The binding properties of cycloxaprid on insect native nAChRs partially explain the low cross‐resistance with imidacloprid in Nilaparvata lugens

Zhang, Yixi; Xu, Xiaoyong; Bao, Haibo; Shao, Xusheng; Li, Zhong; Liu, Zewen

doi:10.1002/ps.5108

The binding properties of cycloxaprid on insect native nAChRs partially explain the low cross‐resistance with imidacloprid in Nilaparvata lugens

Journal Article · Thu Aug 16 00:00:00 UTC 2018 · Pest Management Science

DOI:https://doi.org/10.1002/ps.5108· OSTI ID:1464842

Zhang, Yixi ^[1]; ^[2]; Bao, Haibo ^[1]; Shao, Xusheng ^[2]; Li, Zhong ^[2]; ^[1]

Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection Nanjing Agricultural University Nanjing China
Shanghai Key Laboratory of Chemical Biology, School of Pharmacy East China University of Science and Technology Shanghai China

Abstract BACKGROUND

Neonicotinoids, such as imidacloprid, are selective agonists of insect nicotinic acetylcholine receptors (nAChRs) used to control Nilaparvata lugens , a major rice insect pest. High imidacloprid resistance has been reported in N. lugens both in the laboratory and in the field. Cycloxaprid (CYC), an oxa‐bridged cis ‐nitromethylene neonicotinoid, showed high insecticidal activity against N. lugens and low cross‐resistance in imidacloprid‐resistant strains and field populations.

RESULTS

Binding studies demonstrated that imidacloprid has two binding sites with different affinities ( K _d = 3.18 ± 0.43 p m and 1.78 ± 0.19 n m ) in N. lugens nAChRs. CYC was poor at displacing [ ³ H]imidacloprid at its high‐affinity binding site ( K _i = 159.38 ± 20.43 n m ), but quite efficient at the low‐affinity binding site ( K _i = 1.27 ± 0.35 n m ). These data showed that CYC had overlapping binding sites with imidacloprid only at its low‐affinity binding site. Therefore, the low displacement ability of CYC against imidacloprid binding at its high‐affinity site could partially explain the low cross‐resistance of CYC in imidacloprid‐resistant populations.

CONCLUSION

The high insecticidal activity, low cross‐resistance and different binding properties on insect nAChRs of CYC show that it is a potential insecticide for the control of N. lugens and related insect pests, especially ones with high resistance to neonicotinoids. © 2018 Society of Chemical Industry

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

OSTI ID:: 1464842

Journal Information:: Pest Management Science, Journal Name: Pest Management Science Journal Issue: 1 Vol. 75; ISSN 1526-498X

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

References (27)

