: an example from a natural products discovery programme. Pest Manag. Sci. 2000, 56:696-702.
146. Tietze L.E., Brasche G., Grube A., Bohnke N., Stadler C. Synthesis of novel spinosyn A analogues by Pd-mediated transformations. Chemistry 2007, 13:8543-8563.
147. Tiwari S., Mann R.S., Rogers M.E., Stelinski L.L. Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Manag. Sci. 2011, 67:1258-1268.
148. Todeschini R., Consonni V. Handbook of Molecular Descriptors 2000, Wiley-VCH, New York.
149. Waldstein D.E., Reissig W.H. Synergism of tebufenozide in resistant and susceptible strains of obliquebanded leafroller (Lepidoptera: Tortricidae) and resistance to new insecticides. J. Econ. Entomol. 2000, 93:1768-1772.
150. Wang W., Mo J.C., Cheng J.A., Zhuang P.J., Tang Z.H. Selection and characterization of spinosad resistance in Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae). Pestic. Biochem. Physiol. 2006, 84:180-187.
151. Wang D., Qiu X.H., Ren X.X., Niu F., Wang K.Y. Resistance selection and biochemical characterization of spinosad resistance in Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). Pestic. Biochem. Physiol 2009, 95:90-94.
152. Wang G.L., Huang X.L., Wei H.Y., Fadamiro H.Y. Sublethal effects of larval exposure to indoxacarb on reproductive activities of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). Pestic. Biochem. Physiol. 2011, 101:227-231.
153. Wang Z.Y., Yan H.F., Yang Y.H., Wu Y.D. Biotype and insecticide resistance status of the whitefly Bemisia tabaci from China. Pest Manag. Sci. 2010, 66:1360-1366.
154. Watson G.B. Actions of insecticidal spinosyns on gamma-aminobutyric acid responses from small-diameter cockroach neurons. Pestic. Biochem. Physiol. 2001, 71:20-28.
155. Watson G.B., Chouinard S.W., Cook K.R., Geng C., Gifford J.M., Gustafson G.D., Hasler J.M., Larrinua I.M., Letherer T.J., Mitchell J.C., Pak W.L., Salgado V.L., Sparks T.C., Stilwell G.E. 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. 2010, 40:376-384.
156. Watson G.B., Loso M.R., Babcock J.M., Hasler J.M., Letherer T.J., Young C.D., Zhu Y., Casida J.E., Sparks T.C. Novel nicotinic action of the sulfoximine insecticide sulfoxaflor. Insect Biochem. Mol. Biol. 2011, 41:432-439.
157. Wei Y.P., Appel A.G., Moar W.J., Liu N.N. Pyrethroid resistance and cross-resistance in the German cockroach, Blattella germanica (L). Pest Manag. Sci. 2001, 57:1055-1059.
158. Weill C.L., Mcnamee M.G., Karlin A. Affinity-labeling of purified acetylcholine receptor from Torpedo californica. Biochem. Biophys. Res. Commun. 1974, 61:997-1003.
159. Whalon M.E., Mota-Snachez D., Hollingworth R.M. Analysis of global pesticide resistance in arthropods. Global Pesticide Resistance in Arthropods 2008, 5-31. CAB International, Cambridge, MA. M.E. Whalon, D. Mota-Snachez, R.M. Hollingworth (Eds.).
160. Yin Q., Qian L., Cao G., Han Z. Cross-resistance to several new pesticides exhibited by abamectin- and tebufenozide-resistant Plutella xylostella (L.). J. Nanjing Agric. Univ. 2010, 33:60-64.
161. Young H.P., Bailey W.D., Roe R.M., Iwasa T., Sparks T.C., Thompson G.D., Watson G.B. Mechanism of resistance and cross-resistance in a laboratory, spinosad-selected strain of the tobacco budworm and resistance in laboratory-selected cotton bollworms 2001, National Cotton Council, Memphis TN.
162. Zhang S.Y., Kono S., Murai T., Miyata T. Mechanisms of resistance to spinosad in the western flower thrip, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Insect Sci. 2008, 15:125-132.
163. Zhao J.Z., Li Y.X., Collins H.L., Gusukuma-Minuto L., Mau R.F.L., Thompson G.D., Shelton A.M. Monitoring and characterization of diamondback moth (Lepidoptera: Plutellidae) resistance to spinosad. J. Econ. Entomol. 2002, 95:430-436.
164. Zhao J.Z., Collins H.L., Li Y.X., Mau R.F.L., Thompson G.D., Hertlein M., Andaloro J.T., Boykin R., Shelton A.M. Monitoring of diamondback moth (Lepidoptera: Plutellidae) resistance to spinosad, indoxacarb, and emamectin benzoate. J. Econ. Entomol. 2006, 99:176-181.
165. Zhu Y.M., Loso M.R., Watson G.B., Sparks T.C., Rogers R.B., Huang J.X., Gerwick B.C., Babcock J.M., Kelley D., Hegde V.B., Nugent B.M., Renga J.M., Denholm I., Gorman K., Deboer G.J., Hasler J., Meade T., Thomas J.D. Discovery and characterization of sulfoxaflor, a novel insecticide targeting sap-feeding pests. J. Agric. Food Chem. 2011, 59:2950-2957.
166. Zhu J.X., Wu S.W., Yang Y.H., Wu Y.D. Laboratory selection and inheritance mode of resistance to spinosad in the diamondback moth, Plutella xylostella L. J. Nanjing Agric. Univ. 2007, 30:61-65.