Resistance of insect pests to neonicotinoid insecticides: Current status and future prospects Nauen, Ralf; Denholm, Ian Archives of Insect Biochemistry and Physiology, Vol. 58, Issue 4 https://doi.org/10.1002/arch.20043	journal	January 2005
Edit, cut and paste in the nicotinic acetylcholine receptor gene family ofDrosophila melanogaster Sattelle, D. B.; Jones, A. K.; Sattelle, B. M. BioEssays, Vol. 27, Issue 4 https://doi.org/10.1002/bies.20207	journal	January 2005
Neuronal acetylcholine receptors in Drosophila: the ARD protein is a component of a high-affinity alpha-bungarotoxin binding complex. Schloss, P.; Hermans-Borgmeyer, I.; Betz, H. The EMBO Journal, Vol. 7, Issue 9 https://doi.org/10.1002/j.1460-2075.1988.tb03146.x	journal	September 1988
Selection for imidacloprid resistance inNilaparvata lugens: cross-resistance patterns and possible mechanisms Zewen, Liu; Zhaojun, Han; Yinchang, Wang Pest Management Science, Vol. 59, Issue 12 https://doi.org/10.1002/ps.768	journal	January 2003
[3H]Imidacloprid Labels High- and Low-Affinity Nicotinic Acetylcholine Receptor-like Binding Sites in the AphidMyzus persicae(Hemiptera: Aphididae) Lind, Robert J.; Clough, Martin S.; Reynolds, Stuart E. Pesticide Biochemistry and Physiology, Vol. 62, Issue 1 https://doi.org/10.1006/pest.1998.2364	journal	October 1998
Molecular evolution of the nicotinic acetylcholine receptor: An example of multigene family in excitable cells Le Novere, Nicolas; Changeux, Jean-Pierre Journal of Molecular Evolution, Vol. 40, Issue 2 https://doi.org/10.1007/BF00167110	journal	February 1995
Nicotinic acetylcholine receptors: targets for commercially important insecticides Millar, Neil S.; Denholm, Ian Invertebrate Neuroscience, Vol. 7, Issue 1 https://doi.org/10.1007/s10158-006-0040-0	journal	January 2007
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford, Marion M. Analytical Biochemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/0003-2697(76)90527-3	journal	May 1976
Molecular properties and functions of insect acetylcholine receptors Breer, Heinz; Sattelle, David B. Journal of Insect Physiology, Vol. 33, Issue 11 https://doi.org/10.1016/0022-1910(87)90025-4	journal	January 1987
Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors Matsuda, Kazuhiko; Buckingham, Steven D.; Kleier, Daniel Trends in Pharmacological Sciences, Vol. 22, Issue 11 https://doi.org/10.1016/S0165-6147(00)01820-4	journal	November 2001
Nonlinear regression using spreadsheets Bowen, W. Trends in Pharmacological Sciences, Vol. 16, Issue 12 https://doi.org/10.1016/S0165-6147(00)89091-4	journal	December 1995
Proinsecticide candidates N-(5-methyl-2-oxo-1,3-dioxol-4-yl)methyl derivatives of imidacloprid and 1-chlorothiazolylmethyl-2-nitroimino-imidazolidine Ohno, Ikuya; Hirata, Koichi; Ishida, Chiharu Bioorganic & Medicinal Chemistry Letters, Vol. 17, Issue 16 https://doi.org/10.1016/j.bmcl.2007.06.004	journal	August 2007
Crown-capped imidacloprid: A novel design and insecticidal activity Kagabu, Shinzo; Takagi, Masaru; Ohno, Ikuya Bioorganic & Medicinal Chemistry Letters, Vol. 19, Issue 11 https://doi.org/10.1016/j.bmcl.2009.04.053	journal	June 2009
Bis-neonicotinoid insecticides: Observed and predicted binding interactions with the nicotinic receptor Ohno, Ikuya; Tomizawaa, Motohiro; Durkin, Kathleen A. Bioorganic & Medicinal Chemistry Letters, Vol. 19, Issue 13 https://doi.org/10.1016/j.bmcl.2009.05.016	journal	July 2009
Pharmacological profiles of recombinant and native insect nicotinic acetylcholine receptors Tomizawa, Motohiro; Millar, Neil S.; Casida, John E. Insect Biochemistry and Molecular Biology, Vol. 35, Issue 12 https://doi.org/10.1016/j.ibmb.2005.08.006	journal	December 2005
Native subunit composition of two insect nicotinic receptor subtypes with differing affinities for the insecticide imidacloprid Li, Jian; Shao, Ying; Ding, Zhiping Insect Biochemistry and Molecular Biology, Vol. 40, Issue 1 https://doi.org/10.1016/j.ibmb.2009.12.003	journal	January 2010
Diversity of vertebrate nicotinic acetylcholine receptors Millar, Neil S.; Gotti, Cecilia Neuropharmacology, Vol. 56, Issue 1 https://doi.org/10.1016/j.neuropharm.2008.07.041	journal	January 2009
Cycloxaprid Insecticide: Nicotinic Acetylcholine Receptor Binding Site and Metabolism Shao, Xusheng; Swenson, Tami L.; Casida, John E. Journal of Agricultural and Food Chemistry, Vol. 61, Issue 33 https://doi.org/10.1021/jf4030695	journal	August 2013
Neonicotinoid Substituents Forming a Water Bridge at the Nicotinic Acetylcholine Receptor Ohno, Ikuya; Tomizawa, Motohiro; Durkin, Kathleen A. Journal of Agricultural and Food Chemistry, Vol. 57, Issue 6 https://doi.org/10.1021/jf803985r	journal	March 2009
Divalent and Oxabridged Neonicotinoids Constructed by Dialdehydes and Nitromethylene Analogues of Imidacloprid: Design, Synthesis, Crystal Structure, and Insecticidal Activities ^† Shao, Xusheng; Fu, Hua; Xu, Xiaoyong Journal of Agricultural and Food Chemistry, Vol. 58, Issue 5 https://doi.org/10.1021/jf902531y	journal	March 2010
Potency and Selectivity of Trifluoroacetylimino and Pyrazinoylimino Nicotinic Insecticides and Their Fit at a Unique Binding Site Niche Tomizawa, Motohiro; Kagabu, Shinzo; Ohno, Ikuya Journal of Medicinal Chemistry, Vol. 51, Issue 14 https://doi.org/10.1021/jm800191a	journal	July 2008
Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors Brejc, KatjuS̆a; van Dijk, Willem J.; Klaassen, Remco V. Nature, Vol. 411, Issue 6835 https://doi.org/10.1038/35077011	journal	May 2001
From The Cover: A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper) Liu, Z.; Williamson, M. S.; Lansdell, S. J. Proceedings of the National Academy of Sciences, Vol. 102, Issue 24 https://doi.org/10.1073/pnas.0502901102	journal	June 2005
Functional co-expression of two insect nicotinic receptor subunits (Nlα3 and Nlα8) reveals the effects of a resistance-associated mutation (Nlα3 ^Y151S ) on neonicotinoid insecticides Yixi, Zhang; Liu, Zewen; Han, Zhaojun Journal of Neurochemistry, Vol. 110, Issue 6 https://doi.org/10.1111/j.1471-4159.2009.06280.x	journal	September 2009
The Calculation of the Dosage-Mortality Curve Bliss, C. I. Annals of Applied Biology, Vol. 22, Issue 1 https://doi.org/10.1111/j.1744-7348.1935.tb07713.x	journal	February 1935
The cys-loop ligand-gated ion channel gene superfamily of the red flour beetle, Tribolium castaneum Jones, Andrew K.; Sattelle, David B. BMC Genomics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2164-8-327	journal	January 2007
Preparation of Alkylene-Tethered Acyclic Divalent Neonicotinoids and Their Insecticidal and Neuroblocking Activities for American Cockroach (Periplaneta americana L.) Kagabu, Shinzo; Itazu, Yuki; Nishimura, Keiichiro Journal of Pesticide Science, Vol. 29, Issue 1 https://doi.org/10.1584/jpestics.29.40	journal	January 2004

Similar Records

Atomic interactions of neonicotinoid agonists with AChBP: Molecular recognition of the distinctive electronegative pharmacophore

Journal Article · Mon Jul 28 04:00:00 UTC 2008 · Proc. Natl. Acad. Sci. USA · OSTI ID:1006671

Structural analysis and unique molecular recognition properties of a Bauhinia forficata lectin that inhibits cancer cell growth

Journal Article · Wed Feb 01 00:00:00 UTC 2017 · Federation of European Biochemical Societies (FEBS) Journal · OSTI ID:1400594

Crystal structure of a novel Kunitz type inhibitor, alocasin with anti‐ Aedes aegypti activity targeting midgut proteases

Journal Article · Tue Jul 03 00:00:00 UTC 2018 · Pest Management Science · OSTI ID:1458794

The binding properties of cycloxaprid on insect native nAChRs partially explain the low cross‐resistance with imidacloprid in Nilaparvata lugens

Citation Formats

References (27)

Similar Records

Related Subjects